Chronotopic maps in human supplementary motor area.

Time is a fundamental dimension of everyday experiences. We can unmistakably sense its passage and adjust our behavior accordingly. Despite its ubiquity, the neuronal mechanisms underlying the capacity to perceive time remains unclear. Here, in two experiments using ultrahigh-field 7-Tesla (7T) functional magnetic resonance imaging (fMRI), we show that in the medial premotor cortex (supplementary motor area [SMA]) of the human brain, neural units tuned to different durations are orderly mapped in contiguous portions of the cortical surface so as to form chronomaps. The response of each portion in a chronomap is enhanced by neighboring durations and suppressed by nonpreferred durations represented in distant portions of the map. These findings suggest duration-sensitive tuning as a possible neural mechanism underlying the recognition of time and demonstrate, for the first time, that the representation of an abstract feature such as time can be instantiated by a topographical arrangement of duration-sensitive neural populations.

A Technical Critique of Some Parts of the Free Energy Principle.

We summarize the original formulation of the free energy principle and highlight some technical issues. We discuss how these issues affect related results involving generalised coordinates and, where appropriate, mention consequences for and reveal, up to now unacknowledged, differences from newer formulations of the free energy principle. In particular, we reveal that various definitions of the "Markov blanket" proposed in different works are not equivalent. We show that crucial steps in the free energy argument, which involve rewriting the equations of motion of systems with Markov blankets, are not generally correct without additional (previously unstated) assumptions. We prove by counterexamples that the original free energy lemma, when taken at face value, is wrong. We show further that this free energy lemma, when it does hold, implies the equality of variational density and ergodic conditional density. The interpretation in terms of Bayesian inference hinges on this point, and we hence conclude that it is not sufficiently justified. Additionally, we highlight that the variational densities presented in newer formulations of the free energy principle and lemma are parametrised by different variables than in older works, leading to a substantially different interpretation of the theory. Note that we only highlight some specific problems in the discussed publications. These problems do not rule out conclusively that the general ideas behind the free energy principle are worth pursuing.

Response time in economic games reflects different types of decision conflict for prosocial and proself individuals.

Behavioral and neuroscientific studies explore two pathways through which internalized social norms promote prosocial behavior. One pathway involves internal control of impulsive selfishness, and the other involves emotion-based prosocial preferences that are translated into behavior when they evade cognitive control for pursuing self-interest. We measured 443 participants' overall prosocial behavior in four economic games. Participants' predispositions [social value orientation (SVO)] were more strongly reflected in their overall game behavior when they made decisions quickly than when they spent a longer time. Prosocially (or selfishly) predisposed participants behaved less prosocially (or less selfishly) when they spent more time in decision making, such that their SVO prosociality yielded limited effects in actual behavior in their slow decisions. The increase (or decrease) in slower decision makers was prominent among consistent prosocials (or proselfs) whose strong preference for prosocial (or proself) goals would make it less likely to experience conflict between prosocial and proself goals. The strong effect of RT on behavior in consistent prosocials (or proselfs) suggests that conflict between prosocial and selfish goals alone is not responsible for slow decisions. Specifically, we found that contemplation of the risk of being exploited by others (social risk aversion) was partly responsible for making consistent prosocials (but not consistent proselfs) spend longer time in decision making and behave less prosocially. Conflict between means rather than between goals (immediate versus strategic pursuit of self-interest) was suggested to be responsible for the time-related increase in consistent proselfs' prosocial behavior. The findings of this study are generally in favor of the intuitive cooperation model of prosocial behavior.

Cortical thickness of the dorsolateral prefrontal cortex predicts strategic choices in economic games.

Human prosociality has been traditionally explained in the social sciences in terms of internalized social norms. Recent neuroscientific studies extended this traditional view of human prosociality by providing evidence that prosocial choices in economic games require cognitive control of the impulsive pursuit of self-interest. However, this view is challenged by an intuitive prosociality view emphasizing the spontaneous and heuristic basis of prosocial choices in economic games. We assessed the brain structure of 411 players of an ultimatum game (UG) and a dictator game (DG) and measured the strategic reasoning ability of 386. According to the reflective norm-enforcement view of prosociality, only those capable of strategically controlling their selfish impulses give a fair share in the UG, but cognitive control capability should not affect behavior in the DG. Conversely, we support the intuitive prosociality view by showing for the first time, to our knowledge, that strategic reasoning and cortical thickness of the dorsolateral prefrontal cortex were not related to giving in the UG but were negatively related to giving in the DG. This implies that the uncontrolled choice in the DG is prosocial rather than selfish, and those who have a thicker dorsolateral prefrontal cortex and are capable of strategic reasoning (goal-directed use of the theory of mind) control this intuitive drive for prosociality as a means to maximize reward when there are no future implications of choices.

Visual Perceptual Echo Reflects Learning of Regularities in Rapid Luminance Sequences.

A novel neural signature of active visual processing has recently been described in the form of the "perceptual echo", in which the cross-correlation between a sequence of randomly fluctuating luminance values and occipital electrophysiological signals exhibits a long-lasting periodic (∼100 ms cycle) reverberation of the input stimulus (VanRullen and Macdonald, 2012). As yet, however, the mechanisms underlying the perceptual echo and its function remain unknown. Reasoning that natural visual signals often contain temporally predictable, though nonperiodic features, we hypothesized that the perceptual echo may reflect a periodic process associated with regularity learning. To test this hypothesis, we presented subjects with successive repetitions of a rapid nonperiodic luminance sequence, and examined the effects on the perceptual echo, finding that echo amplitude linearly increased with the number of presentations of a given luminance sequence. These data suggest that the perceptual echo reflects a neural signature of regularity learning.Furthermore, when a set of repeated sequences was followed by a sequence with inverted luminance polarities, the echo amplitude decreased to the same level evoked by a novel stimulus sequence. Crucially, when the original stimulus sequence was re-presented, the echo amplitude returned to a level consistent with the number of presentations of this sequence, indicating that the visual system retained sequence-specific information, for many seconds, even in the presence of intervening visual input. Altogether, our results reveal a previously undiscovered regularity learning mechanism within the human visual system, reflected by the perceptual echo.SIGNIFICANCE STATEMENT How the brain encodes and learns fast-changing but nonperiodic visual input remains unknown, even though such visual input characterizes natural scenes. We investigated whether the phenomenon of "perceptual echo" might index such learning. The perceptual echo is a long-lasting reverberation between a rapidly changing visual input and evoked neural activity, apparent in cross-correlations between occipital EEG and stimulus sequences, peaking in the alpha (∼10 Hz) range. We indeed found that perceptual echo is enhanced by repeatedly presenting the same visual sequence, indicating that the human visual system can rapidly and automatically learn regularities embedded within fast-changing dynamic sequences. These results point to a previously undiscovered regularity learning mechanism, operating at a rate defined by the alpha frequency.

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.

Efficient Algorithms for Searching the Minimum Information Partition in Integrated Information Theory.

The ability to integrate information in the brain is considered to be an essential property for cognition and consciousness. Integrated Information Theory (IIT) hypothesizes that the amount of integrated information ( Φ ) in the brain is related to the level of consciousness. IIT proposes that, to quantify information integration in a system as a whole, integrated information should be measured across the partition of the system at which information loss caused by partitioning is minimized, called the Minimum Information Partition (MIP). The computational cost for exhaustively searching for the MIP grows exponentially with system size, making it difficult to apply IIT to real neural data. It has been previously shown that, if a measure of Φ satisfies a mathematical property, submodularity, the MIP can be found in a polynomial order by an optimization algorithm. However, although the first version of Φ is submodular, the later versions are not. In this study, we empirically explore to what extent the algorithm can be applied to the non-submodular measures of Φ by evaluating the accuracy of the algorithm in simulated data and real neural data. We find that the algorithm identifies the MIP in a nearly perfect manner even for the non-submodular measures. Our results show that the algorithm allows us to measure Φ in large systems within a practical amount of time.

Predictions Shape Confidence in Right Inferior Frontal Gyrus.

It is clear that prior expectations shape perceptual decision-making, yet their contribution to the construction of subjective decision confidence remains largely unexplored. We recorded fMRI data while participants made perceptual decisions and confidence judgments, manipulating perceptual prior expectations while controlling for potential confounds of attention. Results show that subjective confidence increases as expectations increasingly support the decision, and that this relationship is associated with BOLD activity in right inferior frontal gyrus (rIFG). Specifically, rIFG is sensitive to the discrepancy between expectation and decision (mismatch), and higher mismatch responses are associated with lower decision confidence. Connectivity analyses revealed expectancy information to be represented in bilateral orbitofrontal cortex and sensory signals to be represented in intracalcarine sulcus. Together, our results indicate that predictive information is integrated into subjective confidence in rIFG, and reveal an occipital-frontal network that constructs confidence from top-down and bottom-up signals. This interpretation was further supported by exploratory findings that the white matter density of right orbitofrontal cortex negatively predicted its respective contribution to the construction of confidence. Our findings advance our understanding of the neural basis of subjective perceptual processes by revealing an occipitofrontal functional network that integrates prior beliefs into the construction of confidence. SIGNIFICANCE STATEMENT: Perceptual decision-making is typically conceived as an integration of bottom-up and top-down influences. However, perceptual decisions are accompanied by a sense of confidence. Confidence is an important facet of perceptual consciousness yet remains poorly understood. Here we implicate right inferior frontal gyrus in constructing confidence from the discrepancy between perceptual judgment and its prior probability. Furthermore, we place right inferior frontal gyrus within an occipitofrontal network, consisting of orbitofrontal cortex and intracalcarine sulcus, which represents and communicates relevant top-down and bottom-up signals. Together, our data reveal a role of frontal regions in the top-down processes enabling perceptual decisions to become available for conscious report.

Discrete capacity limits and neuroanatomical correlates of visual short-term memory for objects and spatial locations.

Working memory is responsible for keeping information in mind when it is no longer in view, linking perception with higher cognitive functions. Despite such crucial role, short-term maintenance of visual information is severely limited. Research suggests that capacity limits in visual short-term memory (VSTM) are correlated with sustained activity in distinct brain areas. Here, we investigated whether variability in the structure of the brain is reflected in individual differences of behavioral capacity estimates for spatial and object VSTM. Behavioral capacity estimates were calculated separately for spatial and object information using a novel adaptive staircase procedure and were found to be unrelated, supporting domain-specific VSTM capacity limits. Voxel-based morphometry (VBM) analyses revealed dissociable neuroanatomical correlates of spatial versus object VSTM. Interindividual variability in spatial VSTM was reflected in the gray matter density of the inferior parietal lobule. In contrast, object VSTM was reflected in the gray matter density of the left insula. These dissociable findings highlight the importance of considering domain-specific estimates of VSTM capacity and point to the crucial brain regions that limit VSTM capacity for different types of visual information. Hum Brain Mapp 38:767-778, 2017. © 2016 Wiley Periodicals, Inc.

The Uniformity Illusion.

Vision in the fovea, the center of the visual field, is much more accurate and detailed than vision in the periphery. This is not in line with the rich phenomenology of peripheral vision. Here, we investigated a visual illusion that shows that detailed peripheral visual experience is partially based on a reconstruction of reality. Participants fixated on the center of a visual display in which central stimuli differed from peripheral stimuli. Over time, participants perceived that the peripheral stimuli changed to match the central stimuli, so that the display seemed uniform. We showed that a wide range of visual features, including shape, orientation, motion, luminance, pattern, and identity, are susceptible to this uniformity illusion. We argue that the uniformity illusion is the result of a reconstruction of sparse visual information (from the periphery) based on more readily available detailed visual information (from the fovea), which gives rise to a rich, but illusory, experience of peripheral vision.

Larger Stimuli Require Longer Processing Time for Perception.

The time it takes for a stimulus to reach awareness is often assessed by measuring reaction times (RTs) or by a temporal order judgement (TOJ) task in which perceived timing is compared against a reference stimulus. Dissociations of RT and TOJ have been reported earlier in which increases in stimulus intensity such as luminance intensity results in a decrease of RT, whereas perceived perceptual latency in a TOJ task is affected to a lesser degree. Here, we report that a simple manipulation of stimulus size has stronger effects on perceptual latency measured by TOJ than on motor latency measured by RT tasks. When participants were asked to respond to the appearance of a simple stimulus such as a luminance blob, the perceptual latency measured against a standard reference stimulus was up to 40 ms longer for a larger stimulus. In other words, the smaller stimulus was perceived to occur earlier than the larger one. RT on the other hand was hardly affected by size. The TOJ results were further replicated in a simultaneity judgement task, suggesting that the effects of size are not due to TOJ-specific response biases but more likely reflect an effect on perceived timing.

Rhythmic Influence of Top-Down Perceptual Priors in the Phase of Prestimulus Occipital Alpha Oscillations.

Prior expectations have a powerful influence on perception, biasing both decision and confidence. However, how this occurs at the neural level remains unclear. It has been suggested that spontaneous alpha-band neural oscillations represent rhythms of the perceptual system that periodically modulate perceptual judgments. We hypothesized that these oscillations instantiate the effects of expectations. While collecting scalp EEG, participants performed a detection task that orthogonally manipulated perceptual expectations and attention. Trial-by-trial retrospective confidence judgments were also collected. Results showed that, independent of attention, prestimulus occipital alpha phase predicted the weighting of expectations on yes/no decisions. Moreover, phase predicted the influence of expectations on confidence. Thus, expectations periodically bias objective and subjective perceptual decision-making together before stimulus onset. Our results suggest that alpha-band neural oscillations periodically transmit prior evidence to visual cortex, changing the baseline from which evidence accumulation begins. In turn, our results inform accounts of how expectations shape early visual processing.

The structural basis of inter-individual differences in human behaviour and cognition.

Inter-individual variability in perception, thought and action is frequently treated as a source of 'noise' in scientific investigations of the neural mechanisms that underlie these processes, and discarded by averaging data from a group of participants. However, recent MRI studies in the human brain show that inter-individual variability in a wide range of basic and higher cognitive functions - including perception, motor control, memory, aspects of consciousness and the ability to introspect - can be predicted from the local structure of grey and white matter as assessed by voxel-based morphometry or diffusion tensor imaging. We propose that inter-individual differences can be used as a source of information to link human behaviour and cognition to brain anatomy.

Parietal theta burst TMS: Functional fractionation observed during bistable perception not evident in attention tasks.

When visual input is ambiguous, perception spontaneously alternates between interpretations: bistable perception. Studies have identified two distinct sites near the right intraparietal sulcus where inhibitory transcranial magnetic stimulation (TMS) affects the frequency of occurrence of these alternations, but strikingly with opposite directions of effect for the two sites. Lesion and TMS studies on spatial and sustained attention have also indicated a parcellation of right parietal cortex, into areas serving distinct attentional functions. We used the exact TMS procedure previously employed to affect bistable perception, yet measured its effect on spatial and sustained attention tasks. Although there was a trend for TMS to affect performance, trends were consistently similar for both parietal sites, with no indication of opposite effects. We interpret this as signifying that the previously observed parietal fractionation of function regarding the perception of ambiguous stimuli is not due to TMS-induced modification of spatial or sustained attention.

Transcranial Direct Current Stimulation of the Motor Cortex Biases Action Choice in a Perceptual Decision Task.

One of the multiple interacting systems involved in the selection and execution of voluntary actions is the primary motor cortex (PMC). We aimed to investigate whether the transcranial direct current stimulation (tDCS) of this area can modulate hand choice. A perceptual decision-making task was administered. Participants were asked to classify rectangles with different height-to-width ratios into horizontal and vertical rectangles using their right and left index fingers while their PMC was stimulated either bilaterally or unilaterally. Two experiments were conducted with different stimulation conditions: the first experiment (n = 12) had only one stimulation condition (bilateral stimulation), and the second experiment (n = 45) had three stimulation conditions (bilateral, anodal unilateral, and cathodal unilateral stimulations). The second experiment was designed to confirm the results of the first experiment and to further investigate the effects of anodal and cathodal stimulations alone in the observed effects. Each participant took part in two sessions. The laterality of stimulation was reversed over the two sessions. Our results showed that anodal stimulation of the PMC biases participants' responses toward using the contralateral hand whereas cathodal stimulation biases responses toward the ipsilateral hand. Brain stimulation also modulated the RT of the left hand in all stimulation conditions: Responses were faster when the response bias was in favor of the left hand and slower when the response bias was against it. We propose two possible explanations for these findings: the perceptual bias account (bottom-up effects of stimulation on perception) and the motor-choice bias account (top-down modulation of the decision-making system by facilitation of response in one hand over the other). We conclude that motor responses and the choice of hand can be modulated using tDCS.

Brain activity dynamics in human parietal regions during spontaneous switches in bistable perception.

The neural mechanisms underlying conscious visual perception have been extensively investigated using bistable perception paradigms. Previous functional magnetic resonance imaging (fMRI) and transcranial magnetic stimulation (TMS) studies suggest that the right anterior superior parietal (r-aSPL) and the right posterior superior parietal lobule (r-pSPL) have opposite roles in triggering perceptual reversals. It has been proposed that these two areas are part of a hierarchical network whose dynamics determine perceptual switches. However, how these two parietal regions interact with each other and with the rest of the brain during bistable perception is not known. Here, we investigated such a model by recording brain activity using fMRI while participants viewed a bistable structure-from-motion stimulus. Using dynamic causal modeling (DCM), we found that resolving such perceptual ambiguity was specifically associated with reciprocal interactions between these parietal regions and V5/MT. Strikingly, the strength of bottom-up coupling between V5/MT to r-pSPL and from r-pSPL to r-aSPL predicted individual mean dominance duration. Our findings are consistent with a hierarchical predictive coding model of parietal involvement in bistable perception and suggest that visual information processing underlying spontaneous perceptual switches can be described as changes in connectivity strength between parietal and visual cortical regions.

Cross-modal prediction changes the timing of conscious access during the motion-induced blindness.

Despite accumulating evidence that perceptual predictions influence perceptual content, the relations between these predictions and conscious contents remain unclear, especially for cross-modal predictions. We examined whether predictions of visual events by auditory cues can facilitate conscious access to the visual stimuli. We trained participants to learn associations between auditory cues and colour changes. We then asked whether congruency between auditory cues and target colours would speed access to consciousness. We did this by rendering a visual target subjectively invisible using motion-induced blindness and then gradually changing its colour while presenting congruent or incongruent auditory cues. Results showed that the visual target gained access to consciousness faster in congruent than in incongruent trials; control experiments excluded potentially confounding effects of attention and motor response. The expectation effect was gradually established over blocks suggesting a role for extensive training. Overall, our findings show that predictions learned through cross-modal training can facilitate conscious access to visual stimuli.

Selectively altering belief formation in the human brain.

Humans form beliefs asymmetrically; we tend to discount bad news but embrace good news. This reduced impact of unfavorable information on belief updating may have important societal implications, including the generation of financial market bubbles, ill preparedness in the face of natural disasters, and overly aggressive medical decisions. Here, we selectively improved people's tendency to incorporate bad news into their beliefs by disrupting the function of the left (but not right) inferior frontal gyrus using transcranial magnetic stimulation, thereby eliminating the engrained "good news/bad news effect." Our results provide an instance of how selective disruption of regional human brain function paradoxically enhances the ability to incorporate unfavorable information into beliefs of vulnerability.