functional-imaging-auditory-cortex-adult-cats-using-high-field

Functional Imaging of Auditory Cortex in Adult Cats using High-field fMRI

Current knowledge of sensory processing in the mammalian auditory system is mainly derived from electrophysiological studies in a variety of animal ...

University of Western Ontario

Frequency-modulated (FM) stimuli have been used to explore the behavior of neurons in the auditory cortex of several animal models; however, the properties of FM-sensitive auditory cortical neurons in the chinchilla are still unknown. Single-unit responses to FM stimulation were obtained from the auditory cortex of anesthetized adult chinchillas (Chinchilla laniger). Upward and downward linear FM sweeps spanning frequencies from 0.1 to 20 kHz were presented at speeds of 0.05 to 0.82 kHz/ms. Results indicated that >90% of sampled neurons were responsive to FM sweeps. The population preference was for upward FM sweeps and for medium to fast speeds (> or =0.3 kHz/ms). Few units (3%) were selective for downward FM sweeps, whereas <22% of units preferred slow speeds (< or =0.1 kHz/ms). Velocity preference and direction sensitivity were positively correlated for upward sweeps only (r = 0.40, P = 0.0021, t-test). Three types of firing rate patterns were observed in the FM response peristimulus time histograms: a single peak at sweep onset/offset ("onset") and a single peak ("late") or multiple peaks ("burst") during the sweep. "Late" units expressed the highest mean values for direction sensitivity and speed selectivity; "onset" units were selective only for direction and "burst" units were not selective for either direction or speed. The robust responsiveness of these neurons to FM sweeps suggests a functional role for FM detection such as the identification of FM sweeps present in vocalizations of other organisms within the chinchilla's natural environment.

Responses of neurons in chinchilla auditory cortex to frequency-modulated tones.

Responses to cortical neurons to frequency-modulated (FM) stimuli have been described in various adult animal models. Here, we ask whether FM coding at the cortical level is innate or if it is influenced by postnatal environmental experience. We report on the FM response properties of neurons in core auditory cortex of newborn (P3), 1-month-old (P28) and adult (>1-year-old) anesthetized chinchillas (Chinchilla laniger). Upward and downward linear FM sweeps spanning frequencies from 0.1 to 20 kHz were presented monaurally at speeds of 0.05 to 0.82 kHz/ms. Results indicated that neurons in neonatal pups were responsive to FM stimulation. While we observed a developmental increase in the selectivity of units for FM sweep direction (p<0.01, one-way ANOVA), selectivity for sweep speed appeared to be established early in development. Chinchilla pup neurons also demonstrated single-peak (single dominant response during FM sweep presentation) and multi-peak (multiple distinct responses during FM sweep) temporal response patterns to FM stimuli similar to those observed in adults. A developmental increase in the proportion of multi-peak units closely paralleled a previously reported increase in the complexity of pure tone receptive fields. We suggest that units in core auditory cortex of the chinchilla are not uniquely activated by FM sounds but that FM responses are largely predictable based on how changing frequency stimuli interact with the tonal receptive fields of neurons in the auditory cortex.

Postnatal development of neuronal responses to frequency-modulated tones in chinchilla auditory cortex.

Early postnatal exposure to an abnormal acoustic environment has been shown to significantly influence the behaviour of neurons in the auditory cortex. In the present study, we ask if sustained neonatal exposure to an FM sweep affects the development of responses to tonal and FM stimuli in chinchilla auditory cortex. Newborn chinchilla pups were exposed continuously to an upward linear FM sweep (0.1-20 kHz) at 0.05 kHz/ms for 4 weeks. Neuronal responses to pure tones and bidirectional linear FM sweeps (range: 0.1-20 kHz; speeds: 0.05-0.82 kHz/ms) were assessed in anesthetized animals following the exposure period as well as in age-matched controls (P28). We hypothesized that constant FM exposure would increase the response selectivity of cortical neurons to the environmental FM sweep. However, our results show that while tonal response latencies increased after the exposure period (p < 0.0001, one-way ANOVA), the exposure stimulus had minimal effect on neuronal direction sensitivity and decreased neuronal selectivity for any of the presented FM sweep speeds (p < 0.05, one-way ANOVA). We therefore suggest that the development of FM direction sensitivity is experience-independent while normal acoustic experience may be required to maintain FM speed tuning.

Neuronal responses in chinchilla auditory cortex after postnatal exposure to frequency-modulated tones.

Much of what is known about the cortical organization for audition in humans draws from studies of auditory cortex in the cat. However, these data build largely on electrophysiological recordings that are both highly invasive and provide less evidence concerning macroscopic patterns of brain activation. Optical imaging, using intrinsic signals or dyes, allows visualization of surface-based activity but is also quite invasive. Functional magnetic resonance imaging (fMRI) overcomes these limitations by providing a large-scale perspective of distributed activity across the brain in a non-invasive manner. The present study used fMRI to characterize stimulus-evoked activity in auditory cortex of an anesthetized (ketamine/isoflurane) cat, focusing specifically on the blood-oxygen-level-dependent (BOLD) signal time course. Functional images were acquired for adult cats in a 7 T MRI scanner. To determine the BOLD signal time course, we presented 1s broadband noise bursts between widely spaced scan acquisitions at randomized delays (1-12 s in 1s increments) prior to each scan. Baseline trials in which no stimulus was presented were also acquired. Our results indicate that the BOLD response peaks at about 3.5s in primary auditory cortex (AI) and at about 4.5 s in non-primary areas (AII, PAF) of cat auditory cortex. The observed peak latency is within the range reported for humans and non-human primates (3-4 s). The time course of hemodynamic activity in cat auditory cortex also occurs on a comparatively shorter scale than in cat visual cortex. The results of this study will provide a foundation for future auditory fMRI studies in the cat to incorporate these hemodynamic response properties into appropriate analyses of cat auditory cortex.

Characterization of the blood-oxygen level-dependent (BOLD) response in cat auditory cortex using high-field fMRI.

In contrast to numerous studies of transcallosal communication in visual and somatosensory cortices, the functional properties of interhemispheric connections between auditory cortical fields have not been widely scrutinized. Therefore, the purpose of the present investigation was to measure the magnitude and type (inhibitory/excitatory) of modulatory properties of core auditory fields on contralateral primary auditory cortex (A1) activity. We combined single-unit neuronal recordings with reversible cooling deactivation techniques to measure variations in contralateral A1 response levels during A1, anterior auditory field (AAF), or simultaneous A1 and AAF neuronal discharge suppression epochs in cat auditory cortex. Cortical activity was evoked by presentation of pure tones, noise bursts, and frequency-modulated (FM) sweeps before, during, and after cortical deactivation periods. Comparisons of neuronal response changes before and during neuronal silencing revealed three major findings. First, deactivation of A1 and AAF-induced significant peak response reductions in contralateral A1 activity during simple (tonal) and complex (noise bursts and FM sweeps) acoustic exposure. Second, decreases in A1 neuronal activity appear to be in agreement with anatomical laminar termination patterns emanating from contralateral auditory cortex fields. Third, modulatory properties of core auditory areas lack hemispheric lateralization. These findings demonstrate that during periods of acoustic exposure, callosal projections emanating from core auditory areas modulate A1 neuronal activity via excitatory inputs.

Influence of core auditory cortical areas on acoustically evoked activity in contralateral primary auditory cortex.

When conducting auditory investigations using functional magnetic resonance imaging (fMRI), there are inherent potential confounds that need to be considered. Traditional continuous fMRI acquisition methods produce sounds >90dB which compete with stimuli or produce neural activation masking evoked activity. Sparse scanning methods insert a period of reduced MRI-related noise, between image acquisitions, in which a stimulus can be presented without competition. In this study, we compared sparse and continuous scanning methods to identify the optimal approach to investigate acoustically evoked cortical, thalamic and midbrain activity in the cat. Using a 7T magnet, we presented broadband noise, 10kHz tones, or 0.5kHz tones in a block design, interleaved with blocks in which no stimulus was presented. Continuous scanning resulted in larger clusters of activation and more peak voxels within the auditory cortex. However, no significant activation was observed within the thalamus. Also, there was no significant difference found, between continuous or sparse scanning, in activations of midbrain structures. Higher magnitude activations were identified in auditory cortex compared to the midbrain using both continuous and sparse scanning. These results indicate that continuous scanning is the preferred method for investigations of auditory cortex in the cat using fMRI. Also, choice of method for future investigations of midbrain activity should be driven by other experimental factors, such as stimulus intensity and task performance during scanning.

Article	Year
Responses of neurons in chinchilla auditory cortex to frequency-modulated tones. Journal of neurophysiology\| PubMed ID: 19211659	2009
Postnatal development of neuronal responses to frequency-modulated tones in chinchilla auditory cortex. Brain research\| PubMed ID: 19874805	2010
Neuronal responses in chinchilla auditory cortex after postnatal exposure to frequency-modulated tones. Hearing research\| PubMed ID: 21144889	2011
Characterization of the blood-oxygen level-dependent (BOLD) response in cat auditory cortex using high-field fMRI. NeuroImage\| PubMed ID: 23000258	2013
Influence of core auditory cortical areas on acoustically evoked activity in contralateral primary auditory cortex. The Journal of neuroscience : the official journal of the Society for Neuroscience\| PubMed ID: 23303954	2013
There's more than one way to scan a cat: Imaging cat auditory cortex with high-field fMRI using continuous or sparse sampling. Journal of neuroscience methods\| PubMed ID: 24389047	2014

Trecia A. Brown

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