Continuous decision to wait for a future reward is guided by fronto-hippocampal anticipatory dynamics.

Deciding whether to wait for a future reward is crucial for surviving in an uncertain world. While seeking rewards, agents anticipate a reward in the present environment and constantly face a trade-off between staying in their environment or leaving it. It remains unclear, however, how humans make continuous decisions in such situations. Here, we show that anticipatory activity in the anterior prefrontal cortex, ventrolateral prefrontal cortex, and hippocampus underpins continuous stay-leave decision-making. Participants awaited real liquid rewards available after tens of seconds, and their continuous decision was tracked by dynamic brain activity associated with the anticipation of a reward. Participants stopped waiting more frequently and sooner after they experienced longer delays and received smaller rewards. When the dynamic anticipatory brain activity was enhanced in the anterior prefrontal cortex, participants remained in their current environment, but when this activity diminished, they left the environment. Moreover, while experiencing a delayed reward in a novel environment, the ventrolateral prefrontal cortex and hippocampus showed anticipatory activity. Finally, the activity in the anterior prefrontal cortex and ventrolateral prefrontal cortex was enhanced in participants adopting a leave strategy, whereas those remaining stationary showed enhanced hippocampal activity. Our results suggest that fronto-hippocampal anticipatory dynamics underlie continuous decision-making while anticipating a future reward.

Premovement activity in the mesocortical system links peak force but not initiation of force generation under incentive motivation.

Motivation facilitates motor performance; however, the neural substrates of the psychological effects on motor performance remain unclear. We conducted a functional magnetic resonance imaging experiment while human subjects performed a ready-set-go task with monetary incentives. Although subjects were only motivated to respond quickly, increasing the incentives improved not only reaction time but also peak grip force. However, the trial-by-trial correlation between reaction time and peak grip force was weak. Extensive areas in the mesocortical system, including the ventral midbrain (VM) and cortical motor-related areas, exhibited motivation-dependent activity in the premovement "Ready" period when the anticipated monetary reward was displayed. This premovement activity in the mesocortical system correlated only with subsequent peak grip force, whereas the activity in motor-related areas alone was associated with subsequent reaction time and peak grip force. These findings suggest that the mesocortical system linking the VM and motor-related regions plays a role in controlling the peak of force generation indirectly associated with incentives but not the initiation of force generation.

The Japan Monkey Centre Primates Brain Imaging Repository of high-resolution postmortem magnetic resonance imaging: The second phase of the archive of digital records.

A comparison of neuroanatomical features of the brain between humans and our evolutionary relatives, nonhuman primates, is key to understanding the human brain system and the neural basis of mental and neurological disorders. Although most comparative MRI studies of human and nonhuman primate brains have been based on brains of primates that had been used as subjects in experiments, it is essential to investigate various species of nonhuman primates in order to elucidate and interpret the diversity of neuroanatomy features among humans and nonhuman primates. To develop a research platform for this purpose, it is necessary to harmonize the scientific contributions of studies with the standards of animal ethics, animal welfare, and the conservation of brain information for long-term continuation of the field. In previous research, we first developed a gated data-repository of anatomical images obtained using 9.4-T ex vivo MRI of postmortem brain samples from 12 nonhuman primate species, and which are stored at the Japan Monkey Centre. In the present study, as a second phase, we released a collection of T2-weighted images and diffusion tensor images obtained in nine species: white-throated capuchin, Bolivian squirrel monkey, stump-tailed macaque, Tibet monkey, Sykes' monkey, Assamese macaque, pig-tailed macaque, crested macaque, and chimpanzee. Our image repository should facilitate scientific discoveries in the field of comparative neuroscience. This repository can also promote animal ethics and animal welfare in experiments with nonhuman primate models by optimizing methods for in vivo and ex vivo MRI scanning of brains and supporting veterinary neuroradiological education. In addition, the repository is expected to contribute to conservation, preserving information about the brains of various primates, including endangered species, in a permanent digital form.

The dorsal premotor cortex encodes the step-by-step planning processes for goal-directed motor behavior in humans.

The dorsal premotor cortex (PMd) plays an essential role in visually guided goal-directed motor behavior. Although there are several planning processes for achieving goal-directed behavior, the separate neural processes are largely unknown. Here, we created a new visuo-goal task to investigate the step-by-step planning processes for visuomotor and visuo-goal behavior in humans. Using functional magnetic resonance imaging, we found activation in different portions of the bilateral PMd during each processing step. In particular, the activated area for rule-based visuomotor and visuo-goal mapping was located at the ventrorostral portion of the bilateral PMd, that for action plan specification was at the dorsocaudal portion of the left PMd, that for transformation was at the rostral portion of the left PMd, and that for action preparation was at the caudal portion of the bilateral PMd. Thus, the left PMd was involved throughout all of the processes, but the right PMd was involved only in rule-based visuomotor and visuo-goal mapping and action preparation. The locations related to each process were generally spatially separated from each other, but they overlapped partially. These findings revealed that there are functional subregions in the bilateral PMd in humans and these subregions form a functional gradient to achieve goal-directed behavior.

Layer-specific activation in human primary somatosensory cortex during tactile temporal prediction error processing.

The human brain continuously generates predictions of incoming sensory input and calculates corresponding prediction errors from the perceived inputs to update internal predictions. In human primary somatosensory cortex (area 3b), different cortical layers are involved in receiving the sensory input and generation of error signals. It remains unknown, however, how the layers in the human area 3b contribute to the temporal prediction error processing. To investigate prediction error representation in the area 3b across layers, we acquired layer-specific functional magnetic resonance imaging (fMRI) data at 7T from human area 3b during a task of index finger poking with no-delay, short-delay and long-delay touching sequences. We demonstrate that all three tasks increased activity in both superficial and deep layers of area 3b compared to the random sensory input. The fMRI signal was differentially modulated solely in the deep layers rather than the superficial layers of area 3b by the delay time. Compared with the no-delay stimuli, activity was greater in the deep layers of area 3b during the short-delay stimuli but lower during the long-delay stimuli. This difference activity features in the superficial and deep layers suggest distinct functional contributions of area 3b layers to tactile temporal prediction error processing. The functional segregation in area 3b across layers may reflect that the excitatory and inhibitory interplay in the sensory cortex contributions to flexible communication between cortical layers or between cortical areas.

Left parietal involvement in motion sickness susceptibility revealed by multimodal magnetic resonance imaging.

Susceptibility to motion sickness varies greatly across individuals. However, the neural mechanisms underlying this susceptibility remain largely unclear. To address this gap, the current study aimed to identify the neural correlates of motion sickness susceptibility using multimodal MRI. First, we compared resting-state functional connectivity between healthy individuals who were highly susceptible to motion sickness (N = 36) and age/sex-matched controls who showed low susceptibility (N = 36). Seed-based analysis revealed between-group differences in functional connectivity of core vestibular regions in the left posterior Sylvian fissure. A data-driven approach using intrinsic connectivity contrast found greater network centrality of the left intraparietal sulcus in high- rather than in low-susceptible individuals. Moreover, exploratory structural connectivity analysis uncovered an association between motion sickness susceptibility and white matter integrity in the left inferior fronto-occipital fasciculus. Taken together, our data indicate left parietal involvement in motion sickness susceptibility.

The neural representation of facial-emotion categories reflects conceptual structure.

Humans reliably categorize configurations of facial actions into specific emotion categories, leading some to argue that this process is invariant between individuals and cultures. However, growing behavioral evidence suggests that factors such as emotion-concept knowledge may shape the way emotions are visually perceived, leading to variability-rather than universality-in facial-emotion perception. Understanding variability in emotion perception is only emerging, and the neural basis of any impact from the structure of emotion-concept knowledge remains unknown. In a neuroimaging study, we used a representational similarity analysis (RSA) approach to measure the correspondence between the conceptual, perceptual, and neural representational structures of the six emotion categories Anger, Disgust, Fear, Happiness, Sadness, and Surprise. We found that subjects exhibited individual differences in their conceptual structure of emotions, which predicted their own unique perceptual structure. When viewing faces, the representational structure of multivoxel patterns in the right fusiform gyrus was significantly predicted by a subject's unique conceptual structure, even when controlling for potential physical similarity in the faces themselves. Finally, cross-cultural differences in emotion perception were also observed, which could be explained by individual differences in conceptual structure. Our results suggest that the representational structure of emotion expressions in visual face-processing regions may be shaped by idiosyncratic conceptual understanding of emotion categories.

The neural network underpinning social feedback contingent upon one's action: An fMRI study.

Praise enhances motor performance; however, the underlying feedback pathway is unknown. Here, we hypothesized that the social evaluation feedback to the motor system is modified by the top-down effect of the social contingency valuation system, such as the anterior rostral medial prefrontal cortex (arMPFC). We developed a pseudo-interactive task that simplified a conversational student-teacher interaction and conducted a functional magnetic resonance imaging study with 33 participants (13 men, 20 women; mean age = 21.7 years; standard deviation = 2.0 years). The participant inside the scanner uttered the pseudo-English word to the English teacher outside the scanner. The teacher provided feedback of acceptance or rejection by either gestures or words, through video. As a control condition, the pseudo-word was read aloud by a computer. Approval from the teacher enhanced the participants' pleasure rate. Feedback to the participants' utterance, either rejection or acceptance, activated the arMPFC. Irrespective of the preceding utterance by self or computer, acceptance compared with rejection activated the right primary visual cortex (V1), and the reverse activated the left V1. This valence-dependent laterality of V1 activation indicates that the effect is not the domain-general modulation of visual processing. Instead, the early visual cortices are part of the valence-specific representation of the social signal. Physio-physiological interaction analysis with the seed regions in the right and left V1 and the modulator region in the arMPFC showed enhanced connectivity with the bilateral primary motor cortex. These findings indicate that the socially contingent, self-relevant signals from others act as feedback to the motor control system, and this process is mediated by the early visual cortex.

Neural substrates for sharing intention in action during face-to-face imitation.

Face-to-face imitation is a unique social interaction wherein a shared action is executed based on the feedback of the partner. Imitation by the partner is the feedback to the imitatee's action, resulting in sharing actions. The neural mechanisms of the shared representation of action during face-to-face imitation, the core of inter-subjectivity, are not well-known. Here, based on the predictive coding account, we hypothesized that the pair-specific forward internal model is the shared representation of action which is represented by the inter-individual synchronization of some portion of the mirror neuron system. Hyperscanning functional magnetic resonance imaging was conducted during face-to-face interaction in 16 pairs of participants who completed an immediate imitation task of facial expressions. Paired participants were alternately assigned to either an imitator or an imitatee who was prompted to express a happy, sad, or non-emotional face. While neural activation elicited by imitating and being imitated were distinct with little overlap, on-line imitative interaction enhanced inter-brain synchronization in the right inferior parietal lobule that correlated with the similarity in facial movement kinematic profile. This finding indicates a critical role of the right inferior parietal lobule in sharing representation of action as a pair-specific forward internal model through imitative interaction.

Comparative connectomics of the primate social brain.

Social interaction is thought to provide a selection pressure for human intelligence, yet little is known about its neurobiological basis and evolution throughout the primate lineage. Recent advances in neuroimaging have enabled whole brain investigation of brain structure, function, and connectivity in humans and non-human primates (NHPs), leading to a nascent field of comparative connectomics. However, linking social behavior to brain organization across the primates remains challenging. Here, we review the current understanding of the macroscale neural mechanisms of social behaviors from the viewpoint of system neuroscience. We first demonstrate an association between the number of cortical neurons and the size of social groups across primates, suggesting a link between neural information-processing capacity and social capabilities. Moreover, by capitalizing on recent advances in species-harmonized functional MRI, we demonstrate that portions of the mirror neuron system and default-mode networks, which are thought to be important for representation of the other's actions and sense of self, respectively, exhibit similarities in functional organization in macaque monkeys and humans, suggesting possible homologies. With respect to these two networks, we describe recent developments in the neurobiology of social perception, joint attention, personality and social complexity. Together, the Human Connectome Project (HCP)-style comparative neuroimaging, hyperscanning, behavioral, and other multi-modal investigations are expected to yield important insights into the evolutionary foundations of human social behavior.

Frequency-specific task modulation of human brain functional networks: A fast fMRI study.

How coherent neural oscillations are involved in task execution is a fundamental question in neuroscience. Although several electrophysiological studies have tackled this issue, the brain-wide task modulation of neural coherence remains uncharacterized. Here, with a fast fMRI technique, we studied shifts of brain-wide neural coherence across different task states in the ultraslow frequency range (0.01-0.7 Hz). First, we examined whether the shifts of the brain-wide neural coherence occur in a frequency-dependent manner. We quantified the shift of a region's average neural coherence by the inter-state variance of the mean coherence between the region and the rest of the brain. A clustering analysis based on the variance's spatial correlation between frequency components revealed four frequency bands (0.01-0.15 Hz, 0.15-0.37 Hz, 0.37-0.53 Hz, and 0.53-0.7 Hz) showing band-specific shifts of the brain-wide neural coherence. Next, we investigated the similarity of the inter-state variance's spectra between all pairs of regions. We found that regions showing similar spectra correspond to those forming functional modules of the brain network. Then, we investigated the relationship between identified frequency bands and modules' inter-state variances. We found that modules showing the highest variance are those made up of parieto-occipital regions at 0.01-0.15 Hz, while it is replaced with another consisting of frontal regions above 0.15 Hz. Furthermore, these modules showed specific shifting patterns of the mean coherence across states at 0.01-0.15 Hz and above 0.15 Hz, suggesting that identified frequency bands differentially contribute to neural interactions during task execution. Our results highlight that usage of the fast fMRI enables brain-wide investigation of neural coherence up to 0.7 Hz, which opens a promising track for assessment of the large-scale neural interactions in the ultraslow frequency range.

Quantitative Evaluations of Geometrical Distortion Corrections in Cortical Surface-Based Analysis of High-Resolution Functional MRI Data at 7T.

BACKGROUND: Although 7T functional MRI (fMRI) provides better signal-to-noise ratio and higher spatial resolution than 3T fMRI, geometric distortions become more challenging because fMRI is more susceptible to distortions than structural MRI. Accurate alignment of 7T fMRI to structural MRI data is critical for precise cortical surface-based analysis. PURPOSE: To quantify the effectiveness of distortion corrections of 7T fMRI data. STUDY TYPE: Prospective. SUBJECTS: Fifteen healthy individuals aged 19-26 years (mean: 21.9 years). FIELD STRENGTH/SEQUENCE: Multiband gradient-echo echo-planar imaging sequence at 7T; 3D T1 /T2 -weighted sequences (magnetization prepared rapid acquisition with gradient echo [MPRAGE] and sampling perfection with application optimized contrast using different flip angle evolution [SPACE]) at 3T. ASSESSMENT: fMRI data at 7T were registered to cortical surfaces reconstructed from 3T structural data acquired in the same subjects. Distortions induced by B0 inhomogeneity and gradient nonlinearity (B0 and gradient distortions) were evaluated as cortical fallout (misregistration of noncortical areas) and displacement (misregistration along gray matter). STATISTICAL TESTS: Repeated measures analyses of variance with post-hoc t-tests with Bonferroni correction. RESULTS: The accuracy of fully corrected fMRI images based on the intensity distribution was 89.2%. Without any corrections, 9.7% of vertices in the whole surfaces were fallout and the average displacement was 0.96 mm for the rest of the vertices. B0 and gradient distortion corrections significantly reduced the fallout (to 2.1% and 8.7%) and displacement (to 0.29 mm and 0.86 mm). These corrections were effective even around regions with moderate distortions (the somatosensory and visual cortices for B0 distortion, and the anterior frontal, inferior temporal, and posterior occipital cortices for gradient distortion). DATA CONCLUSION: B0 distortion correction is crucial for surface-based analysis of fine-resolution fMRI at 7T. Gradient distortion correction should be considered when regions of interest include regions distant from the isocenter of scanners. EVIDENCE LEVEL: 1 TECHNICAL EFFICACY STAGE: 1.

The Amygdala Network for Processing Itch in Human Brains.

Itch is an unpleasant and aversive somatosensory experience. These negative emotions significantly affect mental health in patients with chronic itch; it is therefore important to understand the brain mechanism of negative emotions due to itch. The amygdala is a key hub of networks regulating negative emotions due to itch. However, the exact network involved in this process is unknown. This study used functional magnetic resonance imaging to investigate the amygdala network processing itch in 25 healthy subjects. Brain activity was measured during electrical itch stimuli using functional magnetic resonance imaging. During itch stimuli the amygdala exhibited increased functional connectivity with key brain regions of the serotonergic system responsible for negative emotions (the medial habenula and the median raphe nucleus) and with the memory system, which is responsible for consolidating emotional experiences (the parahippocampus and perirhinal cortex). The serotonergic and memory systems may become therapeutic targets to prevent or reduce diminished mental health commonly seen in chronic itch patients.

Brain networks underlying tactile softness perception: A functional magnetic resonance imaging study.

Humans are adept at perceiving physical properties of an object through touch. Tangible object properties can be categorized into two types: macro-spatial properties, including shape and orientation; and material properties, such as roughness, softness, and temperature. Previous neuroimaging studies have shown that roughness and temperature are extracted at nodes of a network, such as that involving the parietal operculum and insula, which is different from the network engaged in processing macro-spatial properties. However, it is unclear whether other perceptual dimensions pertaining to material properties engage the same regions. Here, we conducted a functional magnetic resonance imaging study to test whether the parietal operculum and insula were involved in extracting tactually-perceived softness magnitude. Fifty-six healthy right-handed participants estimated perceived softness magnitude using their right middle finger. We presented three stimuli that had the same shape but different compliances. The force applied to the finger was manipulated at two levels. Classical mass-univariate analysis showed that activity in the parietal operculum, insula, and medial prefrontal cortex was positively associated with perceived softness magnitude, regardless of the applied force. Softness-related activity was stronger in the ventral striatum in the high-force condition than in the low-force condition. The multivariate voxel pattern analysis showed higher accuracy than chance levels and control regions in the parietal operculum/insula, postcentral gyrus, posterior parietal lobule, and middle occipital gyrus. These results indicate that a distributed set of the brain regions, including the parietal operculum and insula, is involved in representing perceived softness.

Neural correlates of online cooperation during joint force production.

During joint action, two or more persons depend on each other to accomplish a goal. This mutual recursion, or circular dependency, is one of the characteristics of cooperation. To evaluate the neural substrates of cooperation, we conducted a hyperscanning functional MRI study in which 19 dyads performed a joint force-production task. The goal of the task was to match their average grip forces to the target value (20% of their maximum grip forces) through visual feedback over a 30-s period; the task required taking into account other-produced force to regulate the self-generated one in real time, which represented cooperation. Time-series data of the dyad's exerted grip forces were recorded, and the noise contribution ratio (NCR), a measure of influence from the partner, was computed using a multivariate autoregressive model to identify the degree to which each participant's grip force was explained by that of their partner's, i.e., the degree of cooperation. Compared with the single force-production task, the joint task enhanced the NCR and activated the mentalizing system, including the medial prefrontal cortex, precuneus, and bilateral posterior subdivision of the temporoparietal junction (TPJ). In addition, specific activation of the anterior subdivision of the right TPJ significantly and positively correlated with the NCR across participants during the joint task. The effective connectivity of the anterior to posterior TPJ was upregulated when participants coordinated their grip forces. Finally, the joint task enhanced cross-brain functional connectivity of the right anterior TPJ, indicating shared attention toward the temporal patterns of the motor output of the partner. Since the posterior TPJ is part of the mentalizing system for tracking the intention of perceived agents, our findings indicate that cooperation, i.e., the degree of adjustment of individual motor output depending on that of the partner, is mediated by the interconnected subdivisions of the right TPJ.

Cross-cultural similarity in relationship-specific social touching.

Many species use touching for reinforcing social structures, and particularly, non-human primates use social grooming for managing their social networks. However, it is still unclear how social touch contributes to the maintenance and reinforcement of human social networks. Human studies in Western cultures suggest that the body locations where touch is allowed are associated with the strength of the emotional bond between the person touched and the toucher. However, it is unknown to what extent this relationship is culturally universal and generalizes to non-Western cultures. Here, we compared relationship-specific, bodily touch allowance maps across one Western ( N = 386, UK) and one East Asian ( N = 255, Japan) country. In both cultures, the strength of the emotional bond was linearly associated with permissible touch area. However, Western participants experienced social touching as more pleasurable than Asian participants. These results indicate a similarity of emotional bonding via social touch between East Asian and Western cultures.

Brain networks underlying conscious tactile perception of textures as revealed using the velvet hand illusion.

Humans are adept at perceiving textures through touch. Previous neuroimaging studies have identified a distributed network of brain regions involved in the tactile perception of texture. However, it remains unclear how nodes in this network contribute to the tactile awareness of texture. To examine the hypothesis that such awareness involves the interaction of the primary somatosensory cortex with higher order cortices, we conducted a functional magnetic resonance imaging (fMRI) study utilizing the velvet hand illusion, in which an illusory velvet-like surface is perceived between the hands. Healthy participants were subjected to a strong illusion, a weak illusion, and tactile perception of real velvet. The strong illusion induced greater activation in the primary somatosensory cortex (S1) than the weak illusion, and increases in such activation were positively correlated with the strength of the illusion. Furthermore, both actual and illusory perception of velvet induced common activation in S1. Psychophysiological interaction (PPI) analysis revealed that the strength of the illusion modulated the functional connectivity of S1 with each of the following regions: the parietal operculum, superior parietal lobule, precentral gyrus, insula, and cerebellum. The present results indicate that S1 is associated with the conscious tactile perception of textures, which may be achieved via interactions with higher order somatosensory areas.

Correction: Time Adaptation Shows Duration Selectivity in the Human Parietal Cortex.

[This corrects the article DOI: 10.1371/journal.pbio.1002262.].

Time Adaptation Shows Duration Selectivity in the Human Parietal Cortex.

Although psychological and computational models of time estimation have postulated the existence of neural representations tuned for specific durations, empirical evidence of this notion has been lacking. Here, using a functional magnetic resonance imaging (fMRI) adaptation paradigm, we show that the inferior parietal lobule (IPL) (corresponding to the supramarginal gyrus) exhibited reduction in neural activity due to adaptation when a visual stimulus of the same duration was repeatedly presented. Adaptation was strongest when stimuli of identical durations were repeated, and it gradually decreased as the difference between the reference and test durations increased. This tuning property generalized across a broad range of durations, indicating the presence of general time-representation mechanisms in the IPL. Furthermore, adaptation was observed irrespective of the subject's attention to time. Repetition of a nontemporal aspect of the stimulus (i.e., shape) did not produce neural adaptation in the IPL. These results provide neural evidence for duration-tuned representations in the human brain.