Takeshi Asamizuya

Attention But Not Awareness Modulates the BOLD Signal in the Human V1 During Binocular Suppression

Activity in the primary visual cortex is modulated by attention to an object, but not by whether the object is visible. Although recent psychophysical studies indicate that visual awareness and top-down attention are two distinct processes, it is not clear how they are neurally dissociated in the visual system. Using a two-by-two factorial functional magnetic resonance imaging design with binocular suppression, we found that the visibility or invisibility of a visual target led to only nonsignificant blood oxygenation level–dependent (BOLD) effects in the human primary visual cortex (V1). Directing attention toward and away from the target had much larger and robust effects across all study participants. The difference in the lower-level limit of BOLD activation between attention and awareness illustrates dissociated neural correlates of the two processes. Our results agree with previously reported V1 BOLD effects on attention, while they invite a reconsideration of the functional role of V1 in visual awareness.

Gray and white matter changes associated with tool-use learning in macaque monkeys

We used noninvasive MRI and voxel-based morphometry (VBM) to detect changes in brain structure in three adult Japanese macaques trained to use a rake to retrieve food rewards. Monkeys, who were naive to any previous tool use, were scanned repeatedly in a 4-T scanner over 6 weeks, comprising 2 weeks of habituation followed by 2 weeks of intensive daily training and a 2-week posttraining period. VBM analysis revealed significant increases in gray matter with rake performance across the three monkeys. The effects were most significant (P < 0.05 corrected for multiple comparisons across the whole brain) in the right superior temporal sulcus, right second somatosensory area, and right intraparietal sulcus, with less significant effects (P < 0.001 uncorrected) in these same regions of the left hemisphere. Bilateral increases were also observed in the white matter of the cerebellar hemisphere in lobule 5. In two of the monkeys who exhibited rapid learning of the rake task, gray matter volume in peak voxels increased by up to 17% during the intensive training period; the earliest changes were seen after 1 week of intensive training, and they generally peaked when performance on the task plateaued. In the third monkey, who was slower to learn the task, peak voxels showed no systematic changes. Thus, VBM can detect significant brain changes in individual trained monkeys exposed to tool-use training for the first time. This approach could open up a means of investigating the underlying neurobiology of motor learning and other higher brain functions in individual animals.

The neural basis of intuitive best next-move generation in board game experts.

Compared with amateurs, expert shogi players show specific brain activation patterns. The superior capability of cognitive experts largely depends on quick automatic processes. To reveal their neural bases, we used functional magnetic resonance imaging to study brain activity of professional and amateur players in a board game named shogi. We found two activations specific to professionals: one in the precuneus of the parietal lobe during perception of board patterns, and the other in the caudate nucleus of the basal ganglia during quick generation of the best next move. Activities at these two sites covaried in relevant tasks. These results suggest that the precuneus-caudate circuit implements the automatic, yet complicated, processes of board-pattern perception and next-move generation in board game experts.

Creating a population-averaged standard brain template for Japanese macaques (M. fuscata)

A number of modern digital anatomy techniques, based on structural MR brain images, have recently become applicable to the non-human primate brain. Such voxel-based quantitative techniques require a species-specific standardized brain template. Here we present a brain template for the Japanese macaque (Macaca fuscata). The template was designed to be used as a tool for spatially normalising Japanese macaque brains into a standard space. Although this species of macaque monkey is widely used in neuroscience research, including studies of higher cognitive brain functions, no standard MRI template of its brain is presently available. The template presented here is based on T1/T2* weighted, high-resolution 4 T MR images obtained from 16 male adult Japanese macaque monkeys. T1/T2* images were used to correct the signal inequalities resulting from the use of a surface coil. Based on these images, population-averaged probability maps were created for grey matter, white matter and cerebrospinal fluid. The new template presented here should facilitate future brain research using the Japanese macaque monkey. Whole brain templates are available at http://brainatlas.brain.riken.jp/jm/modules/xoonips/listitem.php?index_id=9.

Opposing Effects of Contextual Surround in Human Early Visual Cortex Revealed by Functional Magnetic Resonance Imaging with Continuously Modulated Visual Stimuli

Spatial context in vision has profound effects on neural responses and perception. Recent animal studies suggest that the effect of surround on a central stimulus can dramatically change its character depending on the contrast of the center stimulus, but such a drastic change has not been demonstrated in the human visual cortex. To examine the dependency of the surround effect on the contrast of the center stimulus, we conducted an functional magnetic resonance imaging experiment by using a low or a high contrast in the center region while the surround contrast was sinusoidally modulated between the two contrasts. We found that the blood oxygen level-dependent response in human V1 corresponding to the center region was differentially modulated by the surround contrast, depending crucially on the center contrast: whereas a suppressive effect was observed in conditions in which the center contrast was high, a facilitative effect was seen in conditions where the center contrast was low.

Developing intuition: neural correlates of cognitive-skill learning in caudate nucleus.

The superior capability of cognitive experts largely depends on automatic, quick information processing, which is often referred to as intuition. Intuition develops following extensive long-term training. There are many cognitive models on intuition development, but its neural basis is not known. Here we trained novices for 15 weeks to learn a simple board game and measured their brain activities in early and end phases of the training while they quickly generated the best next-move to a given board pattern. We found that the activation in the head of caudate nucleus developed over the course of training, in parallel to the development of the capability to quickly generate the best next-move, and the magnitude of the caudate activity was correlated with the subjects performance. In contrast, cortical activations, which already appeared in the early phase of training, did not further change. Thus, neural activation in the caudate head, but not those in cortical areas, tracked the development of capability to quickly generate the best next-move, indicating that circuitries including the caudate head may automate cognitive computations.

Neural basis of decision-making guided by emotional outcomes

Emotional events resulting from a choice influence an individuals subsequent decision making. Although the relationship between emotion and decision making has been widely discussed, previous studies have mainly investigated decision outcomes that can easily be mapped to reward and punishment, including monetary gain/loss, gustatory stimuli, and pain. These studies regard emotion as a modulator of decision making that can be made rationally in the absence of emotions. In our daily lives, however, we often encounter various emotional events that affect decisions by themselves, and mapping the events to a reward or punishment is often not straightforward. In this study, we investigated the neural substrates of how such emotional decision outcomes affect subsequent decision making. By using functional magnetic resonance imaging (fMRI), we measured brain activities of humans during a stochastic decision-making task in which various emotional pictures were presented as decision outcomes. We found that pleasant pictures differentially activated the midbrain, fusiform gyrus, and parahippocampal gyrus, whereas unpleasant pictures differentially activated the ventral striatum, compared with neutral pictures. We assumed that the emotional decision outcomes affect the subsequent decision by updating the value of the options, a process modeled by reinforcement learning models, and that the brain regions representing the prediction error that drives the reinforcement learning are involved in guiding subsequent decisions. We found that some regions of the striatum and the insula were separately correlated with the prediction error for either pleasant pictures or unpleasant pictures, whereas the precuneus was correlated with prediction errors for both pleasant and unpleasant pictures.

Hand before foot? Cortical somatotopy suggests manual dexterity is primitive and evolved independently of bipedalism

People have long speculated whether the evolution of bipedalism in early hominins triggered tool use (by freeing their hands) or whether the necessity of making and using tools encouraged the shift to upright gait. Either way, it is commonly thought that one led to the other. In this study, we sought to shed new light on the origins of manual dexterity and bipedalism by mapping the neural representations in the brain of the fingers and toes of living people and monkeys. Contrary to the ‘hand-in-glove’ notion outlined above, our results suggest that adaptations underlying tool use evolved independently of those required for human bipedality. In both humans and monkeys, we found that each finger was represented separately in the primary sensorimotor cortex just as they are physically separated in the hand. This reflects the ability to use each digit independently, as required for the complex manipulation involved in tool use. The neural mapping of the subjects’ toes differed, however. In the monkeys, the somatotopic representation of the toes was fused, showing that the digits function predominantly as a unit in general grasping. Humans, by contrast, had an independent neurological representation of the big toe (hallux), suggesting association with bipedal locomotion. These observations suggest that the brain circuits for the hand had advanced beyond simple grasping, whereas our primate ancestors were still general arboreal quadrupeds. This early adaptation laid the foundation for the evolution of manual dexterity, which was preserved and enhanced in hominins. In hominins, a separate adaptation, involving the neural separation of the big toe, apparently occurred with bipedality. This accords with the known fossil evidence, including the recently reported hominin fossils which have been dated to 4.4 million years ago.

Neural basis of economic bubble behavior

Throughout human history, economic bubbles have formed and burst. As a bubble grows, microeconomic behavior ceases to be constrained by realistic predictions. This contradicts the basic assumption of economics that agents have rational expectations. To examine the neural basis of behavior during bubbles, we performed functional magnetic resonance imaging while participants traded shares in a virtual stock exchange with two non-bubble stocks and one bubble stock. The price was largely deflected from the fair price in one of the non-bubble stocks, but not in the other. Their fair prices were specified. The price of the bubble stock showed a large increase and battering, as based on a real stock-market bust. The imaging results revealed modulation of the brain circuits that regulate trade behavior under different market conditions. The premotor cortex was activated only under a market condition in which the price was largely deflected from the fair price specified. During the bubble, brain regions associated with the cognitive processing that supports order decisions were identified. The asset preference that might bias the decision was associated with the ventrolateral prefrontal cortex and the dorsolateral prefrontal cortex (DLPFC). The activity of the inferior parietal lobule (IPL) was correlated with the score of future time perspective, which would bias the estimation of future price. These regions were deemed to form a distinctive network during the bubble. A functional connectivity analysis showed that the connectivity between the DLPFC and the IPL was predominant compared with other connectivities only during the bubble. These findings indicate that uncertain and unstable market conditions changed brain modes in traders. These brain mechanisms might lead to a loss of control caused by wishful thinking, and to microeconomic bubbles that expand, on the macroscopic scale, toward bust.

Tracking Individual Differences in Perception by TMS-EEG Intrinsic Effective Connectivity

Non-invasive human electroencephalography (EEG) coupled with transcranial magnetic stimulation (TMS) is currently used to measure coarse stimulus-response relationships in brain physiology during behavior. However, with key modifications, the TMS-EEG technique holds even greater promise for monitoring fine-scale neural signatures of human behavior. Here, we demonstrate that a novel TMS-EEG co-registration technique can dynamically monitor individual human variation in perception based solely on EEG resting-state intrinsic effective connectivity probed by TMS-based phase resetting of ongoing activity. We used a bistable stimulus task, where the percept is perceived as either horizontal or vertical apparent motion, to record gamma band interhemispheric integration of information. Fine-grained inter-individual behavioral differences in horizontal motion bias could be measured by tracking resting-state gamma-band effective connectivity from right hMT+ to left hMT+. Thus, our method of triggering intrinsic resting-state effective connectivity in oscillatory dynamics can monitor individual differences in perception via the long-range integration of information. This technique will be useful for the manipulative dissection of individual-scale human cognition mediated by neural dynamics and may also expand neurofeedback approaches.