Akitoshi Ogawa

Neural correlates of species-typical illogical cognitive bias in human inference

The ability to think logically is a hallmark of human intelligence, yet our innate inferential abilities are marked by implicit biases that often lead to illogical inference. For example, given AB (“if A then B”), people frequently but fallaciously infer the inverse, BA. This mode of inference, called symmetry, is logically invalid because, although it may be true, it is not necessarily true. Given pairs of conditional relations, such as AB and BC, humans reflexively perform two additional modes of inference: transitivity, whereby one (validly) infers AC; and equivalence, whereby one (invalidly) infers CA. In sharp contrast, nonhuman animals can handle transitivity but can rarely be made to acquire symmetry or equivalence. In the present study, human subjects performed logical and illogical inferences about the relations between abstract, visually presented figures while their brain activation was monitored with fMRI. The prefrontal, medial frontal, and intraparietal cortices were activated during all modes of inference. Additional activation in the precuneus and posterior parietal cortex was observed during transitivity and equivalence, which may reflect the need to retrieve the intermediate stimulus (B) from memory. Surprisingly, the patterns of brain activation in illogical and logical inference were very similar. We conclude that the observed inference-related fronto-parietal network is adapted for processing categorical, but not logical, structures of association among stimuli. Humans might prefer categorization over the memorization of logical structures in order to minimize the cognitive working memory load when processing large volumes of information.

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.

Audio-visual perception of 3D cinematography: an fMRI study using condition-based and computation-based analyses.

The use of naturalistic stimuli to probe sensory functions in the human brain is gaining increasing interest. Previous imaging studies examined brain activity associated with the processing of cinematographic material using both standard “condition-based” designs, as well as “computational” methods based on the extraction of time-varying features of the stimuli (e.g. motion). Here, we exploited both approaches to investigate the neural correlates of complex visual and auditory spatial signals in cinematography. In the first experiment, the participants watched a piece of a commercial movie presented in four blocked conditions: 3D vision with surround sounds (3D-Surround), 3D with monaural sound (3D-Mono), 2D-Surround, and 2D-Mono. In the second experiment, they watched two different segments of the movie both presented continuously in 3D-Surround. The blocked presentation served for standard condition-based analyses, while all datasets were submitted to computation-based analyses. The latter assessed where activity co-varied with visual disparity signals and the complexity of auditory multi-sources signals. The blocked analyses associated 3D viewing with the activation of the dorsal and lateral occipital cortex and superior parietal lobule, while the surround sounds activated the superior and middle temporal gyri (S/MTG). The computation-based analyses revealed the effects of absolute disparity in dorsal occipital and posterior parietal cortices and of disparity gradients in the posterior middle temporal gyrus plus the inferior frontal gyrus. The complexity of the surround sounds was associated with activity in specific sub-regions of S/MTG, even after accounting for changes of sound intensity. These results demonstrate that the processing of naturalistic audio-visual signals entails an extensive set of visual and auditory areas, and that computation-based analyses can track the contribution of complex spatial aspects characterizing such life-like stimuli.

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.

Orienting of visuo-spatial attention in complex 3D space: Search and detection

The ability to detect changes in the environment is necessary for appropriate interactions with the external world. Changes in the background go more unnoticed than foreground changes, possibly because attention prioritizes processing of foreground/near stimuli. Here, we investigated the detectability of foreground and background changes within natural scenes and the influence of stereoscopic depth cues on this. Using a flicker paradigm, we alternated a pair of images that were exactly same or differed for one single element (i.e., a color change of one object in the scene). The participants were asked to find the change that occurred either in a foreground or background object, while viewing the stimuli either with binocular and monocular cues (bmC) or monocular cues only (mC). The behavioral results showed faster and more accurate detections for foreground changes and overall better performance in bmC than mC conditions. The imaging results highlighted the involvement of fronto‐parietal attention controlling networks during active search and target detection. These attention networks did not show any differential effect as function of the presence/absence of the binocular cues, or the detection of foreground/background changes. By contrast, the lateral occipital cortex showed greater activation for detections in foreground compared to background, while area V3A showed a main effect of bmC vs. mC, specifically during search. These findings indicate that visual search with binocular cues does not impose any specific requirement on attention‐controlling fronto‐parietal networks, while the enhanced detection of front/near objects in the bmC condition reflects bottom‐up sensory processes in visual cortex. Hum Brain Mapp 36:2231–2247, 2015.

Perceived moral traits of others differentiate the neural activation that underlies inequity-aversion

We have a social preference to reduce inequity in the outcomes between oneself and others. Such a preference varies according to others. We performed functional magnetic resonance imaging during an economic game to investigate how the perceived moral traits of others modulate the neural activities that underlie inequity-aversion. The participants unilaterally allocated money to three partners (good, neutral, and bad). During presentation of the good and neutral partners, the anterior region of the rostral medial frontal cortex (arMFC) showed increased functional connectivity with the caudate head and the anterior insula, respectively. Following this, participants allocated more money to the good partner, and less to the bad partner, compared with the neutral partner. The caudate head and anterior insula showed greater activation during fair allocation to the good and unfair allocation to the neutral partners, respectively. However, these regions were silent during allocations to the bad partner. Therefore, the arMFC-caudate/insula circuit encompasses distinct neural processes that underlie inequity-aversion in monetary allocations that the different moral traits of others can modulate.

Visual and auditory spatial signals in naturalistic environments: A computationally-based analysis of functional imaging data

A major challenge for fMRI studies is to use realistic stimuli, which is relevant for the understanding of multisensory interactions in the real world. Computational models (Itti et al., 1998; Kayser et al., 2005) have been used to track brain activity during viewing of complex audio-visual stimuli (Bartels et al., 2007; Bordier et al., 2013). We extended this approach to investigate activity associated with high-order spatial aspects in both vision and audition. We utilized a 3D-surround movie that included visual disparity cues and multiple sound sources (centre, front left/right, back left/right). For each visual frame, we computed a disparity map (Liu et al., 2011) and indexed absolute disparity (sum over the entire map) and gradient disparity (local contrast, Bordier et al., 2013). For audition, we indexed sound-spatiality by computing the correlation between each of the 5 external channels and a sixth channel that was delivered over headphones during fMRI (this contained primarily the ‘centre’ sound). We also indexed the sound intensity contrast (Bordier et al., 2013) to control for mere intensity changes over time. These indexes were used to fit the BOLD signal in 16 subjects, who watched the 3D-surround movie during fMRI. The results showed a dissociation between absolute disparity (PPC and V3A) and gradient disparity (V6, STS and IFG). The auditory–spatiality index correlated with activity in auditory cortex, even after accounting for changes of auditory-intensity. We conclude that the combination of computational models and fMRI enables studying brain activity associated with complex spatial signals in naturalistic multisensory environments.

Neural Correlates of Reasoning by Exclusion

When asked to select a label for a novel object from a given group of labels that includes both novel and familiar labels, one tends to choose a novel label. Nonhuman animals robustly fail to demonstrate the same tendency, although this tendency called “exclusion” that can bias human behavior may seem quite natural. The functional magnetic resonance imaging study described here investigated the neural correlates of this bias. The subjects were trained on two sample-to-comparison associations. In the scanner, they were shown a novel sample and were asked to choose between a trained comparison and a novel comparison. The subjects readily chose the novel comparison and rejected the trained one, thus demonstrating exclusion. Significant activation was observed in the prefrontal cortex (PFC) and inferior parietal lobule (IPL) during exclusion. Medial frontal activation was also observed when the novel stimuli appeared. These results suggest that the medial frontal cortex is associated with novelty detection and that the PFC and IPL are involved in rejecting the defined comparison.

Toe representation in the primary somatosensory cortex

Neocortical GABAergic interneurons are roughly classified into three subgroups and distinguished by chemical markers, such as parvalbumin (PV), somatostatin (SS) and the others. PV-expressing neurons, fast-spiking neurons, are a major component of GABAergic interneurons in the neocortex and have been implicated in higher order functions, such as learning and memory, by generating gamma frequency oscillations. We previously generated BAC transgenic mice expressing dendritic membrane-targeted GFP selectively in PV-expressing neurons, and succeeded in visualizing the somata and dendrites in a Golgi stain-like fashion. By combining the immunofluorescence labeling of GABAergic terminals with the antibody to vesicular GABA transporter, we revealed that GABAergic terminals preferentially apposed to the proximal dendrites and somata. It is, however, unclear which type of GABAergic interneurons innervates the proximal dendrites and somata of PV-expressing neurons. In the present study, we visualize the axon terminals of PVor SS-expressing neurons by immunofluorescence staining in the transgenic mice, observe the close appositions to PV-expressing neurons under confocal laser-scanning microscope, and analyze the synaptic inputs quantitatively. These experiments would provide new insights into the local circuits composed by neocortical interneurons.