Intracranial recordings show evidence of numerosity tuning in human parietal cortex.

Numerosity is the set size of a group of items. Numerosity perception is a trait shared across numerous species. Numerosity-selective neural populations are thought to underlie numerosity perception. These neurons have been identified primarily using electrical recordings in animal models and blood oxygen level dependent (BOLD) functional magnetic resonance imaging (fMRI) in humans. Here we use electrical intracranial recordings to investigate numerosity tuning in humans, focusing on high-frequency transient activations. These recordings combine a high spatial and temporal resolution and can bridge the gap between animal models and human recordings. In line with previous studies, we find numerosity-tuned responses at parietal sites in two out of three participants. Neuronal populations at these locations did not respond to other visual stimuli, i.e. faces, houses, and letters, in contrast to several occipital sites. Our findings further corroborate the specificity of numerosity tuning of in parietal cortex, and further link fMRI results and electrophysiological recordings.

A population receptive field model of the magnetoencephalography response.

Computational models which predict the neurophysiological response from experimental stimuli have played an important role in human neuroimaging. One type of computational model, the population receptive field (pRF), has been used to describe cortical responses at the millimeter scale using functional magnetic resonance imaging (fMRI) and electrocorticography (ECoG). However, pRF models are not widely used for non-invasive electromagnetic field measurements (EEG/MEG), because individual sensors pool responses originating from several centimeter of cortex, containing neural populations with widely varying spatial tuning. Here, we introduce a forward-modeling approach in which pRFs estimated from fMRI data are used to predict MEG sensor responses. Subjects viewed contrast-reversing bar stimuli sweeping across the visual field in separate fMRI and MEG sessions. Individual subject's pRFs were modeled on the cortical surface at the millimeter scale using the fMRI data. We then predicted cortical time series and projected these predictions to MEG sensors using a biophysical MEG forward model, accounting for the pooling across cortex. We compared the predicted MEG responses to observed visually evoked steady-state responses measured in the MEG session. We found that pRF parameters estimated by fMRI could explain a substantial fraction of the variance in steady-state MEG sensor responses (up to 60% in individual sensors). Control analyses in which we artificially perturbed either pRF size or pRF position reduced MEG prediction accuracy, indicating that MEG data are sensitive to pRF properties derived from fMRI. Our model provides a quantitative approach to link fMRI and MEG measurements, thereby enabling advances in our understanding of spatiotemporal dynamics in human visual field maps.

Body-Space Interactions: Same Spatial Encoding but Different Influence of Valence for Reaching and Defensive Purposes.

The space around our body, the so-called peripersonal space, is where interactions with nearby objects may occur. "Defensive space" and "Reaching space", respectively, refer to two opposite poles of interaction between our body and the external environment: protecting the body and performing a goal-directed action. Here, we hypothesized that mechanisms underlying these two action spaces are differentially modulated by the valence of visual stimuli, as stimuli with negative valence are more likely to activate protective actions whereas stimuli with positive valence may activate approaching actions. To test whether such distinction in cognitive/evaluative processing exists between Reaching and Defensive spaces, we measured behavioral responses as well as neural activations over sensorimotor cortex using EEG while participants performed several tasks designed to tap into mechanisms underlying either Defensive (e.g., respond to touch) or Reaching space (e.g., estimate whether object is within reaching distance). During each task, pictures of objects with either positive or negative valence were presented at different distances from the participants' body. We found that Defensive space was smaller for positively compared with negatively valenced visual stimuli. Furthermore, sensorimotor cortex activation (reflected in modulation of beta power) during tactile processing was enhanced when coupled with negatively rather than positively valenced visual stimuli regarding Defensive space. On the contrary, both the EEG and behavioral measures capturing the mechanisms underlying Reaching space did not reveal any modulation by valence. Thus, although valence encoding had differential effects on Reaching and Defensive spaces, the distance of the visual stimulus modulated behavioral measures as well as activity over sensorimotor cortex (reflected in modulations of mu power) in a similar way for both types of spaces. Our results are compatible with the idea that Reaching and Defensive spaces involve the same distance-dependent neural representations of sensory input, whereas task goals and stimulus valence (i.e., contextual information) are implemented at a later processing stage and exert an influence on motor output rather than sensory/space encoding.

Intracranial Recordings Reveal Unique Shape and Timing of Responses in Human Visual Cortex during Illusory Visual Events.

During binocular rivalry, perception spontaneously changes without any alteration to the visual stimulus. What neural events bring about this illusion that a constant stimulus is changing? We recorded from intracranial electrodes placed on the occipital and posterior temporal cortex of two patients with epilepsy while they experienced illusory changes of a face-house binocular-rivalry stimulus or observed a control stimulus that physically changed. We performed within-patient comparisons of broadband high-frequency responses, focusing on single epochs recorded along the ventral processing stream. We found transient face- and house-selective responses localized to the same electrodes for illusory and physical changes, but the temporal characteristics of these responses markedly differed. In comparison with physical changes, responses to illusory changes were longer lasting, in particular exhibiting a characteristic slow rise. Furthermore, the temporal order of responses across the visual hierarchy was reversed for illusory as compared to physical changes: for illusory changes, higher order fusiform and parahippocampal regions responded before lower order occipital regions. Our tentative interpretation of these findings is that two stages underlie the initiation of illusory changes: a destabilization stage in which activity associated with the impending change gradually accumulates across the visual hierarchy, ultimately graduating in a top-down cascade of activity that may stabilize the new perceptual interpretation of the stimulus.

The influence of joint attention and partner trustworthiness on cross-modal sensory cueing.

Joint attention refers to the coordinated attention between social partners to an object of shared interest, usually involving shared gaze toward the object. In the laboratory, however, joint attention is often investigated using computerized gaze cueing tasks that do not allow shared gaze. Instead, these computerized tasks require the participant to maintain fixation on the virtual partner's face, while the partner gazes to the left or right. Here we designed a modified gaze cueing task that better simulates a natural joint attention episode by allowing shared gaze, while still maintaining tight experimental control. In our computerized task the participant's gaze and the gaze of a virtual partner were manipulated independently, resulting in shared or unshared gaze. Following each gaze shift of the virtual partner a touch stimulus was delivered on one of the cheeks of the participant. We analyzed behavioral and neural (electro-encephalography) responses to the touch. Faster reaction-times and stronger lateralization of alpha power were observed when the touched cheek was in a jointly attended hemispace compared with a singly attended or unattended hemispace. Importantly, these effects were unique to joint attention and could not be explained as the additive effects of own gaze and gaze cue direction. Underlining its social nature, we found that the behavioral effect was absent when we repeated our experiment with nonsocial cues (arrows) instead of gaze cues. Furthermore, when we compared trustworthy with untrustworthy virtual partners (trustworthiness judgements based on facial appearance) we found the effect only for trustworthy and not for untrustworthy virtual partners. We conclude that joint attention based on shared gaze influences attentional orienting such that cross-modal sensory processing at the jointly attended location is facilitated, particularly when the partner is trustworthy. This indicates that social interactions and trustworthiness judgements affect cortical and behavioral responses to sensory information.

Intracranial Recordings of Occipital Cortex Responses to Illusory Visual Events.

UNLABELLED: Ambiguous visual stimuli elicit different perceptual interpretations over time, creating the illusion that a constant stimulus is changing. We investigate whether such spontaneous changes in visual perception involve occipital brain regions specialized for processing visual information, despite the absence of concomitant changes in stimulation. Spontaneous perceptual changes observed while viewing a binocular rivalry stimulus or an ambiguous structure-from-motion stimulus were compared with stimulus-induced perceptual changes that occurred in response to an actual stimulus change. Intracranial recordings from human occipital cortex revealed that spontaneous and stimulus-induced perceptual changes were both associated with an early transient increase in high-frequency power that was more spatially confined than a later transient decrease in low-frequency power. We suggest that the observed high-frequency and low-frequency modulations relate to initiation and maintenance of a percept, respectively. Our results are compatible with the idea that spontaneous changes in perception originate from competitive interactions within visual neural networks. SIGNIFICANCE STATEMENT: Ambiguous visual stimuli elicit different perceptual interpretations over time, creating the illusion that a constant stimulus is changing. The literature on the neural correlates of conscious visual perception remains inconclusive regarding the extent to which such spontaneous changes in perception involve sensory brain regions. In an attempt to bridge the gap between existing animal and human studies, we recorded from intracranial electrodes placed on the human occipital lobe. We compared two different kinds of ambiguous stimuli, binocular rivalry and the phenomenon of ambiguous structure-from-motion, enabling generalization of our findings across different stimuli. Our results indicate that spontaneous and stimulus-induced changes in perception (i.e., "illusory" and "real" changes in the stimulus, respectively) may involve sensory regions to a similar extent.

Implicit perceptual memory modulates early visual processing of ambiguous images.

The way we perceive the present visual environment is influenced by past visual experiences. Here we investigated the neural basis of such experience dependency. We repeatedly presented human observers with an ambiguous visual stimulus (structure-from-motion) that can give rise to two distinct perceptual interpretations. Past visual experience is known to influence the perception of such stimuli. We recorded fast dynamics of neural activity shortly after stimulus onset using event-related electroencephalography. The number of previous occurrences of a certain percept modulated early posterior brain activity starting as early as 50 ms after stimulus onset. This modulation developed across hundreds of percept repetitions, reflecting several minutes of accumulating perceptual experience. Importantly, there was no such modulation when the mere number of previous stimulus presentations was considered regardless of how they were perceived. This indicates that the effect depended on previous perception rather than previous visual input. The short latency and posterior scalp location of the effect suggest that perceptual history modified bottom-up stimulus processing in early visual cortex. We propose that bottom-up neural responses to a given visual presentation are shaped, in part, by feedback modulation that occurred during previous presentations, thus allowing these responses to be biased in light of previous perceptual decisions.

Perceptual experience modulates cortical circuits involved in visual awareness.

Successful interactions with the environment entail interpreting ambiguous sensory information. To address this challenge it has been suggested that the brain optimizes performance through experience. Here we used functional magnetic resonance imaging (fMRI) to investigate whether perceptual experience modulates the cortical circuits involved in visual awareness. Using ambiguous visual stimuli (binocular rivalry or ambiguous structure-from-motion) we were able to disentangle the co-occurring influences of stimulus repetition and perceptual repetition. For both types of ambiguous stimuli we observed that the mere repetition of the stimulus evoked an entirely different pattern of activity modulations than the repetition of a particular perceptual interpretation of the stimulus. Regarding stimulus repetition, decreased fMRI responses were evident during binocular rivalry but weaker during 3-D motion rivalry. Perceptual repetition, on the other hand, entailed increased activity in stimulus-specific visual brain regions - for binocular rivalry in the early visual regions and for ambiguous structure-from-motion in both early as well as higher visual regions. This indicates that the repeated activation of a visual network mediating a particular percept facilitated its later reactivation. Perceptual repetition was also associated with a response change in the parietal cortex that was similar for the two types of ambiguous stimuli, possibly relating to the temporal integration of perceptual information. We suggest that perceptual repetition is associated with a facilitation of neural activity within and between percept-specific visual networks and parietal networks involved in the temporal integration of perceptual information, thereby enhancing the stability of previously experienced percepts.

On the functional relevance of frontal cortex for passive and voluntarily controlled bistable vision.

In bistable vision, one constant ambiguous stimulus leads to 2 alternating conscious percepts. This perceptual switching occurs spontaneously but can also be influenced through voluntary control. Neuroimaging studies have reported that frontal regions are activated during spontaneous perceptual switches, leading some researchers to suggest that frontal regions causally induce perceptual switches. But the opposite also seems possible: frontal activations may themselves be caused by spontaneous switches. Classically implicated in attentional processes, these same regions are also candidates for the origins of voluntary control over bistable vision. Here too, it remains unknown whether frontal cortex is actually functionally relevant. It is even possible that spontaneous perceptual switches and voluntarily induced switches are mediated by the same top-down mechanisms. To directly address these issues, we here induced "virtual lesions," with transcranial magnetic stimulation, in frontal, parietal, and 2 lower level visual cortices using an established ambiguous structure-from-motion stimulus. We found that dorsolateral prefrontal cortex was causally relevant for voluntary control over perceptual switches. In contrast, we failed to find any evidence for an active role of frontal cortex in passive bistable vision. Thus, it seems the same pathway used for willed top-down modulation of bistable vision is not used during passive bistable viewing.