Atsumichi Tachibana

Effects of chewing in working memory processing

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 (Brodmanns 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 on cognitive processing speed

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.

CHEWING AMELIORATES STRESS-INDUCED SUPPRESSION OF HIPPOCAMPAL LONG-TERM POTENTIATION

Research has established that severe stress adversely affects hippocampal memory, and chewing has been suggested to restore impaired cognitive functions in the hippocampus. To address how chewing involves stress-attenuated hippocampal memory process, we measured the long-term potentiation (LTP) of hippocampal slices of adult male rats that had experienced restraint stress, including some rats that were allowed to chew a wooden stick during the stress period and other rats that were not. The three experimental conditions were: 1) restraint stress without chewing (ST), 2) restraint stress with chewing (SC), and 3) no treatment (CT). We prepared hippocampal slices and collected trunk blood from all experimental animals. For rats in the two stressed groups, we collected tissue and blood at one of three post-stress time points: immediately after, 24 h after, or 48 h after exposure to the stressor. We found that the magnitude of LTP in both group ST and SC was significantly attenuated immediately after stress exposure. However, within 24 h after the end of the stress period, LTP had returned to the control level in group SC whereas it remained low in group ST. At the same post-stress time point, we found that facilitation of N-methyl-D-aspartate (NMDA) receptors by bath-applied glycine had less effect on the magnitude of LTP in group SC than on group ST, suggesting that most NMDA receptors had already become functionally restored in group SC by that time. Plasma concentration of adrenocorticotropic hormone was significantly elevated only in group ST immediately after exposure to the stressor, reflecting the involvement of chewing in decreasing subsequent corticosterone secretion. Thus, the present study demonstrates that chewing ameliorates the stress-induced impairment of NMDA receptor-mediated LTP, suggesting chewing as a good strategy to cope with severe stress by suppressing excessive endocrine responses.

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

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.

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

PURPOSE 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. METHODS Four edentulous patients (3 males and 1 female, aged 64 to 79 years) participated in the study. All subjects received a set of new maxillary and mandibular complete dentures (CD), followed by a maxillary complete denture and a new mandibular implant-supported removable overdentures (IOD). A 3-T fMRI scanner produced images of the regional brain activity for each subject that showed changes in the blood-oxygenation-level-dependent (BOLD) contrast in the axial orientation during gum-chewing with CD and IOD. RESULTS Region-of-interest analysis showed that IOD treatment significantly suppressed chewing-induced brain activity in the prefrontal cortex. The chewing-induced brain activities in the primary sensorimotor cortex and cerebellum tended to decrease with IOD treatment, however they did not reach to significance level. There was no change in brain activity in the supplementary motor area, thalamus and insula between gum chewing with CD and IOD. Group comparison using statistical parametrical mapping further showed that, within the prefrontal cortex, the neural activity of the frontal pole significantly decreased during gum-chewing with IOD when compared to that with CD (P<0.05). CONCLUSION Despite the limitation of a small sample size, these results suggest that the gum-chewing task in elderly edentulous patients resulted in differential neural activity in the frontal pole within the prefrontal cortex between the 2 prosthodontic therapies-mandibular CD and IOD.

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

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.

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 version of the task using fMRI (functional magnetic resonance imaging). Recently, it has been shown that fNIRS can accurately record functional brain activities equivalent to those concurrently recorded with functional magnetic resonance imaging for classic psychophysical tasks and simple finger tapping paradigms. However, an often quoted benefit of fNIRS is that the technique allows for studying neural mechanisms of complex, naturalistic behaviors that are not possible using the constrained environment of fMRI. Our goal was to extend the findings of previous studies that have shown high correlation between concurrently recorded fNIRS and fMRI signals to compare neural recordings obtained in fMRI procedures to those separately obtained in naturalistic fNIRS experiments. Specifically, we developed a modified version of the dance video game Dance Dance Revolution (DDR) to be compatible with both fMRI and fNIRS imaging procedures. In this methodology we explain the modifications to the software and hardware for compatibility with each technique as well as the scanning and calibration procedures used to obtain representative results. The results of the study show a task-related increase in oxyhemoglobin in both modalities and demonstrate that it is possible to replicate the findings of fMRI using fNIRS in a naturalistic task. This technique represents a methodology to compare fMRI imaging paradigms which utilize a reduced-world environment to fNIRS in closer approximation to naturalistic, full-body activities and behaviors. Further development of this technique may apply to neurodegenerative diseases, such as Parkinson’s disease, late states of dementia, or those with magnetic susceptibility which are contraindicated for fMRI scanning.

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

BackgroundThe 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.MethodsWe used functional magnetic resonance imaging (fMRI) to evaluate changes in the blood oxygenation level-dependent (BOLD) signal in young healthy adults during performance of a computerized KPT dual task (comprised of reading comprehension and picking out vowels) and compared it to its single task components (reading or vowel pick-out alone).ResultsBehavioral performance of the KPT degraded compared to its single task components. Performance of the KPT markedly increased BOLD signal intensity in the PFC, and also activated sensorimotor, parietal association, and visual cortex areas. In conjunction analyses, bilateral BOLD signal in the dorsolateral PFC (Brodmanns areas 45, 46) was present only in the KPT.ConclusionsOur results support the central bottleneck theory and suggest that the dorsolateral PFC is an important mediator of neural activity for both short-term storage and executive processes. Quantitative evaluation of the KPT with fMRI in healthy adults is the first step towards understanding the effects of aging or cognitive impairment on KPT performance.

Interactions between chewing and brain activity in humans

The involvement of chewing in brain activity in humans has been studied. In our studies using functional magnetic resonance imaging (fMRI) and behavioral techniques, chewing resulted in a bilateral increase in blood oxygenation leveldependent (BOLD) signals in the sensorimotor cortex, supplementary motor area, insula, thalamus, and cerebellum. In addition, in the first three regions, chewing moderately hard gum produced stronger signals than chewing hard gum. However, in the aged group, the BOLD signal increases were smaller in the first three regions and higher in the cerebellum. Only the aged subjects showed significant increases in various association areas to which input activities in the primary sensorimotor cortex, supplementary area, or insula had positive path coefficients. Furthermore, chewing ameliorates the age-related decrease in hippocampal activities during encoding and that in retrieval memory. The findings suggest the involvement of chewing in memory processes.

Multi-core processing within the frontal lobe

Study of the brain is somewhat similar to understanding a multi-core processor. Video games offer a way to study how different sensory inputs affect motor output. Co-processors, comparator elements, and integrators of executive function and working memory work to balance sensory modalities and integrate this information into motor output. In this paper we describe the differences in functional brain activity using magnetic resonance imaging (MRI) while actively interacting with the game Dance Dance Revolution. We hypothesized that distinct patterns of activity within frontal lobe would be seen with respect to motor output when presented with various types of modified sensory cues. 16 subjects underwent the scanning procedure that included four different conditions. Results indicate that depending on the type of sensory information made available, different areas associated with working memory and executive function could be isolated.