fmri-validation-of-fnirs-measurements-during-a-naturalistic-task

fMRI Validation of fNIRS Measurements During a Naturalistic Task

We present a method to compare brain activity recorded with near-infrared spectroscopy (fNIRS) in a dance video game task to that recorded in a reduced ...

Dokkyo Medical University School of Medicine

Bipedal locomotion is a common daily activity. Despite its apparent simplicity, it is a complex set of movements that requires the integrated neural control of multiple body segments. We have recently shown that the juvenile Japanese monkey, M. fuscata, can be operant-trained to walk bipedally on moving treadmill. It can control the body axis and lower limb movements when confronted by a change in treadmill speed. M. fuscata can also walk bipedally on a slanted treadmill. Furthermore, it can learn to clear an obstacle attached to the treadmill's belt. When failing to clear the obstacle, the monkey stumbles but quickly corrects its posture and the associated movements of multiple motor segments to again resume smooth bipedal walking. These results give indication that in learning to walk bipedally, M. fuscata transforms relevant visual, vestibular, proprioceptive, and exteroceptive sensory inputs into commands that engage both anticipatory and reactive motor mechanisms. Both mechanisms are essential for meeting external demands imposed upon posture and locomotion.

Reactive and anticipatory control of posture and bipedal locomotion in a nonhuman primate.

This study investigated developmental aspects of the acquisition of operant-trained bipedal (Bp) standing and Bp walking in the normally quadrupedal (Qp) juvenile Japanese monkey (M. fuscata). Four male monkeys (age: 1.6 to 2.4 years, body weight: 3.3 to 4.6 kg) were initially operantly trained to stand upright on a smooth floor and a stationary treadmill belt (width = 60 cm, walking length = 150 cm). They were then trained to walk bipedally on the moving treadmill belt (speed: 0.4-0.7 m/s). A regular training program (5 days/week; 30-60 min/day) was given to each monkey for the first 40 to 60 days, followed by less intensive training. After the beginning of locomotor training, upright postural stability and Bp walking capability were assessed kinematically for 592, 534, 526, and 537 days on monkeys A, B, C, and D, respectively. Left side- and back-views of the walking monkey were photographed (10 frames/s) and videotaped (250 frames/s). Stick figures of the head, body, and hindlimbs were drawn with reference to ink-marks positioned in front of the ear and over the pivot points of hindlimb joints. All kinematic data were digitized and analyzed using image-analyzing software. After sufficient physical growth and locomotor training, all the monkeys gradually acquired: (a) a more upright and a more stable posture with a constant body axis orientation during Bp locomotion; (b) a more stable and a stronger functional coupling between the body and hindlimb movements with a less anterior (A)-posterior (P) fluctuation of a body axis; (c) a smaller leftward (Lt)-rightward (Rt) displacement of the midline pelvic position, allowing the monkey to walk along a straight course; (d) a more coordinated relationship among hip-knee, knee-ankle, and ankle-metatarsophalangeal (MTP) joints; and finally (e) the acquisition of well-coordinated Bp walking even at high treadmill belt speeds up to 1.5 m/s. All of these results demonstrated the capability of the physically developing monkey to integrate the neural and musculoskeletal mechanisms required for sufficient coordination of upper (head, neck, trunk) and lower (hindlimbs) motor segments so that Bp standing and Bp walking could be elaborated.

Acquisition of operant-trained bipedal locomotion in juvenile Japanese monkeys (Macaca fuscata): a longitudinal study.

studies are needed which consider CNS-controlled strategies for accommodating perturbed bipedal (Bp) posture and walking.

Obstacle clearance and prevention from falling in the bipedally walking Japanese monkey, Macaca fuscata.

It has been generally suggested that chewing produces an enhancing effect on cognitive performance-related aspects of memory by the test battery. Furthermore, recent studies have shown that chewing is associated with activation of various brain regions, including the prefrontal cortex. However, little is known about the relation between cognitive performances affected by chewing and the neuronal activity in specified regions in the brain. We therefore examined the effects of chewing on neuronal activities in the brain during a working memory task using fMRI. The subjects chewed gum, without odor and taste components, between continuously performed two- or three-back (n-back) working memory tasks. Chewing increased the BOLD signals in the middle frontal gyrus (Brodmann's areas 9 and 46) in the dorsolateral prefrontal cortex during the n-back tasks. Furthermore, there were more prominent activations in the right premotor cortex, precuneus, thalamus, hippocampus and inferior parietal lobe during the n-back tasks after the chewing trial. These results suggest that chewing may accelerate or recover the process of working memory besides inducing improvement in the arousal level by the chewing motion.

Effects of chewing in working memory processing.

We used functional magnetic resonance imaging (fMRI) to investigate the change in brain regional activity during gum chewing when edentulous subjects switched from mandibular complete dentures to implant-supported removable overdentures.

Chewing-induced regional brain activity in edentulous patients who received mandibular implant-supported overdentures: a preliminary report.

Using functional near infrared spectroscopy (fNIRS) we studied how playing a dance video game employs coordinated activation of sensory-motor integration centers of the superior parietal lobe (SPL) and superior temporal gyrus (STG). Subjects played a dance video game, in a block design with 30s of activity alternating with 30s of rest, while changes in oxy-hemoglobin (oxy-Hb) levels were continuously measured. The game was modified to compare difficult (4-arrow), simple (2-arrow), and stepping conditions. Oxy-Hb levels were greatest with increased task difficulty. The quick-onset, trapezoidal time-course increase in SPL oxy-Hb levels reflected the on-off neuronal response of spatial orienting and rhythmic motor timing that were required during the activity. Slow-onset, bell-shaped increases in oxy-Hb levels observed in STG suggested the gradually increasing load of directing multisensory information to downstream processing centers associated with motor behavior and control. Differences in temporal relationships of SPL and STG oxy-Hb concentration levels may reflect the functional roles of these brain structures during the task period. NIRS permits insights into temporal relationships of cortical hemodynamics during real motor tasks.

Parietal and temporal activity during a multimodal dance video game: an fNIRS study.

The Kana Pick-out Test (KPT), which uses Kana or Japanese symbols that represent syllables, requires parallel processing of discrete (pick-out) and continuous (reading) dual tasks. As a dual task, the KPT is thought to test working memory and executive function, particularly in the prefrontal cortex (PFC), and is widely used in Japan as a clinical screen for dementia. Nevertheless, there has been little neurological investigation into PFC activity during this test.

Activation of dorsolateral prefrontal cortex in a dual neuropsychological screening test: an fMRI approach.

In recent years, chewing has been discussed as producing effects of maintaining and sustaining cognitive performance. We have reported that chewing may improve or recover the process of working memory; however, the mechanisms underlying these phenomena are still to be elucidated. We investigated the effect of chewing on aspects of attention and cognitive processing speed, testing the hypothesis that this effect induces higher cognitive performance. Seventeen healthy adults (20-34 years old) were studied during attention task with blood oxygenation level-dependent functional (fMRI) at 3.0 T MRI. The attentional network test (ANT) within a single task fMRI containing two cue conditions (no cue and center cue) and two target conditions (congruent and incongruent) was conducted to examine the efficiency of alerting and executive control. Participants were instructed to press a button with the right or left thumb according to the direction of a centrally presented arrow. Each participant underwent two back-to-back ANT sessions with or without chewing gum, odorless and tasteless to remove any effect other than chewing. Behavioral results showed that mean reaction time was significantly decreased during chewing condition, regardless of speed-accuracy trade-off, although there were no significant changes in behavioral effects (both alerting and conflict effects). On the other hand, fMRI analysis revealed higher activations in the anterior cingulate cortex and left frontal gyrus for the executive network and motor-related regions for both attentional networks during chewing condition. These results suggested that chewing induced an increase in the arousal level and alertness in addition to an effect on motor control and, as a consequence, these effects could lead to improvements in cognitive performance.

Effects of chewing on cognitive processing speed.

We utilized the high temporal resolution of functional near-infrared spectroscopy to explore how sensory input (visual and rhythmic auditory cues) are processed in the cortical areas of multimodal integration to achieve coordinated motor output during unrestricted dance simulation gameplay. Using an open source clone of the dance simulation video game, Dance Dance Revolution, two cortical regions of interest were selected for study, the middle temporal gyrus (MTG) and the frontopolar cortex (FPC). We hypothesized that activity in the FPC would indicate top-down regulatory mechanisms of motor behavior; while that in the MTG would be sustained due to bottom-up integration of visual and auditory cues throughout the task. We also hypothesized that a correlation would exist between behavioral performance and the temporal patterns of the hemodynamic responses in these regions of interest. Results indicated that greater temporal accuracy of dance steps positively correlated with persistent activation of the MTG and with cumulative suppression of the FPC. When auditory cues were eliminated from the simulation, modifications in cortical responses were found depending on the gameplay performance. In the MTG, high-performance players showed an increase but low-performance players displayed a decrease in cumulative amount of the oxygenated hemoglobin response in the no music condition compared to that in the music condition. In the FPC, high-performance players showed relatively small variance in the activity regardless of the presence of auditory cues, while low-performance players showed larger differences in the activity between the no music and music conditions. These results suggest that the MTG plays an important role in the successful integration of visual and rhythmic cues and the FPC may work as top-down control to compensate for insufficient integrative ability of visual and rhythmic cues in the MTG. The relative relationships between these cortical areas indicated high- to low-performance levels when performing cued motor tasks. We propose that changes in these relationships can be monitored to gauge performance increases in motor learning and rehabilitation programs.

Frontotemporal oxyhemoglobin dynamics predict performance accuracy of dance simulation gameplay: temporal characteristics of top-down and bottom-up cortical activities.

Information about the material from which objects are made provide rich and useful clues that enable us to categorize and identify those objects, know their state (e.g., ripeness of fruits), and properly act on them. However, despite its importance, little is known about the neural processes that underlie material perception in nonhuman primates. Here we conducted an fMRI experiment in awake macaque monkeys to explore how information about various real-world materials is represented in the visual areas of monkeys, how these neural representations correlate with perceptual material properties, and how they correspond to those in human visual areas that have been studied previously. Using a machine-learning technique, the representation in each visual area was read out from multivoxel patterns of regional activity elicited in response to images of nine real-world material categories (metal, wood, fur, etc.). The congruence of the neural representations with either a measure of low-level image properties, such as spatial frequency content, or with the visuotactile properties of materials, such as roughness, hardness, and warmness, were tested. We show that monkey V1 shares a common representation with human early visual areas reflecting low-level image properties. By contrast, monkey V4 and the posterior inferior temporal cortex represent the visuotactile properties of material, as in human ventral higher visual areas, although there were some interspecies differences in the representational structures. We suggest that, in monkeys, V4 and the posterior inferior temporal cortex are important stages for constructing information about the material properties of objects from their low-level image features.

Representation of the material properties of objects in the visual cortex of nonhuman primates.

Although age-related decline in the useful field of view (UFOV) is well recognized as a risk factor for at-fault crash involvement in elderly drivers, there is still room to study its applicability to elderly Japanese drivers. In the current study, we thus examined the relationship between UFOV and at-fault crash history in an elderly Japanese population. We also explored whether potential factors that create awareness of reduced driving fitness could be a trigger for the self-regulation of driving in elderly drivers.

Article	Year
Reactive and anticipatory control of posture and bipedal locomotion in a nonhuman primate. Progress in brain research\| PubMed ID: 14653164	2004
Acquisition of operant-trained bipedal locomotion in juvenile Japanese monkeys (Macaca fuscata): a longitudinal study. Motor control\| PubMed ID: 14999136	2003
Obstacle clearance and prevention from falling in the bipedally walking Japanese monkey, Macaca fuscata. Age and ageing\| PubMed ID: 16926198	2006
Effects of chewing in working memory processing. Neuroscience letters\| PubMed ID: 18403120	2008
Chewing-induced regional brain activity in edentulous patients who received mandibular implant-supported overdentures: a preliminary report. Journal of prosthodontic research\| PubMed ID: 20951664	2011
Parietal and temporal activity during a multimodal dance video game: an fNIRS study. Neuroscience letters\| PubMed ID: 21875646	2011
Activation of dorsolateral prefrontal cortex in a dual neuropsychological screening test: an fMRI approach. Behavioral and brain functions : BBF\| PubMed ID: 22640773	2012
Effects of chewing on cognitive processing speed. Brain and cognition\| PubMed ID: 23375117	2013
Frontotemporal oxyhemoglobin dynamics predict performance accuracy of dance simulation gameplay: temporal characteristics of top-down and bottom-up cortical activities. NeuroImage\| PubMed ID: 23707582	2014
Representation of the material properties of objects in the visual cortex of nonhuman primates. The Journal of neuroscience : the official journal of the Society for Neuroscience\| PubMed ID: 24523555	2014
Is the useful field of view a good predictor of at-fault crash risk in elderly Japanese drivers? Geriatrics & gerontology international\| PubMed ID: 25110186	2015

Atsumichi Tachibana

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