Using a concurrent-chain schedule, we demonstrated the effect of absolute reinforcement (i.e., the magnitude effect) on choice behavior in rats. In general, animals' simultaneous choices conform to a relative reinforcement ratio between alternatives. However, studies in pigeons and rats have found that on a concurrent-chain schedule, the overall reinforcement ratio, or absolute amount, also influences choice. The effect of reinforcement amount has also been studied in inter-temporal choice situations, and this effect has been referred to as the magnitude effect. The magnitude effect has been observed in humans under various conditions, but little research has assessed it in animals (e.g., pigeons and rats). The present study confirmed the effect of reinforcement amount in rats during simultaneous and inter-temporal choice situations. We used a concurrent-chain procedure to examine the cause of the magnitude effect during inter-temporal choice. Our results suggest that rats can use differences in reinforcement amount as a contextual cue during choice, and the direction of the magnitude effect in rats might be similar to humans when using the present procedure. Furthermore, our results indicate that the magnitude effect was caused by the initial-link effect when the reinforcement amount was relatively small, while a loss aversion tendency was observed when the reinforcement amount changed within a session. The emergence of the initial-link effect and loss aversion suggests that rats make choices through cognitive processes predicted by prospect theory.
The Bengalese finch is the domesticated strain of the wild white-rumped munia. Bengalese finches have been domesticated and reproductively isolated for over 250 years from the wild strain. During this period, the courtship songs of the domesticated birds became phonologically and syntactically complex. In addition, psychological and physiological stress reactions to environmental and social factors diverged between the two strains. Based on our behavioral and histological studies, we consider the balance between the glucocorticoid- and mineralocorticoid receptors in song control nuclei and in the avian amygdala as to determine whether a bird can develop complex songs or rather has to devote the neural resources for the maintenance of stress reactions. We therefore suggest that phonological and syntactical complexity in Bengalese finch songs initially evolved because domestication freed them from species recognition and environmental stress, and then sexual selection increased the complexity. Neural and molecular studies also support the notion that Bengalese finches keep more song plasticity as adults. In conclusion, the present study suggests that domestication changed factors related with psychobiology of stress reactions and learning in finches.
Social learning in infancy is known to be facilitated by multimodal (e.g., visual, tactile, and verbal) cues provided by caregivers. In parallel with infants' development, recent research has revealed that maternal neural activity is altered through interaction with infants, for instance, to be sensitive to infant-directed speech (IDS). The present study investigated the effect of mother- infant multimodal interaction on maternal neural activity. Event-related potentials (ERPs) of mothers were compared to non-mothers during perception of tactile-related words primed by tactile cues. Only mothers showed ERP modulation when tactile cues were incongruent with the subsequent words, and only when the words were delivered with IDS prosody. Furthermore, the frequency of mothers' use of those words was correlated with the magnitude of ERP differentiation between congruent and incongruent stimuli presentations. These results suggest that mother-infant daily interactions enhance multimodal integration of the maternal brain in parenting contexts.
Birdsongs are acquired by imitating the sounds produced by conspecifics. Within a species, songs diverge by cultural transmission, but the range of species-specific features is restricted by innate constraints. Bengalese finches (Lonchura striata var. domestica) are a domesticated strain of the wild White-rumped munia (Lonchura striata). The songs of the domesticated strain have more tonal sounds and more variable sequences than those of the wild strain. We compared the features of songs that were produced by normal birds, isolation-reared birds, and cross-fostered birds in both White-rumped munias and Bengalese finches to identify differences in the genetic and environmental factors of their songs. Factor analyses were conducted based on 17 song measurements. We found that isolated songs differed from normal and cross-fostered songs, especially in unstable prosodic features. In addition, there were significant differences in sound property of mean frequency between the two strains regardless of the rearing conditions. Thus, innate constraints that partially determine birdsong phenotypes may be altered through domestication.
Music is an essential communication tool that can convey emotional information. Segmentation of a sound stream of music at event boundaries is necessary for identification and extraction of musical context and features. To investigate recognition of music termination structure, or cadence, we composed music sequences with two types of dominant-tonic termination structures and presented them to participants and analyzed their segment recognition and brain activities using EEG. The results revealed that a sense of termination was caused by listening to a tonic chord. Frontal area positivity at 380-480 ms was elicited by a dominant chord in cadence type I with a stronger sense of termination. These activities possibly reflected the expectation of the next tonic chord in the cadence.
Birdsong is an excellent research model for sound sequences consisting of complex structures. Neural and behavioral experiments have shown that auditory feedback is necessary for songbirds, especially Bengalese finches, to maintain the quality of the songs and that the nucleus HVC (used as proper name) and the anterior forebrain pathway (AFP) in the nervous system play key roles in this maintenance process. Neurons in the HVC and AFP exhibit higher spike rate to the bird's own song (BOS) than to other sound stimuli, such as temporally reversed song. To systematically evaluate what aspects of the BOS are captured by the different types of neural activities, both average spike rate and trial-to-trial spike timing variability in the BOS-selective neurons in the HVC and Area X (used as proper name), a gateway to the AFP from the HVC, were investigated following the presentation of auditory stimuli consisting of the BOS with systematic temporal inversion. Within-subjects analysis of the average spike rate and spike timing revealed that neural activity in the HVC and Area X is more sensitive to the local sound modulation of songs than to the global amplitude modulation. In addition, neurons in the HVC exhibit greater consistency of spike timing than neurons in Area X.
Language is a characteristic feature of human communication. Several familial language impairments have been identified, and candidate genes for language impairments already isolated. Studies comparing expression patterns of these genes in human brain are necessary to further understanding of these genes. However, it is difficult to examine gene expression in human brain. In this study, we used a non-human primate (common marmoset; Callithrix jacchus) as a biological model of the human brain to investigate expression patterns of human speech- and reading-related genes. Expression patterns of speech disorder- (FoxP2, FoxP1, CNTNAP2, and CMIP) and dyslexia- (ROBO1, DCDC2, and KIAA0319) related genes were analyzed. We found the genes displayed overlapping expression patterns in the ocular, auditory, and motor systems. Our results enhance understanding of the molecular mechanisms underlying language impairments.
The cadherin superfamily is a large (now more than 100 proteins) protein family originally identified as cell adhesion molecules. Each cadherin shows distinct expression patterns in the nervous system, and their expressions are both spatially and temporally regulated and diverse among different species. Mounting evidence has suggested that cadherins play multiple roles in neural development and functions. Recently, using songbirds and mice, the potential role of cadherins in vocal behavior has been demonstrated. Here, we will briefly introduce general function of cadherins, and analyze the potential involvement of cadherins in vocal behaviors and their evolution.
The purpose of the present study was to determine whether and how single finger tapping in synchrony with sound sequences contributed to the auditory processing of them. The participants learned two unfamiliar sound sequences via different methods. In the tapping condition, they learned an auditory sequence while they tapped in synchrony with each sound onset. In the no tapping condition, they learned another sequence while they kept pressing a key until the sequence ended. After these learning sessions, we presented the two melodies again and recorded event-related potentials (ERPs). During the ERP recordings, 10% of the tones within each melody deviated from the original tones. An analysis of the grand average ERPs showed that deviant stimuli elicited a significant P300 in the tapping but not in the no-tapping condition. In addition, the significance of the P300 effect in the tapping condition increased as the participants showed highly synchronized tapping behavior during the learning sessions. These results indicated that single finger tapping promoted the conscious detection and evaluation of deviants within the learned sequences. The effect was related to individuals' musical ability to coordinate their finger movements along with external auditory events.
How human language arose is a mystery in the evolution of Homo sapiens. Miyagawa et al. (2013) put forward a proposal, which we will call the Integration Hypothesis of human language evolution, that holds that human language is composed of two components, E for expressive, and L for lexical. Each component has an antecedent in nature: E as found, for example, in birdsong, and L in, for example, the alarm calls of monkeys. E and L integrated uniquely in humans to give rise to language. A challenge to the Integration Hypothesis is that while these non-human systems are finite-state in nature, human language is known to require characterization by a non-finite state grammar. Our claim is that E and L, taken separately, are in fact finite-state; when a grammatical process crosses the boundary between E and L, it gives rise to the non-finite state character of human language. We provide empirical evidence for the Integration Hypothesis by showing that certain processes found in contemporary languages that have been characterized as non-finite state in nature can in fact be shown to be finite-state. We also speculate on how human language actually arose in evolution through the lens of the Integration Hypothesis.
Why do we listen to sad music? We seek to answer this question using a psychological approach. It is possible to distinguish perceived emotions from those that are experienced. Therefore, we hypothesized that, although sad music is perceived as sad, listeners actually feel (experience) pleasant emotions concurrent with sadness. This hypothesis was supported, which led us to question whether sadness in the context of art is truly an unpleasant emotion. While experiencing sadness may be unpleasant, it may also be somewhat pleasant when experienced in the context of art, for example, when listening to sad music. We consider musically evoked emotion vicarious, as we are not threatened when we experience it, in the way that we can be during the course of experiencing emotion in daily life. When we listen to sad music, we experience vicarious sadness. In this review, we propose two sides to sadness by suggesting vicarious emotion.
Birdsong provides a unique model for understanding the behavioral and neural bases underlying complex sequential behaviors. However, birdsong analyses require laborious effort to make the data quantitatively analyzable. The previous attempts had succeeded to provide some reduction of human efforts involved in birdsong segment classification. The present study was aimed to further reduce human efforts while increasing classification performance. In the current proposal, a linear-kernel support vector machine was employed to minimize the amount of human-generated label samples for reliable element classification in birdsong, and to enable the classifier to handle highly-dimensional acoustic features while avoiding the over-fitting problem. Bengalese finch's songs in which distinct elements (i.e., syllables) were aligned in a complex sequential pattern were used as a representative test case in the neuroscientific research field. Three evaluations were performed to test (1) algorithm validity and accuracy with exploring appropriate classifier settings, (2) capability to provide accuracy with reducing amount of instruction dataset, and (3) capability in classifying large dataset with minimized manual labeling. The results from the evaluation (1) showed that the algorithm is 99.5% reliable in song syllables classification. This accuracy was indeed maintained in evaluation (2), even when the instruction data classified by human were reduced to one-minute excerpt (corresponding to 300-400 syllables) for classifying two-minute excerpt. The reliability remained comparable, 98.7% accuracy, when a large target dataset of whole day recordings (?30,000 syllables) was used. Use of a linear-kernel support vector machine showed sufficient accuracies with minimized manually generated instruction data in bird song element classification. The methodology proposed would help reducing laborious processes in birdsong analysis without sacrificing reliability, and therefore can help accelerating behavior and studies using songbirds.
The decision making behaviors of humans and animals adapt and then satisfy an "operant matching law" in certain type of tasks. This was first pointed out by Herrnstein in his foraging experiments on pigeons. The matching law has been one landmark for elucidating the underlying processes of decision making and its learning in the brain. An interesting question is whether decisions are made deterministically or probabilistically. Conventional learning models of the matching law are based on the latter idea; they assume that subjects learn choice probabilities of respective alternatives and decide stochastically with the probabilities. However, it is unknown whether the matching law can be accounted for by a deterministic strategy or not. To answer this question, we propose several deterministic Bayesian decision making models that have certain incorrect beliefs about an environment. We claim that a simple model produces behavior satisfying the matching law in static settings of a foraging task but not in dynamic settings. We found that the model that has a belief that the environment is volatile works well in the dynamic foraging task and exhibits undermatching, which is a slight deviation from the matching law observed in many experiments. This model also demonstrates the double-exponential reward history dependency of a choice and a heavier-tailed run-length distribution, as has recently been reported in experiments on monkeys.
Vocal learning, a critical component of speech acquisition, is a rare trait in animals. Songbirds are a well-established animal model in vocal learning research; male birds acquire novel vocal patterns and have a well-developed song system in the brain. Although this system is unique to songbirds, anatomical and physiological studies have reported similarities between the song system and the thalamo-cortico-basal ganglia circuit that is conserved among reptiles, birds, and mammals. Here, we focused on the similarity of the neural response between these two systems while animals were engaging in operant tasks. Neurons in the basal ganglia of vertebrates are activated in response to food rewards and reward predictions in behavioral tasks. A striatal nucleus in the avian song system, Area X, is necessary for vocal learning and is considered specialized for singing. We found that the spiking activity of singing-related Area X neurons was modulated by food rewards and reward signals in an operant task. As previous studies showed that Area X is not critical for general cognitive tasks, the role of Area X in general learning might be limited and vestigial. However, our results provide a new viewpoint to investigate the independence of the vocal learning system from neural systems involved in other cognitive tasks.
We examined differences in the fear response between Bengalese finches and their wild ancestor, the white-backed munia, to explore the evolutionary mechanisms of behavioural changes due to domestication. The Bengalese finch (Lonchura striata var. domestica) was domesticated from the wild-living white-backed munia (L. striata) approximately 250 years ago. A previous study indicated that Bengalese finches sing much more complex songs than white-backed munias. We hypothesised that Bengalese finches are likely able to allocate more resources to reproduction in exchange for reduced survival effort. We measured tonic immobility (TI) reactions as a response to physical restraint to evaluate fearfulness related to coping with predation. The results showed that Bengalese finches exhibited decreased TI responses compared with white-backed munias. TI responses were unaffected by sex, body weight or growth conditions. These differences suggest that the fearfulness in Bengalese finches has been reduced by selective pressure during domestication. Bengalese finches may have been able to increase the investment of energy in reproduction in exchange for reduced costs of predation and coping necessary to survive in the wild; these behavioural changes may have been a major target of domestication effects in this species.
In songbirds, a specialized neural system, the song system, is responsible for acquisition and expression of species-specific vocal patterns. We report evidence for differential gene expression between wild and domesticated strains having different learned vocal phenotypes. A domesticated strain of the wild white-rumped munia, the Bengalese finch, has a distinct song pattern with a more complicated syntax than the wild strain. We identified differential androgen receptor (AR) expression in basal ganglia nucleus Area X GABAergic neurons between the two strains, and within different domesticated populations. Differences in AR expression were correlated with the mean coefficient of variation of the inter-syllable duration in the two strains. Differential AR expression in Area X was observed before the initiation of singing, suggesting that inherited and/or early developmental mechanisms may affect expression within and between strains. However, there were no distinct differences in regions upstream of the AR start codon among all the birds in the study. In contrast, an epigenetic modification, DNA methylation state in regions upstream of AR in Area X, was observed to differ between strains and within domesticated populations. These results provide insight into the molecular basis of behavioral evolution through the regulation of hormone-related genes and demonstrate the potential association between epigenetic modifications and behavioral phenotype regulation.
Human language, as well as birdsong, relies on the ability to arrange vocal elements in new sequences. However, little is known about the ontogenetic origin of this capacity. Here we track the development of vocal combinatorial capacity in three species of vocal learners, combining an experimental approach in zebra finches (Taeniopygia guttata) with an analysis of natural development of vocal transitions in Bengalese finches (Lonchura striata domestica) and pre-lingual human infants. We find a common, stepwise pattern of acquiring vocal transitions across species. In our first study, juvenile zebra finches were trained to perform one song and then the training target was altered, prompting the birds to swap syllable order, or insert a new syllable into a string. All birds solved these permutation tasks in a series of steps, gradually approximating the target sequence by acquiring new pairwise syllable transitions, sometimes too slowly to accomplish the task fully. Similarly, in the more complex songs of Bengalese finches, branching points and bidirectional transitions in song syntax were acquired in a stepwise fashion, starting from a more restrictive set of vocal transitions. The babbling of pre-lingual human infants showed a similar pattern: instead of a single developmental shift from reduplicated to variegated babbling (that is, from repetitive to diverse sequences), we observed multiple shifts, where each new syllable type slowly acquired a diversity of pairwise transitions, asynchronously over development. Collectively, these results point to a common generative process that is conserved across species, suggesting that the long-noted gap between perceptual versus motor combinatorial capabilities in human infants may arise partly from the challenges in constructing new pairwise vocal transitions.
An object that includes occluded parts is sometimes perceived as a complete image and this phenomenon is known as amodal or visual completion. A sign stimulus is a minimum set of information that elicits a behavior, but this notion raises questions about whether animals ever engage in the behavior when they cannot see the occluded sign stimulus, but they can visually complete it. Male Bengalese finches engage in courtship behavior toward video images of female finches. We conducted three experiments with Bengalese finches to show both sign stimuli and visual completion function in an ecological context. We used three types of visual images recorded from female finches as stimuli: the head, the body, and the whole. Results showed that male Bengalese finches showed courtship behavior toward the head-occluded stimuli whereas they did not toward the headless body image. The results imply that the males completed this occluded sign stimulus through the process of visual completion. Exposure to a sign stimulus combined with the process of visual completion may operate cooperatively to facilitate adaptive responses under conditions of limited information.
Newborns admitted to the neonatal intensive care unit are repeatedly subjected to painful or stressful procedures; therefore, objective assessment of their pain is essential. An increasing number of scales for neonatal pain assessment have been developed, many of which are based on physiological and behavioral factors. Recently, salivary biomarkers have been used to assess stress in adults and older infants. This study aimed to determine whether salivary biomarkers can be useful objective indices for assessing newborn pain.
Involuntary microsaccades and voluntary saccades reflect human brain activities during attention and cognitive tasks. Our eye movements can also betray our emotional state. However, the effects of attention to emotion on microsaccadic activity remain unknown. The present study was conducted in healthy volunteers to investigate the effects of devoting attention to exogenous emotional stimuli on microsaccadic response, with change in pupil size as an index of sympathetic nervous system activity. Event-related responses to unpleasant images significantly inhibited the rate of microsaccade appearance and altered pupil size (Experiment 1). Additionally, microsaccadic responses to covert orienting of attention to emotional stimuli appeared significantly in the anti-direction to a target, with a fast reaction time (Experiment 2). Therefore, we concluded that attentional shifts induced by exogenous emotional stimuli can modulate microsaccadic activities. Future studies of the interaction between miniature eye movements and emotion may be beneficial in the assessment of pathophysiological responses in mental disorders.
The rodent granular retrosplenial cortex (GRS) has dense connections with the hippocampal formation and anterior thalamic nuclei. However, functional connectivity within the GRS has not been examined. The aim of this study is to investigate the intracortical circuit of the GRS, including late-spiking (LS) neurons in layers 2 and 3. We conducted extracellular recordings of field potentials from slice preparations of the rat GRS following stimulations of layer 1a and white matter (WM). Current source-density analysis demonstrated that layer 1a stimulation first evoked synaptic current sinks in layer 1 followed by sinks in layers 2-4. These sinks were extinguished by glutamate antagonists. WM stimulation induced long latency synaptic current sinks in layers 2-4 and 6. Thus, signal inputs from the thalamus to layer 1a might be transmitted to layer 5, presumably delayed by LS neurons in layers 2 and 3. According to previous anatomical studies, current sinks in layers 2-4 following WM stimulation were attributed to the horizontal connections of LS neurons. Based on these results we suggest that GRS microcircuitry possibly enables layer 5 neurons to integrate time-delayed thalamic inputs with direct inputs from other brain regions.
Preterm infants are at increased risk of language-related problems later in life; however, few studies have examined the effects of preterm birth on cerebral responses to speech at very early developmental stages. This study examined cerebral activation and functional connectivity in response to infant-directed speech (IDS) and adult-directed speech (ADS) in full-term neonates and preterm infants at term-equivalent age using 94-channel near-infrared spectroscopy. The results showed that compared with ADS, IDS increased activity in larger brain areas such as the bilateral frontotemporal, temporal, and temporoparietal regions, both in full-term and preterm infants. Preterm infants exhibited decreased activity in response to speech stimuli in the right temporal region compared with full-term infants, although the significance was low. Moreover, preterm infants exhibited increased interhemispheric connectivity compared with full-term controls, especially in the temporal and temporoparietal regions. These differences suggest that preterm infants may follow different developmental trajectories from those born at term owing to differences in intrauterine and extrauterine development.
Protocadherin-11 is a cell adhesion molecule of the cadherin superfamily. Since, only in humans, its paralog is found on the Y chromosome, it is expected that protocadherin-11X/Y plays some role in human brain evolution or sex differences. Recently, a genetic mutation of protocadherin-11X/Y was reported to be associated with a language development disorder. Here, we compared the expression of protocadherin-11 X-linked in developing postnatal brains of mouse (rodent) and common marmoset (non-human primate) to explore its possible involvement in mammalian brain evolution. We also investigated its expression in the Bengalese finch (songbird) to explore a possible function in animal vocalization and human language faculties.
We propose a novel account for the emergence of human language syntax. Like many evolutionary innovations, language arose from the adventitious combination of two pre-existing, simpler systems that had been evolved for other functional tasks. The first system, Type E(xpression), is found in birdsong, where the same song marks territory, mating availability, and similar "expressive" functions. The second system, Type L(exical), has been suggestively found in non-human primate calls and in honeybee waggle dances, where it demarcates predicates with one or more "arguments," such as combinations of calls in monkeys or compass headings set to sun position in honeybees. We show that human language syntax is composed of two layers that parallel these two independently evolved systems: an "E" layer resembling the Type E system of birdsong and an "L" layer providing words. The existence of the "E" and "L" layers can be confirmed using standard linguistic methodology. Each layer, E and L, when considered separately, is characterizable as a finite state system, as observed in several non-human species. When the two systems are put together they interact, yielding the unbounded, non-finite state, hierarchical structure that serves as the hallmark of full-fledged human language syntax. In this way, we account for the appearance of a novel function, language, within a conventional Darwinian framework, along with its apparently unique emergence in a single species.
The songs of Bengalese finches (Lonchura striata var. domestica) have complex syntax and provide an opportunity to investigate how complex sequential behaviour emerges via the evolutionary process. In this study, we suggest that a simple mechanism, i.e. many-to-one mapping from internal states onto syllables, may underlie the emergence of apparent complex syllable sequences that have higher order history dependencies. We analysed the songs of Bengalese finches and of their wild ancestor, the white-rumped munia (L. striata), whose songs are more stereotypical and simpler compared with those of Bengalese finches. The many-to-one mapping mechanism sufficiently accounted for the differences in the complexity of song syllable sequences of these two strains.
OUR UNDERSTANDING OF FACIAL EMOTION PERCEPTION HAS BEEN DOMINATED BY TWO SEEMINGLY OPPOSING THEORIES: the categorical and dimensional theories. However, we have recently demonstrated that hybrid processing involving both categorical and dimensional perception can be induced in an implicit manner (Fujimura etal., 2012). The underlying neural mechanisms of this hybrid processing remain unknown. In this study, we tested the hypothesis that separate neural loci might intrinsically encode categorical and dimensional processing functions that serve as a basis for hybrid processing. We used functional magnetic resonance imaging to measure neural correlates while subjects passively viewed emotional faces and performed tasks that were unrelated to facial emotion processing. Activity in the right fusiform face area (FFA) increased in response to psychologically obvious emotions and decreased in response to ambiguous expressions, demonstrating the role of the FFA in categorical processing. The amygdala, insula and medial prefrontal cortex exhibited evidence of dimensional (linear) processing that correlated with physical changes in the emotional face stimuli. The occipital face area and superior temporal sulcus did not respond to these changes in the presented stimuli. Our results indicated that distinct neural loci process the physical and psychological aspects of facial emotion perception in a region-specific and implicit manner.
A Noh mask, worn by expert actors during performance on the Japanese traditional Noh drama, conveys various emotional expressions despite its fixed physical properties. How does the mask change its expressions? Shadows change subtly during the actual Noh drama, which plays a key role in creating elusive artistic enchantment. We here describe evidence from two experiments regarding how attached shadows of the Noh masks influence the observers recognition of the emotional expressions.
We perceive our surrounding environment by using different sense organs. However, it is not clear how the brain estimates information from our surroundings from the multisensory stimuli it receives. While Bayesian inference provides a normative account of the computational principle at work in the brain, it does not provide information on how the nervous system actually implements the computation. To provide an insight into how the neural dynamics are related to multisensory integration, we constructed a recurrent network model that can implement computations related to multisensory integration. Our model not only extracts information from noisy neural activity patterns, it also estimates a causal structure; i.e., it can infer whether the different stimuli came from the same source or different sources. We show that our model can reproduce the results of psychophysical experiments on spatial unity and localization bias which indicate that a shift occurs in the perceived position of a stimulus through the effect of another simultaneous stimulus. The experimental data have been reproduced in previous studies using Bayesian models. By comparing the Bayesian model and our neural network model, we investigated how the Bayesian prior is represented in neural circuits.
The abilities of animals and humans to extract rules from sound sequences have previously been compared using observation of spontaneous responses and conditioning techniques. However, the results were inconsistently interpreted across studies possibly due to methodological and/or species differences. Therefore, we examined the strategies for discrimination of sound sequences in Bengalese finches and humans using the same protocol. Birds were trained on a GO/NOGO task to discriminate between two categories of sound stimulus generated based on an "AAB" or "ABB" rule. The sound elements used were taken from a variety of male (M) and female (F) calls, such that the sequences could be represented as MMF and MFF. In test sessions, FFM and FMM sequences, which were never presented in the training sessions but conformed to the rule, were presented as probe stimuli. The results suggested two discriminative strategies were being applied: (1) memorizing sound patterns of either GO or NOGO stimuli and generating the appropriate responses for only those sounds; and (2) using the repeated element as a cue. There was no evidence that the birds successfully extracted the abstract rule (i.e., AAB and ABB); MMF-GO subjects did not produce a GO response for FFM and vice versa. Next we examined whether those strategies were also applicable for human participants on the same task. The results and questionnaires revealed that participants extracted the abstract rule, and most of them employed it to discriminate the sequences. This strategy was never observed in bird subjects, although some participants used strategies similar to the birds when responding to the probe stimuli. Our results showed that the human participants applied the abstract rule in the task even without instruction but Bengalese finches did not, thereby reconfirming that humans have to extract abstract rules from sound sequences that is distinct from non-human animals.
Medical advancements in neonatology have significantly increased the number of high-risk preterm survivors. However, recent long-term follow-up studies have suggested that preterm infants are at risk for behavioral, educational, and emotional problems. Although clear relationships have been demonstrated between preterm infants and developmental problems during childhood and adolescence, less is known about the early indications of these problems. Recently, numerous studies on resting-state functional connectivity (RSFC) have demonstrated temporal correlations of activity between spatially remote cortical regions not only in healthy adults but also in neuropathological disorders and early childhood development. In order to compare RSFC of the cerebral cortex between preterm infants at term-equivalent ages and full-term neonates without any anatomical abnormality risk during natural sleep, we used an optical topography system, which is a recently developed extension of near-infrared spectroscopy. We clarified the presence of RSFC in both preterm infants and full-term neonates and showed differences between these groups. The principal differences were that on comparison of RSFC between the bilateral temporal regions, and bilateral parietal regions, RSFC was enhanced in preterm infants compared with full-term neonates; whereas on comparison of RSFC between the left temporal and left parietal regions, RSFC was enhanced in full-term neonates compared with preterm infants. We also demonstrated a difference between the groups in developmental changes of RSFC related to postmenstrual age. Most importantly, these findings suggested that preterm infants and full-term neonates follow different developmental trajectories during the perinatal period because of differences in perinatal experiences and physiological and structural development.
In general, sad music is thought to cause us to experience sadness, which is considered an unpleasant emotion. As a result, the question arises as to why we listen to sad music if it evokes sadness. One possible answer to this question is that we may actually feel positive emotions when we listen to sad music. This suggestion may appear to be counterintuitive; however, in this study, by dividing musical emotion into perceived emotion and felt emotion, we investigated this potential emotional response to music. We hypothesized that felt and perceived emotion may not actually coincide in this respect: sad music would be perceived as sad, but the experience of listening to sad music would evoke positive emotions. A total of 44 participants listened to musical excerpts and provided data on perceived and felt emotions by rating 62 descriptive words or phrases related to emotions on a scale that ranged from 0 (not at all) to 4 (very much). The results revealed that the sad music was perceived to be more tragic, whereas the actual experiences of the participants listening to the sad music induced them to feel more romantic, more blithe, and less tragic emotions than they actually perceived with respect to the same music. Thus, the participants experienced ambivalent emotions when they listened to the sad music. After considering the possible reasons that listeners were induced to experience emotional ambivalence by the sad music, we concluded that the formulation of a new model would be essential for examining the emotions induced by music and that this new model must entertain the possibility that what we experience when listening to music is vicarious emotion.
Infant shyness, in which infants react shyly to adult strangers, presents during the third quarter of the first year. Researchers claim that shy children over the age of three years are experiencing approach-avoidance conflicts. Counter-intuitively, shy children do not avoid the eyes when scanning faces; rather, they spend more time looking at the eye region than non-shy children do. It is currently unknown whether young infants show this conflicted shyness and its corresponding characteristic pattern of face scanning. Here, using infant behavioral questionnaires and an eye-tracking system, we found that highly shy infants had high scores for both approach and fear temperaments (i.e., approach-avoidance conflict) and that they showed longer dwell times in the eye regions than less shy infants during their initial fixations to facial stimuli. This initial hypersensitivity to the eyes was independent of whether the viewed faces were of their mothers or strangers. Moreover, highly shy infants preferred strangers with an averted gaze and face to strangers with a directed gaze and face. This initial scanning of the eye region and the overall preference for averted gaze faces were not explained solely by the infants age or temperament (i.e., approach or fear). We suggest that infant shyness involves a conflict in temperament between the desire to approach and the fear of strangers, and this conflict is the psychological mechanism underlying infants characteristic behavior in face scanning.
A series of emotional events successively occur in temporal context. The present study investigated how physiological and psychological responses are modulated by emotional context. Skin conductance response (SCR), heart rate, corrugator activity, zygomatic activity, and subjective feelings during emotional picture viewing were measured. To create an emotional context, a unpleasant or pleasant picture was preceded by three types of pictures, i.e., unpleasant, pleasant, and neutral pictures, resulting in six pairings. The results showed that viewing an unpleasant picture attenuated pleasant feelings induced by the following pleasant picture. On the other hand, preceding pleasant pictures decreased SCR to the following pictures. The effects of contextual modulation on emotional responses might be due to the informative function of pre-existing feelings; unpleasant feelings signal a threatening environment, whereas pleasant feelings signal a benign environment. With respect to facial muscle activities, viewing a pleasant picture decreased corrugator activity in response to the preceding picture. These findings suggest several types of contextual modulation effects on psychological, autonomic, and somatic responses to emotional stimuli.
The ability to detect emotional change in the environment is essential for adaptive behavior. The current study investigated whether event-related potentials (ERPs) can reflect emotional change in a visual sequence. To assess pre-attentive processing, we examined visual mismatch negativity (vMMN): the negative potentials elicited by a deviant (infrequent) stimulus embedded in a sequence of standard (frequent) stimuli. Participants in two experiments pre-attentively viewed visual sequences of Japanese kanji with different emotional connotations while ERPs were recorded. The visual sequence in Experiment 1 consisted of neutral standards and two types of emotional deviants with a strong and weak intensity. Although the results indicated that strongly emotional deviants elicited more occipital negativity than neutral standards, it was unclear whether these negativities were derived from emotional deviation in the sequence or from the emotional significance of the deviants themselves. In Experiment 2, the two identical emotional deviants were presented against different emotional standards. One type of deviants was emotionally incongruent with the standard and the other type of deviants was emotionally congruent with the standard. The results indicated that occipital negativities elicited by deviants resulted from perceptual changes in a visual sequence at a latency of 100-200 ms and from emotional changes at latencies of 200-260 ms. Contrary to the results of the ERP experiment, reaction times to deviants showed no effect of emotional context; negative stimuli were consistently detected more rapidly than were positive stimuli. Taken together, the results suggest that brain signals can reflect emotional change in a temporal context.
The paper describes an application of machine learning techniques to identify expiratory and inspiration phases from the audio recording of human baby cries. Crying episodes were recorded from 14 infants, spanning four vocalization contexts in their first 12 months of age; recordings from three individuals were annotated manually to identify expiratory and inspiratory sounds and used as training examples to segment automatically the recordings of the other 11 individuals. The proposed algorithm uses a hidden Markov model architecture, in which state likelihoods are estimated either with Gaussian mixture models or by converting the classification decisions of a support vector machine. The algorithm yields up to 95% classification precision (86% average), and its ability generalizes over different babies, different ages, and vocalization contexts. The technique offers an opportunity to quantify expiration duration, count the crying rate, and other time-related characteristics of baby crying for screening, diagnosis, and research purposes over large populations of infants.
Mineralocorticoid receptor is the receptor for corticosteroids such as corticosterone or aldosterone. Previously, we found that mineralocorticoid receptor was highly expressed in song nuclei of a songbird, Bengalese finch (Lonchura striata var. domestica). Here, to examine the relationship between mineralocorticoid receptor expression and avian vocal learning, we analyzed mineralocorticoid receptor expression in the developing brain of another vocal learner, budgerigar (Melopsittacus undulatus) and non-vocal learners, quail (Coturnix japonica) and ring dove (Streptopelia capicola). Mineralocorticoid receptor showed vocal control area-related expressions in budgerigars as Bengalese finches, whereas no such mineralocorticoid receptor expressions were seen in the telencephalon of non-vocal learners. Thus, these results suggest the possibility that mineralocorticoid receptor plays a role in vocal development of parrots as songbirds and that the acquisition of mineralocorticoid receptor expression is involved in the evolution of avian vocal learning.
We investigated whether categorical perception and dimensional perception can co-occur while decoding emotional facial expressions. In Experiment 1, facial continua with endpoints consisting of four basic emotions (i.e., happiness-fear and anger-disgust) were created by a morphing technique. Participants rated each facial stimulus using a categorical strategy and a dimensional strategy. The results show that the happiness-fear continuum was divided into two clusters based on valence, even when using the dimensional strategy. Moreover, the faces were arrayed in order of the physical changes within each cluster. In Experiment 2, we found a category boundary within other continua (i.e., surprise-sadness and excitement-disgust) with regard to the arousal and valence dimensions. These findings indicate that categorical perception and dimensional perception co-occurred when emotional facial expressions were rated using a dimensional strategy, suggesting a hybrid theory of categorical and dimensional accounts.
The emotional outcome of a choice affects subsequent decision making. While the relationship between decision making and emotion has attracted attention, studies on emotion and decision making have been independently developed. In this study, we investigated how the emotional valence of pictures, which was stochastically contingent on participants choices, influenced subsequent decision making. In contrast to traditional value-based decision-making studies that used money or food as a reward, the "reward value" of the decision outcome, which guided the update of value for each choice, is unknown beforehand. To estimate the reward value of emotional pictures from participants choice data, we used reinforcement learning models that have successfully been used in previous studies for modeling value-based decision making. Consequently, we found that the estimated reward value was asymmetric between positive and negative pictures. The negative reward value of negative pictures (relative to neutral pictures) was larger in magnitude than the positive reward value of positive pictures. This asymmetry was not observed in valence for an individual picture, which was rated by the participants regarding the emotion experienced upon viewing it. These results suggest that there may be a difference between experienced emotion and the effect of the experienced emotion on subsequent behavior. Our experimental and computational paradigm provides a novel way for quantifying how and what aspects of emotional events affect human behavior. The present study is a first step toward relating a large amount of knowledge in emotion science and in taking computational approaches to value-based decision making.
Cadherins, cell adhesion molecules widely expressed in the nervous system, are thought to be involved in synapse formation and function. To explore the role of cadherins in neuronal activity, we performed electrophysiological and morphological analyses of rat hippocampal cultured neurons overexpressing type-II cadherins, such as cadherin-6B and cadherin-7. We found that cadherin-6B increased but cadherin-7 decreased the number of protrusions of dendritic spines, and affected the frequency of miniature excitatory postsynaptic currents. Our results suggest that type-II cadherins may modulate neural activity by regulating neuronal morphology.
Bird species with vocal learning possess a projection from the telencephalic nucleus to the nucleus nervi hypoglossi, pars tracheosyringealis (XIIts) in the medulla, where a final common pathway that controls the vocal organ, i.e., the synrinx, originates. The anatomical basis of this projection has not been well investigated in one species of songbird, the Bengalese finch (Lonchura striata var. domestica). The present study used anterograde and retrograde tracing experiments to examine and describe this projection in Bengalese finches. Following iontophoretic injections of biotinylated dextran amine into the telencephalic nucleus robustus arcopallialis (RA), we detected anterograde-labeled terminations in the XIIts. In addition, labeled terminals were seen in other vocal-respiratory-related nuclei, such as the dorsomedial nucleus of the nucleus intercollicularis, nucleus infraolivaris superior, nucleus of the rostral ventrolateral medulla, nucleus parambigualis, nucleus ambiguous, and nucleus retroambigualis. Furthermore, following injections into the XIIts, we detected retrograde-labeled cell bodies scattered throughout the ipsilateral RA. The present results revealed that the direct projections of the RA to the XIIts in male Bengalese finches are similar to those in other songbirds with vocal learning abilities.
The ability to statistically segment a continuous auditory stream is one of the most important preparations for initiating language learning. Such ability is available to human infants at 8 months of age, as shown by a behavioral measurement. However, behavioral study alone cannot determine how early this ability is available. A recent study using measurements of event-related potential (ERP) revealed that neonates are able to detect statistical boundaries within auditory streams of speech syllables. Extending this line of research will allow us to better understand the cognitive preparation for language acquisition that is available to neonates. The aim of the present study was to examine the domain-generality of such statistical segmentation. Neonates were presented with nonlinguistic tone sequences composed of four tritone units, each consisting of three semitones extracted from one octave, for two 5-minute sessions. Only the first tone of each unit evoked a significant positivity in the frontal area during the second session, but not in the first session. This result suggests that the general ability to distinguish units in an auditory stream by statistical information is activated at birth and is probably innately prepared in humans.
Generation of the motor patterns of emotional sounds in mammals occurs in the periaqueductal gray matter of the midbrain and is not directly controlled by the cortex. The medial frontal cortex indirectly controls vocalizations, based on the recognition of social context. We examined whether the medial frontal cortex was responsible for antiphonal vocalization, or turn-taking, in naked mole-rats. In normal turn-taking, naked mole-rats vocalize more frequently to dominant individuals than to subordinate ones. Bilateral lesions of the medial frontal cortex disrupted differentiation of call rates to the stimulus animals, which had varied social relationships to the subject. However, medial frontal cortex lesions did not affect either the acoustic properties of the vocalizations or the timing of the vocal exchanges. This suggests that the medial frontal cortex may be involved in social cognition or decision making during turn-taking, while other regions of the brain regulate when animals vocalize and the vocalizations themselves.
Neural networks can learn flexible input-output associations by changing their synaptic weights. The representational performance and learning dynamics of neural networks are intensively studied in several fields. Neural networks face the "credit assignment problem" in situations in which only incomplete performance evaluations are available. The credit assignment problem is that a network should assign credit or blame for its behaviors according to the contribution to the network performance. In reinforcement learning, a scalar evaluation signal is delivered to a network. The two main types of credit assignment problems in reinforcement learning are structural and temporal, that is, which parameters of the network (structural) and which past network activities (temporal) are related to an evaluation signal given from an environment. In this study, we apply statistical mechanical analysis to the learning processes in a simple neural network model to clarify the effects of two kinds of credit assignments and their interactions. Our model is based on node perturbation learning with eligibility trace. Node perturbation is a stochastic gradient learning method that can solve structural credit assignment problems by introducing a perturbation into the system output. The eligibility trace preserves the past network activities with a temporal credit to deal with the delay of an instruction signal. We show that both credit assignment effects mutually interact and the optimal time constant of the eligibility trace varies not only for the evaluation delay but also the network size.
Birds use various vocalizations to communicate with one another, and some are acquired through learning. So far, three families of birds (songbirds, parrots, and hummingbirds) have been identified as having vocal learning ability. Previously, we found that cadherins, a large family of cell-adhesion molecules, show vocal control-area-related expression in a songbird, the Bengalese finch. To investigate the molecular basis of evolution in avian species, we conducted comparative analysis of cadherin expressions in the vocal and other neural systems among vocal learners (Bengalese finch and budgerigar) and a non-learner (quail and ring dove). The gene expression analysis revealed that cadherin expressions were more variable in vocal and auditory areas compared to vocally unrelated areas such as the visual areas among these species. Thus, it appears that such diverse cadherin expressions might have been related to generating species diversity in vocal behavior during the evolution of avian vocal learning.
The cerebral cortex is an indispensable region for higher cognitive function that is remarkably diverse among mammalian species. Although previous research has shown that the cortical area map in the mammalian cerebral cortex is formed by innate and activity-dependent mechanisms, it remains unknown how these mechanisms contribute to the evolution and diversification of the functional cortical areas in various species. The naked mole rat (Heterocephalus glaber) is a subterranean, eusocial rodent. Physiological and anatomical studies have revealed that the visual system is regressed and the somatosensory system is enlarged. To examine whether species differences in cortical area development are caused by intrinsic factors or environmental factors, we performed comparative gene expression analysis of neonatal naked mole rat and mouse brains. The expression domain of cadherin-6, a somatosensory marker, was expanded caudally and shifted dorsally in the cortex, whereas the expression domain of cadherin-8, a visual marker, was reduced caudally in the neonatal naked mole rat cortex. The expression domain of cadherin-8 was also reduced in other visual areas, such as the lateral geniculate nucleus and superior colliculus. Immunohistochemical analysis of thalamocortical fibers further suggested that somatosensory input did not affect cortical gene expression in the neonatal naked mole rat brain. These results suggest that the development of the somatosensory system and the regression of the visual system in the naked mole rat cortex are due to intrinsic genetic mechanisms as well as sensory input-dependent mechanisms. Intrinsic genetic mechanisms thus appear to contribute to species diversity in cortical area formation.
How the brain learns and generates temporal sequences is a fundamental issue in neuroscience. The production of birdsongs, a process which involves complex learned sequences, provides researchers with an excellent biological model for this topic. The Bengalese finch in particular learns a highly complex song with syntactical structure. The nucleus HVC (HVC), a premotor nucleus within the avian song system, plays a key role in generating the temporal structures of their songs. From lesion studies, the nucleus interfacialis (NIf) projecting to the HVC is considered one of the essential regions that contribute to the complexity of their songs. However, the types of interaction between the HVC and the NIf that can produce complex syntactical songs remain unclear. In order to investigate the function of interactions between the HVC and NIf, we have proposed a neural network model based on previous biological evidence. The HVC is modeled by a recurrent neural network (RNN) that learns to generate temporal patterns of songs. The NIf is modeled as a mechanism that provides auditory feedback to the HVC and generates random noise that feeds into the HVC. The model showed that complex syntactical songs can be replicated by simple interactions between deterministic dynamics of the RNN and random noise. In the current study, the plausibility of the model is tested by the comparison between the changes in the songs of actual birds induced by pharmacological inhibition of the NIf and the changes in the songs produced by the model resulting from modification of parameters representing NIf functions. The efficacy of the model demonstrates that the changes of songs induced by pharmacological inhibition of the NIf can be interpreted as a trade-off between the effects of noise and the effects of feedback on the dynamics of the RNN of the HVC. These facts suggest that the current model provides a convincing hypothesis for the functional role of NIf-HVC interaction.
Complex sequencing rules observed in birdsongs provide an opportunity to investigate the neural mechanism for generating complex sequential behaviors. To relate the findings from studying birdsongs to other sequential behaviors such as human speech and musical performance, it is crucial to characterize the statistical properties of the sequencing rules in birdsongs. However, the properties of the sequencing rules in birdsongs have not yet been fully addressed. In this study, we investigate the statistical properties of the complex birdsong of the Bengalese finch (Lonchura striata var. domestica). Based on manual-annotated syllable labeles, we first show that there are significant higher-order context dependencies in Bengalese finch songs, that is, which syllable appears next depends on more than one previous syllable. We then analyze acoustic features of the song and show that higher-order context dependencies can be explained using first-order hidden state transition dynamics with redundant hidden states. This model corresponds to hidden Markov models (HMMs), well known statistical models with a large range of application for time series modeling. The song annotation with these models with first-order hidden state dynamics agreed well with manual annotation, the score was comparable to that of a second-order HMM, and surpassed the zeroth-order model (the Gaussian mixture model; GMM), which does not use context information. Our results imply that the hierarchical representation with hidden state dynamics may underlie the neural implementation for generating complex behavioral sequences with higher-order dependencies.
The Bengalese finch (Lonchura striata var. domestica) is a species of songbird. Males sing courtship songs with complex note-to-note transition rules, while females discriminate these songs when choosing their mate. The present study uses serial reaction time (RT) to examine the characteristics of the Bengalese finches sequential behaviours beyond song production. The birds were trained to produce the sequence with an "A-B-A" structure. After the RT to each key position was determined to be stable, we tested the acquisition of the trained sequential response by presenting novel and random three-term sequences (random test). We also examined whether they could abstract the embedded rule in the trained sequence and apply it to the novel test sequence (abstract test). Additionally, we examined rule abstraction through example training by increasing the number of examples in baseline training from 1 to 5. When considered as (gender) groups, training with 5 examples resulted in no statistically significant differences in the abstract tests, while statistically significant differences were observed in the random tests, suggesting that the male birds learned the trained sequences and transferred the abstract structure they had learned during the training trials. Individual data indicated that males, as opposed to females, were likely to learn the motor pattern of the sequence. The results are consistent with observations that males learn to produce songs with complex sequential rules, whereas females do not.
In all ages and countries, music and dance have constituted a central part in human culture and communication. Recently, vocal-learning animals such as parrots and elephants have been found to share rhythmic ability with humans. Thus, we investigated the rhythmic synchronization of budgerigars, a vocal-mimicking parrot species, under controlled conditions and a systematically designed experimental paradigm as a first step in understanding the evolution of musical entrainment. We trained eight budgerigars to perform isochronous tapping tasks in which they pecked a key to the rhythm of audio-visual metronome-like stimuli. The budgerigars showed evidence of entrainment to external stimuli over a wide range of tempos. They seemed to be inherently inclined to tap at fast tempos, which have a similar time scale to the rhythm of budgerigars natural vocalizations. We suggest that vocal learning might have contributed to their performance, which resembled that of humans.
Vocal learning is a central functional constituent of human speech, and recent studies showing that adult male mice emit ultrasonic sound sequences characterized as "songs" have suggested that the ultrasonic courtship sounds of mice provide a mammalian model of vocal learning.
Since, similarly to humans, songbirds learn their vocalization through imitation during their juvenile stage, they have often been used as model animals to study the mechanisms of human verbal learning. Numerous anatomical and physiological studies have suggested that songbirds have a neural network called song system specialized for vocal learning and production in their brain. However, it still remains unknown what molecular mechanisms regulate their vocal development. It has been suggested that type-II cadherins are involved in synapse formation and function. Previously, we found that type-II cadherin expressions are switched in the robust nucleus of arcopallium from cadherin-7-positive to cadherin-6B-positive during the phase from sensory to sensorimotor learning stage in a songbird, the Bengalese finch. Furthermore, in vitro analysis using cultured rat hippocampal neurons revealed that cadherin-6B enhanced and cadherin-7 suppressed the frequency of miniature excitatory postsynaptic currents via regulating dendritic spine morphology.
Previous studies of rodents reported that the hippocampus plays an important role in social behavior as well as spatial behavior. However, there are inconsistencies between reports of the effects of hippocampal lesions on social behavior. The present study sought to clarify the aspects of social behavior in which the hippocampus plays a role in the degu, Octodon degus, a social rodent. We examined the effects of hippocampal lesions on social behavior in the degu using familiar and novel partners. When placed in a familiar environment with a familiar partner after surgery, sham operation control (S.Cont) degus exhibited affinitive behavior longer compared with hippocampal lesioned (HPC) degus. In a novel environment, S.Cont degus exhibited longer aggressive behavior toward novel partners, and longer affinitive behavior with familiar partners compared with HPC degus. HPC degus did not show evidence of differentiation in social behavior, regardless of partners novelty. The results of an anxiety test confirmed that these findings could not be attributed to changes in emotional state. We conducted an object-recognition test with the same subjects. HPC degus showed an impairment in spatial recognition but not object recognition. Taken together, these results suggest that the degu hippocampus plays an important role not only in spatial recognition but also social recognition. The changes in social behavior resulting from hippocampal lesions were interpreted as due to an impairment of social recognition rather than an impairment in novelty detection.
Unlike our primate cousins, many species of bird share with humans a capacity for vocal learning, a crucial factor in speech acquisition. There are striking behavioural, neural and genetic similarities between auditory-vocal learning in birds and human infants. Recently, the linguistic parallels between birdsong and spoken language have begun to be investigated. Although both birdsong and human language are hierarchically organized according to particular syntactic constraints, birdsong structure is best characterized as phonological syntax, resembling aspects of human sound structure. Crucially, birdsong lacks semantics and words. Formal language and linguistic analysis remains essential for the proper characterization of birdsong as a model system for human speech and language, and for the study of the brain and cognition evolution.
Vocal imitation in human infants and in some orders of birds relies on auditory-guided motor learning during a sensitive period of development. It proceeds from babbling (in humans) and subsong (in birds) through distinct phases towards the full-fledged communication system. Language development and birdsong learning have parallels at the behavioural, neural and genetic levels. Different orders of birds have evolved networks of brain regions for song learning and production that have a surprisingly similar gross anatomy, with analogies to human cortical regions and basal ganglia. Comparisons between different songbird species and humans point towards both general and species-specific principles of vocal learning and have identified common neural and molecular substrates, including the forkhead box P2 (FOXP2) gene.
Node perturbation learning is a stochastic gradient descent method for neural networks. It estimates the gradient by comparing an evaluation of the perturbed output and the unperturbed output performance, which we call the baseline. Node perturbation learning has primarily been investigated without taking noise on the baseline into consideration. In real biological systems, however, neural activities are intrinsically noisy, and hence, the baseline is likely contaminated with the noise. In this paper, we propose an alternative learning method that does not require such a noiseless baseline. Our method uses a "second perturbation", which is calculated with different noise than the first perturbation. By comparing the evaluation of the outcomes with the first perturbation and with the second perturbation, the network weights are updated. We reveal that the learning speed showed only a linear decrease with the variance of the second perturbation. Moreover, using the second perturbation can lead to a decrease in residual error compared to the case of using the noiseless baseline.
Autism is a highly variable brain developmental disorder and has a strong genetic basis. Pax6 is a pivotal player in brain development and maintenance. It is expressed in embryonic and adult neural stem cells, in astrocytes in the entire central nervous system, and in neurons in the olfactory bulb, amygdala, thalamus, and cerebellum, functioning in highly context-dependent manners. We have recently reported that Pax6 heterozygous mutant (rSey(2)/+) rats with a spontaneous mutation in the Pax6 gene, show impaired prepulse inhibition (PPI). In the present study, we further examined behaviors of rSey(2)/+ rats and revealed that they exhibited abnormality in social interaction (more aggression and withdrawal) in addition to impairment in rearing activity and in fear-conditioned memory. Ultrasonic vocalization (USV) in rSey(2)+ rat pups was normal in male but abnormal in female. Moreover, treatment with clozapine successfully recovered the defects in sensorimotor gating function, but not in fear-conditioned memory. Taken together with our prior human genetic data and results in other literatures, rSey(2)/+ rats likely have some phenotypic components of autism.
Songbirds have a specialized neural substrate for learned vocalization, called the song circuit, which consists of several song nuclei in the brain. The song control nucleus HVC (a letter-based name) is the intersection point of the song learning and vocal motor pathways. Knowledge of the types of genes expressed in the HVC is essential in understanding the molecular aspects of the HVC. Gene expression in the HVC under silent conditions shows the competence necessary for singing. To investigate this, we compared the HVC with its adjacent tissues in searching for the molecular specificities of the song nucleus HVC using an in-house cDNA microarray of the Bengalese finch (Lonchura striata var. domestica). Our microarray analysis revealed that 70 genes were differentially expressed in the HVC compared with the adjacent tissue. We investigated 27 of the microarray-selected genes that were enriched or repressed in the HVC by in situ hybridization. We found that multiple calcium-binding proteins (e.g., CAPS2, parvalbumin and ATH) were enriched in the HVC. Meanwhile, the adult HVC showed low expression levels of plasticity-related genes (e.g., CAMK2A and MAP2K1) compared with the juvenile HVC. The HVC plays an important role during song learning, but our results suggest that the plasticity of this nucleus may be suppressed during adulthood. Our findings provide new information about the molecular features that characterize the HVC.
Male Bengalese finches sing complex song sequences during courtship. To examine the female perception of sequence complexity, we tested female auditory processing with respect to sequential differences in the caudomedial nidopallium and caudomedial mesopallium. Repeated song presentations caused lower expression of the immediate early gene ZENK; however, consecutive presentation of a new song reinduced full ZENK expression. We presented a sequence-shuffled version of the fathers song after repeated presentation of the original (unmodified) fathers song. The shuffled songs caused lower ZENK expression in both the caudomedial nidopallium and caudomedial mesopallium. Although phonological differences caused full ZENK expression, sequential differences in song elements did not induce ZENK expression. Thus, it appears that female song perception is based on phonological, rather than sequential, information.
We examined the relationship between motor practice and auditory memory for sound sequences to evaluate the hypothesis that practice involving physical performance might enhance auditory memory. Participants learned two unfamiliar sound sequences using different training methods. Under the key-press condition, they learned a melody while pressing a key during auditory input. Under the no-key-press condition, they listened to another melody without any key pressing. The two melodies were presented alternately, and all participants were trained in both methods. Participants were instructed to pay attention under both conditions. After training, they listened to the two melodies again without pressing keys, and ERPs were recorded. During the ERP recordings, 10% of the tones in these melodies deviated from the originals. The grand-average ERPs showed that the amplitude of mismatch negativity (MMN) elicited by deviant stimuli was larger under the key-press condition than under the no-key-press condition. This effect appeared only in the high absolute pitch group, which included those with a pronounced ability to identify a note without external reference. This result suggests that the effect of training with key pressing was mediated by individual musical skills.
Neural activity is nonstationary and varies across time. Hidden Markov models (HMMs) have been used to track the state transition among quasi-stationary discrete neural states. Within this context, an independent Poisson model has been used for the output distribution of HMMs; hence, the model is incapable of tracking the change in correlation without modulating the firing rate. To achieve this, we applied a multivariate Poisson distribution with correlation terms for the output distribution of HMMs. We formulated a variational Bayes (VB) inference for the model. The VB could automatically determine the appropriate number of hidden states and correlation types while avoiding the overlearning problem. We developed an efficient algorithm for computing posteriors using the recursive relationship of a multivariate Poisson distribution. We demonstrated the performance of our method on synthetic data and real spike trains recorded from a songbird.
The anterior portion of the inferior parietal cortex possesses comprehensive representations of actions embedded in behavioural contexts. Mirror neurons, which respond to both self-executed and observed actions, exist in this brain region in addition to those originally found in the premotor cortex. We found that parietal mirror neurons responded differentially to identical actions embedded in different contexts. Another type of parietal mirror neuron represents an inverse and complementary property of responding equally to dissimilar actions made by itself and others for an identical purpose. Here, we propose a hypothesis that these sets of inferior parietal neurons constitute a neural basis for encoding the semantic equivalence of various actions across different agents and contexts. The neurons have mirror neuron properties, and they encoded generalization of agents, differentiation of outcomes, and categorization of actions that led to common functions. By integrating the activities of these mirror neurons with various codings, we further suggest that in the ancestral primates brains, these various representations of meaningful action led to the gradual establishment of equivalence relations among the different types of actions, by sharing common action semantics. Such differential codings of the components of actions might represent precursors to the parts of protolanguage, such as gestural communication, which are shared among various members of a society. Finally, we suggest that the inferior parietal cortex serves as an interface between this action semantics system and other higher semantic systems, through common structures of action representation that mimic language syntax.
Two novel RFamide peptides, kisspeptins and gonadotropin-inhibitory hormone (GnIH) are neuropeptides that appear critical in the regulation of the reproductive neuroendocrine axis. GnIH was first identified in avian brain, however, kisspeptins have not been identified in birds. To determine biochemically the presence of kisspeptins and GnIH in the zebra finch, a study was conducted to isolate these two peptides from zebra finch brain. Peptides were isolated by immunoaffinity purification and only one peptide was characterized by mass spectrometry. This peptide was confirmed to be a 12-amino acid sequence with RFamide at its C-terminus; its sequence is SIKPFSNLPLRFamide (zebra finch GnIH). By this approach, however, identification of kisspeptin from zebra finch brain was not achieved. Cloned zebra finch GnIH precursor cDNA encoded three peptides that possess characteristic LPXRFamide (X=L or Q) motifs at the C-termini. In situ hybridization and immunohistochemical analysis revealed the cellular localization of zebra finch GnIH mRNA and peptide in the paraventricular nucleus and the dorsomedial nucleus of the hypothalamus. Fluorescent immunohistochemistry with confocal microscopy indicated that GnIH-immunoreactive (ir) fibers are very close appositions with gonadotropin-releasing hormone-I (GnRH-I) cells. Furthermore GnIH-ir nerve fibers were widely distributed in the multiple brain regions including the septum, preoptic area, median eminence, optic tectum and median eminence. The prominent fibers were seen in the ventral tegmental area, midbrain central gray and dorsal motor nucleus of the vagus in the medulla. Thus, GnIH may participate in not only neuroendocrine functions but also regulation of motivation for social behavior and autonomic mechanisms.
Node perturbation learning has been receiving much attention as a method for achieving stochastic gradient descent. As it does not require direct gradient calculations, it can be applied to a reinforcement learning framework. However, in conventional node perturbation learning, the residual error due to perturbation is not eliminated even after convergence. Using infinitesimal perturbations suppresses the residual error, but such perturbations are less robust against uncertainty and noise in an eligibility trace, which is a memory of perturbation and input. We derive an optimal parameter schedule for node perturbation learning used with linear perceptrons with uncertainty in the eligibility trace. Our adaptive learning rule resolves the trade-off between robustness against the uncertainty and residual error reduction. The results obtained will be useful in designing learning rules and interpreting related biological knowledge.
Like humans, songbirds, including Bengalese finches, have hierarchical structures in their vocalizations. When humans perceive a sentence, processing occurs in phrase units, not words. In this study, we investigated whether songbirds also perceive their songs by chunks (clusters of song notes) rather than single song notes. We trained male Bengalese finches to react to a short noise in a Go/NoGo task. We then superimposed the noise onto recordings of their own songs and examined whether the reaction time was affected by the location of the short noise, that is, whether the noise was placed between chunks or in the middle of a chunk. The subjects reaction times to the noise in the middle of a chunk were significantly longer than those to the noise placed between chunks. This result was not observed, however, when the songs were played in reverse. We thus concluded that Bengalese finches perceive their songs by chunks rather than single notes.
Birds use various vocalizations to mark their territory and attract mates. Three groups of birds (songbirds, parrots, and hummingbirds) learn their vocalizations through imitation. In the brain of such vocal learners, there is a neural network called the song system specialized for vocal learning and production. In contrast, birds such as chickens and pigeons do not have such a neural network and can only produce innate sounds. Since each avian species shows distinct, genetically inherited vocal learning abilities that are related to its morphology, the avian vocal system is a good model for studying the evolution of functional neural circuits. Nevertheless, studies on avian vocalization from an evolutionary developmental-biological (Evo-Devo) perspective are scant. In the present review, we summarize the results of songbird studies and our recent work that used the Evo-Devo approach to understand the evolution of the avian vocal system.
Behavioral experiments have found that infants and adults learn statistically defined patterns presented in auditory and visual input sequences in the same manner regardless of whether the input was linguistic (syllables) or nonlinguistic (tones and shapes). In order do determine the time course and neural processes involved in online word segmentation and statistical learning of visual sequence, we recorded event-related potentials (ERPs) while participants were exposed to continuous sequences with elements organized into shape-words randomly connected to each other. After viewing three 6.6min sessions of sequences, the participants performed a behavioral choice test. The participants were divided into two groups (high and low learners) based on their behavioral performance. The overall mean performance was 72.2%, indicating that the shape sequence was segmented and that the participants learned the shape-triplets statistically. Grand-averaged ERPs showed that triplet-onset (the initial shapes of shape-words) elicited larger N400 amplitudes than did middle and final shapes embedded in continuous streams during the early learning sessions of high learners, but no triplet-onset effect was found among low learners. The results suggested that the N400 effect indicated online segmentation of the visual sequence and the degree of statistical learning. Our results also imply that statistical learning represents a common learning device.
The avian vocal system is a good model for exploring the molecular basis of neural circuit evolution related to behavioral diversity. Previously, we conducted a comparative gene expression analysis among two different families of vocal learner, the Bengalese finch (Lonchura striata var. domestica), a songbird, and the budgerigar (Melopsittacus undulatus), a parrot; and a non-learner, the quail (Coturnix coturnix), to identify various axon guidance molecules such as cadherin and neuropilin-1 as vocal control area-related genes. Here, we continue with this study and examine the expression of neuropilin and related genes in these species in more detail. We found that neuropilin-1 and its coreceptor, plexin-A4, were expressed in several vocal control areas in both Bengalese finch and budgerigar brains. In addition, semaphorin-3A, the ligand of neuropilin-1, expression was not detected in vocal control areas in both species. Furthermore, there was some similar gene expression in the quail brain. These results suggest the possibility that a change in the expression of a combination of semaphorin/neuropilin/plexin was involved in the acquisition of vocal learning ability during evolution.
We examined the integrative process between emotional facial expressions and musical excerpts by using an affective priming paradigm. Happy or sad musical stimuli were presented after happy or sad facial images during electroencephalography (EEG) recordings. We asked participants to judge the affective congruency of the presented face-music pairs. The congruency of emotionally congruent pairs was judged more rapidly than that of incongruent pairs. In addition, the EEG data showed that incongruent musical targets elicited a larger N400 component than congruent pairs. Furthermore, these effects occurred in nonmusicians as well as musicians. In sum, emotional integrative processing of face-music pairs was facilitated in congruent music targets and inhibited in incongruent music targets; this process was not significantly modulated by individual musical experience. This is the first study on musical stimuli primed by facial expressions to demonstrate that the N400 component reflects the affective priming effect.
A Noh mask worn by expert actors when performing on a Japanese traditional Noh drama is suggested to convey countless different facial expressions according to different angles of head/body orientation. The present study addressed the question of how different facial parts of a Noh mask, including the eyebrows, the eyes, and the mouth, may contribute to different emotional expressions. Both experimental situations of active creation and passive recognition of emotional facial expressions were introduced.
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