Skin type and nerve effects on cortical tactile processing: a somatosensory evoked potentials study.

Somatosensory evoked potential (SEP) studies typically characterize short-latency components following median nerve stimulations of the wrist. However, these studies rarely considered 1) skin type (glabrous/hairy) at the stimulation site, 2) nerve being stimulated, and 3) middle-latency (>30 ms) components. Our aim was to investigate middle-latency SEPs following simple mechanical stimulation of two skin types innervated by two different nerves. Eighteen adults received 400 mechanical stimulations over four territories of the right hand (two nerves: radial/median; two skin types: hairy/glabrous skin) while their EEG was recorded. Four middle-latency components were identified: P50, N80, N130, and P200. As expected, significantly shorter latencies and larger amplitudes were found over the contralateral hemisphere for all components. A skin type effect was found for the N80; glabrous skin stimulations induced larger amplitude than hairy skin stimulations. Regarding nerve effects, median stimulations induced larger P50 and N80. Latency of the N80 was longer after median nerve stimulation compared with radial nerve stimulation. This study showed that skin type and stimulated nerve influence middle-latency SEPs, highlighting the importance of considering these parameters in future studies. These modulations could reflect differences in cutaneous receptors and somatotopy. Middle-latency SEPs can be used to evaluate the different steps of tactile information cortical processing. Modulation of SEP components before 100 ms possibly reflects somatotopy and differential processing in primary somatosensory cortex.NEW & NOTEWORTHY The current paper highlights the influences of stimulated skin type (glabrous/hairy) and nerve (median/radial) on cortical somatosensory evoked potentials. Mechanical stimulations were applied over four territories of the right hand in 18 adults. Four middle-latency components were identified: P50, N80, N130, and P200. A larger N80 was found after glabrous skin stimulations than after hairy skin ones, regardless of the nerve being stimulated. P50 and N80 were larger after median than radial nerve stimulations.

Neuronal population correlates of target selection and distractor filtering.

Frontal Eye Field (FEF) neurons discriminate between relevant and irrelevant visual stimuli and their response magnitude predicts conscious perception. How this is reflected in the spatial representation of a visual stimulus at the neuronal population level is unknown. We recorded neuronal population activity in the FEF while monkeys were performing a forced choice cued detection task with identical target and distractor stimuli. We quantified, using machine learning techniques, estimates of target and distractor location from FEF population multiunit activities. We found that the FEF population activity provides a precise single trial estimate of reported stimuli locations. Importantly, the closer this prefrontal population single trial estimate is to the veridical stimulus location, the higher the probability that the target or the distractor is reported as perceived. We show that stimulus perception is rescued by the estimate of attention allocation specifically when the latter is close enough to the actual stimulus location, thus indicating a partial independence between attention and perception. Overall, we thus show that how and what we perceive of our environment depends on the spatial precision with which this environment is coded by prefrontal neuronal populations.

The pupil: a window on social automatic processing in autism spectrum disorder children.

BACKGROUND: Faces are crucial social stimuli, eliciting automatic processing associated with increased physiological arousal in observers. The level of arousal can be indexed by pupil diameter (the 'Event-Related Pupil Dilation', ERPD). However, many parameters could influence the arousal evoked by a face and its social saliency (e.g. virtual vs. real, neutral vs. emotional, static vs. dynamic). A few studies have shown an atypical ERPD in autism spectrum disorder (ASD) patients using several kinds of faces but no study has focused on identifying which parameter of the stimulus is the most interfering with face processing in ASD. METHODS: In order to disentangle the influence of these parameters, we propose an original paradigm including stimuli along an ecological social saliency gradient: from static objects to virtual faces to dynamic emotional faces. This strategy was applied to 186 children (78 ASD and 108 typically developing (TD) children) in two pupillometric studies (22 ASD and 47 TD children in the study 1 and 56 ASD and 61 TD children in the study 2). RESULTS: Strikingly, the ERPD in ASD children is insensitive to any of the parameters tested: the ERPD was similar for objects, static faces or dynamic faces. On the opposite, the ERPD in TD children is sensitive to all the parameters tested: the humanoid, biological, dynamic and emotional quality of the stimuli. Moreover, ERPD had a good discriminative power between ASD and TD children: ASD had a larger ERPD than TD in response to virtual faces, while TD had a larger ERPD than ASD for dynamic faces. CONCLUSIONS: This novel approach evidences an abnormal physiological adjustment to socially relevant stimuli in ASD.

Fast Compensatory Functional Network Changes Caused by Reversible Inactivation of Monkey Parietal Cortex.

The brain has a remarkable capacity to recover after lesions. However, little is known about compensatory neural adaptations at the systems level. We addressed this question by investigating behavioral and (correlated) functional changes throughout the cortex that are induced by focal, reversible inactivations. Specifically, monkeys performed a demanding covert spatial attention task while the lateral intraparietal area (LIP) was inactivated with muscimol and whole-brain fMRI activity was recorded. The inactivation caused LIP-specific decreases in task-related fMRI activity. In addition, these local effects triggered large-scale network changes. Unlike most studies in which animals were mainly passive relative to the stimuli, we observed heterogeneous effects with more profound muscimol-induced increases of task-related fMRI activity in areas connected to LIP, especially FEF. Furthermore, in areas such as FEF and V4, muscimol-induced changes in fMRI activity correlated with changes in behavioral performance. Notably, the activity changes in remote areas did not correlate with the decreased activity at the site of the inactivation, suggesting that such changes arise via neuronal mechanisms lying in the intact portion of the functional task network, with FEF a likely key player. The excitation-inhibition dynamics unmasking existing excitatory connections across the functional network might initiate these rapid adaptive changes.

The Prediction of Impact of a Looming Stimulus onto the Body Is Subserved by Multisensory Integration Mechanisms.

In the jungle, survival is highly correlated with the ability to detect and distinguish between an approaching predator and a putative prey. From an ecological perspective, a predator rapidly approaching its prey is a stronger cue for flight than a slowly moving predator. In the present study, we use functional magnetic resonance imaging in the nonhuman primate, to investigate the neural bases of the prediction of an impact to the body by a looming stimulus, i.e., the neural bases of the interaction between a dynamic visual stimulus approaching the body and its expected consequences onto an independent sensory modality, namely, touch. We identify a core cortical network of occipital, parietal, premotor, and prefrontal areas maximally activated by tactile stimulations presented at the predicted time and location of impact of the looming stimulus on the faces compared with the activations observed for spatially or temporally incongruent tactile and dynamic visual cues. These activations reflect both an active integration of visual and tactile information and of spatial and temporal prediction information. The identified cortical network coincides with a well described multisensory visuotactile convergence and integration network suggested to play a key role in the definition of peripersonal space. These observations are discussed in the context of multisensory integration and spatial, temporal prediction and Bayesian causal inference.SIGNIFICANCE STATEMENT Looming stimuli have a particular ecological relevance as they are expected to come into contact with the body, evoking touch or pain sensations and possibly triggering an approach or escape behavior depending on their identity. Here, we identify the nonhuman primate functional network that is maximally activated by tactile stimulations presented at the predicted time and location of impact of the looming stimulus. Our findings suggest that the integration of spatial and temporal predictive cues possibly rely on the same neural mechanisms that are involved in multisensory integration.

Cortical networks for encoding near and far space in the non-human primate.

While extra-personal space is often erroneously considered as a unique entity, early neuropsychological studies report a dissociation between near and far space processing both in humans and in monkeys. Here, we use functional MRI in a naturalistic 3D environment to describe the non-human primate near and far space cortical networks. We describe the co-occurrence of two extended functional networks respectively dedicated to near and far space processing. Specifically, far space processing involves occipital, temporal, parietal, posterior cingulate as well as orbitofrontal regions not activated by near space, possibly subserving the processing of the shape and identity of objects. In contrast, near space processing involves temporal, parietal, prefrontal and premotor regions not activated by far space, possibly subserving the preparation of an arm/hand mediated action in this proximal space. Interestingly, this network also involves somatosensory regions, suggesting a cross-modal anticipation of touch by a nearby object. Last, we also describe cortical regions that process both far and near space with a preference for one or the other. This suggests a continuous encoding of relative distance to the body, in the form of a far-to-near gradient. We propose that these cortical gradients in space representation subserve the physically delineable peripersonal spaces described in numerous psychology and psychophysics studies.

Reward activations and face fields in monkey cingulate motor areas.

Several premotor areas have been identified within primate cingulate cortex; however their function is yet to be uncovered. Recent brain imaging work in humans revealed a topographic anatomofunctional overlap between feedback processing during exploratory behaviors and the corresponding body fields in the rostral cingulate motor area (RCZa), suggesting an embodied representation of feedback. In particular, a face field in RCZa processes juice feedback. Here we tested an extension of the embodied principle in which unexpected or relevant information obtained through the eye or the face would be processed by face fields in cingulate motor areas, and whether this applied to monkey cingulate cortex. We show that activations for juice reward, eye movement, eye blink, and tactile stimulation on the face overlap over two subfields within the cingulate sulcus likely corresponding to the rostral and caudal cingulate motor areas. This suggests that in monkeys as is the case in humans, behaviorally relevant information is processed through multiple cingulate body/effector maps. NEW & NOTEWORTHY What is the role of cingulate motor areas? In this study we observed in monkeys that, as in humans, neural responses to face-related events, juice reward, eye movement, eye blink, and tactile stimulations, clustered redundantly in two separate cingulate subfields. This suggests that behaviorally relevant information is processed by multiple cingulate effector maps. Importantly, this overlap supports the principle that the cingulate cortex processes feedback based on where it is experienced on the body.

Impact prediction by looming visual stimuli enhances tactile detection.

From an ecological point of view, approaching objects are potentially more harmful than receding objects. A predator, a dominant conspecific, or a mere branch coming up at high speed can all be dangerous if one does not detect them and produce the appropriate escape behavior fast enough. And indeed, looming stimuli trigger stereotyped defensive responses in both monkeys and human infants. However, while the heteromodal somatosensory consequences of visual looming stimuli can be fully predicted by their spatiotemporal dynamics, few studies if any have explored whether visual stimuli looming toward the face predictively enhance heteromodal tactile sensitivity around the expected time of impact and at its expected location on the body. In the present study, we report that, in addition to triggering a defensive motor repertoire, looming stimuli toward the face provide the nervous system with predictive cues that enhance tactile sensitivity on the face. Specifically, we describe an enhancement of tactile processes at the expected time and location of impact of the stimulus on the face. We additionally show that a looming stimulus that brushes past the face also enhances tactile sensitivity on the nearby cheek, suggesting that the space close to the face is incorporated into the subjects' body schema. We propose that this cross-modal predictive facilitation involves multisensory convergence areas subserving the representation of a peripersonal space and a safety boundary of self.

Tactile representation of the head and shoulders assessed by fMRI in the nonhuman primate.

In nonhuman primates, tactile representation at the cortical level has mostly been studied using single-cell recordings targeted to specific cortical areas. In this study, we explored the representation of tactile information delivered to the face or the shoulders at the whole brain level, using functional magnetic resonance imaging (fMRI) in the nonhuman primate. We used air puffs delivered to the center of the face, the periphery of the face, or the shoulders. These stimulations elicited activations in numerous cortical areas, encompassing the primary and secondary somatosensory areas, prefrontal and premotor areas, and parietal, temporal, and cingulate areas as well as low-level visual cortex. Importantly, a specific parieto-temporo-prefrontal network responded to the three stimulations but presented a marked preference for air puffs directed to the center of the face. This network corresponds to areas that are also involved in near-space representation, as well as in the multisensory integration of information at the interface between this near space and the skin of the face, and is probably involved in the construction of a peripersonal space representation around the head.

fMRI Cortical Correlates of Spontaneous Eye Blinks in the Nonhuman Primate.

Eyeblinks are defined as a rapid closing and opening of the eyelid. Three types of blinks are defined: spontaneous, reflexive, and voluntary. Here, we focus on the cortical correlates of spontaneous blinks, using functional magnetic resonance imaging (fMRI) in the nonhuman primate. Our observations reveal an ensemble of cortical regions processing the somatosensory, proprioceptive, peripheral visual, and possibly nociceptive consequences of blinks. These observations indicate that spontaneous blinks have consequences on the brain beyond the visual cortex, possibly contaminating fMRI protocols that generate in the participants heterogeneous blink behaviors. This is especially the case when these protocols induce (nonunusual) eye fatigue and corneal dryness due to demanding fixation requirements, as is the case here. Importantly, no blink related activations were observed in the prefrontal and parietal blinks motor command areas nor in the prefrontal, parietal, and medial temporal blink suppression areas. This indicates that the absence of activation in these areas is not a signature of the absence of blink contamination in the data. While these observations increase our understanding of the neural bases of spontaneous blinks, they also strongly call for new criteria to identify whether fMRI recordings are contaminated by a heterogeneous blink behavior or not.

Whole brain mapping of visual and tactile convergence in the macaque monkey.

The proposal that sensory processing is achieved in segregated anatomical pathways has been profoundly revisited following the description of cross-modal anatomical connections both at higher and at lower processing levels. However, an understanding of the cortical extent of these long range cross-modal functional influences has been missing. Here, we use functional magnetic resonance imaging (fMRI) to map, in the non-human primate brain, the cortical regions which are activated by both visual and tactile stimulations. We describe an unprecedented pattern of functional visuo-tactile convergence, encompassing both low-level visual and somatosensory areas and multiple higher-order associative areas. We also show that the profile of this convergence depends on the physical properties of the mapping stimuli, indicating that visuo-tactile convergence is most probably even more prevailing than what we actually describe. Overall, these observations substantiate the view that the brain is massively multisensory.

Multimodal convergence within the intraparietal sulcus of the macaque monkey.

The parietal cortex is highly multimodal and plays a key role in the processing of objects and actions in space, both in human and nonhuman primates. Despite the accumulated knowledge in both species, we lack the following: (1) a general description of the multisensory convergence in this cortical region to situate sparser lesion and electrophysiological recording studies; and (2) a way to compare and extrapolate monkey data to human results. Here, we use functional magnetic resonance imaging (fMRI) in the monkey to provide a bridge between human and monkey studies. We focus on the intraparietal sulcus (IPS) and specifically probe its involvement in the processing of visual, tactile, and auditory moving stimuli around and toward the face. We describe three major findings: (1) the visual and tactile modalities are strongly represented and activate mostly nonoverlapping sectors within the IPS. The visual domain occupies its posterior two-thirds and the tactile modality its anterior one-third. The auditory modality is much less represented, mostly on the medial IPS bank. (2) Processing of the movement component of sensory stimuli is specific to the fundus of the IPS and coincides with the anatomical definition of monkey ventral intraparietal area (VIP). (3) A cortical sector within VIP processes movement around and toward the face independently of the sensory modality. This amodal representation of movement may be a key component in the construction of peripersonal space. Overall, our observations highlight strong homologies between macaque and human VIP organization.

Default mode of brain function in monkeys.

Human neuroimaging has revealed a specific network of brain regions-the default-mode network (DMN)-that reduces its activity during goal-directed behavior. So far, evidence for a similar network in monkeys is mainly indirect, since, except for one positron emission tomography study, it is all based on functional connectivity analysis rather than activity increases during passive task states. Here, we tested whether a consistent DMN exists in monkeys using its defining property. We performed a meta-analysis of functional magnetic resonance imaging data collected in 10 awake monkeys to reveal areas in which activity consistently decreases when task demands shift from passive tasks to externally oriented processing. We observed task-related spatially specific deactivations across 15 experiments, implying in the monkey a functional equivalent of the human DMN. We revealed by resting-state connectivity that prefrontal and medial parietal regions, including areas 9/46d and 31, respectively, constitute the DMN core, being functionally connected to all other DMN areas. We also detected two distinct subsystems composed of DMN areas with stronger functional connections between each other. These clusters included areas 24/32, 8b, and TPOC and areas 23, v23, and PGm, respectively. Such a pattern of functional connectivity largely fits, but is not completely consistent with anatomical tract tracing data in monkeys. Also, analysis of afferent and efferent connections between DMN areas suggests a multisynaptic network structure. Like humans, monkeys increase activity during passive epochs in heteromodal and limbic association regions, suggesting that they also default to internal modes of processing when not actively interacting with the environment.

Proactive inhibitory control varies with task context.

The goal of executive control is to adjust our behaviour to the environment. It involves not only the continuous planning and adaptation of actions but also the inhibition of inappropriate movements. Recently, a proactive form of inhibitory control has been shown, demonstrating that actions can be withheld, in an uncertain environment, thanks to the proactive locking of the mechanism by which motor commands are triggered (e.g. while waiting at traffic lights in a dense pedestrian zone, one will refrain in anticipation of a brisk acceleration when the green light comes on). However, little is known about this executive function and it remains unclear whether the overall amount of inhibitory control can be modulated as a function of the context. Here, we show that the level of this control varies parametrically as a function of the exogenous and endogenous factors setting the task context. We also show that the level of implemented proactive inhibitory control is dynamically readjusted to match the implicit temporal structure of the environment. These observations are discussed in relation to possible underlying functional substrates and related neurological and psychiatric pathologies.

COVID-19 masks: A barrier to facial and vocal information.

With the COVID-19 pandemic, we have become used to wearing masks and have experienced how masks seem to impair emotion and speech recognition. While several studies have focused on facial emotion recognition by adding images of masks on photographs of emotional faces, we have created a video database with actors really wearing masks to test its effect in more ecological conditions. After validating the emotions displayed by the actors, we found that surgical mask impaired happiness and sadness recognition but not neutrality. Moreover, for happiness, this effect was specific to the mask and not to covering the lower part of the face, possibly due to a cognitive bias associated with the surgical mask. We also created videos with speech and tested the effect of mask on emotion and speech recognition when displayed in auditory, visual, or audiovisual modalities. In visual and audiovisual modalities, mask impaired happiness and sadness but improved neutrality recognition. Mask impaired the recognition of bilabial syllables regardless of modality. In addition, it altered speech recognition only in the audiovisual modality for participants above 70 years old. Overall, COVID-19 masks mainly impair emotion recognition, except for older participants for whom it also impacts speech recognition, probably because they rely more on visual information to compensate age-related hearing loss.

Facial mask disturbs ocular exploration but not pupil reactivity.

Introduction: The COVID-19 pandemic has imposed to wear a face mask that may have negative consequences for social interactions despite its health benefits. A lot of recent studies focused on emotion recognition of masked faces, as the mouth is, with the eyes, essential to convey emotional content. However, none have studied neurobehavioral and neurophysiological markers of masked faces perception, such as ocular exploration and pupil reactivity. The purpose of this eye tracking study was to quantify how wearing a facial accessory, and in particular a face mask, affected the ocular and pupillary response to a face, emotional or not. Methods: We used videos of actors wearing a facial accessory to characterize the visual exploration and pupillary response in several occlusion (no accessory, sunglasses, scarf, and mask) and emotional conditions (neutral, happy, and sad) in a population of 44 adults. Results: We showed that ocular exploration differed for face covered with an accessory, and in particular a mask, compared to the classical visual scanning pattern of a non-covered face. The covered areas of the face were less explored. Pupil reactivity seemed only slightly affected by the mask, while its sensitivity to emotions was observed even in the presence of a facial accessory. Discussion: These results suggest a mixed impact of the mask on attentional capture and physiological adjustment, which does not seem to be reconcilable with its strong effect on behavioral emotional recognition previously described.

Atypical Response to Affective Touch in Children with Autism: Multi-Parametric Exploration of the Autonomic System.

This study aimed at evaluating the autonomic response to pleasant affective touch in children with Autism Spectrum Disorders (ASD) and age-matched typically developing (TD) peers, thanks to multiple autonomic nervous system (ANS) parameters and by contrasting CT (C-tactile fibers) high- vs. low-density territory stimulations. We measured pupil diameter, skin conductance, and heart rate during gentle stroking of two skin territories (CT high- and low-density, respectively, forearm and palm of the hand) in thirty 6-12-year-old TD children and twenty ASD children. TD children showed an increase in pupil diameter and skin conductance associated with a heart rate deceleration in response to tactile stimulations at the two locations. Only the pupil was influenced by the stimulated location, with a later dilation peak following CT low-density territory stimulation. Globally, ASD children exhibited reduced autonomic responses, as well as different ANS baseline values compared to TD children. These atypical ANS responses to pleasant touch in ASD children were not specific to CT-fiber stimulation. Overall, these results point towards both basal autonomic dysregulation and lower tactile autonomic evoked responses in ASD, possibly reflecting lower arousal and related to social disengagement.

Autonomic tone in children and adults: Pupillary, electrodermal and cardiac activity at rest.

Considering the suspected involvement of the autonomic nervous system (ANS) in several neurodevelopmental disorders, a description of its tonus in typical populations and of its maturation between childhood and adulthood is necessary. We aimed to arrive at a better understanding of the maturation of the sympathetic (SNS) and parasympathetic (PNS) tonus by comparing children and adults at rest, via recordings of multiple ANS indices. We recorded simultaneously pupil diameter, electrodermal activity (EDA) and cardiac activity (RR interval and HRV: heart rate variability) in 29 children (6-12 years old) and 30 adults (20-42 years old) during a 5-min rest period. Children exhibited lower RR intervals, higher LF peak frequencies, and lower LF/HF (low frequency/high frequency) ratios compared to adults. Children also produced more spontaneous EDA peaks, reflected in a larger EDA AUC (area under the curve), in comparison with adults. Finally, children displayed a larger median pupil diameter and a higher pupillary hippus frequency than adults. Our results converged towards higher SNS and PNS tones in children compared to adults. Childhood would thus be characterized by a high autonomic tone, possibly reflecting a physiological state compatible with developmental acquisitions.

Anterior regions of monkey parietal cortex process visual 3D shape.

The intraparietal cortex is involved in the control of visually guided actions, like reach-to-grasp movements, which require extracting the 3D shape and position of objects from 2D retinal images. Using fMRI in behaving monkeys, we investigated the role of the intraparietal cortex in processing stereoscopic information for recovering the depth structure and the position in depth of objects. We found that while several areas (CIP, LIP, and AIP on the lateral bank; PIP and MIP on the medial bank) are activated by stereoscopic stimuli, AIP and an adjoining portion of LIP are sensitive only to depth structure. Furthermore, only these two regions are sensitive to both the depth structure and the 2D shape of small objects. These results indicate that extracting 3D spatial information from stereo involves several intraparietal areas, among which AIP and anterior LIP are more specifically engaged in extracting the 3D shape of objects.

Attention to baseline: does orienting visuospatial attention really facilitate target detection?

Standard protocols testing the orientation of visuospatial attention usually present spatial cues before targets and compare valid-cue trials with invalid-cue trials. The valid/invalid contrast results in a relative behavioral or physiological difference that is generally interpreted as a benefit of attention orientation. However, growing evidence suggests that inhibitory control of response is closely involved in this kind of protocol that requires the subjects to withhold automatic responses to cues, probably biasing behavioral and physiological baselines. Here, we used two experiments to disentangle the inhibitory control of automatic responses from orienting of visuospatial attention in a saccadic reaction time task in humans, a variant of the classical cue-target detection task and a sustained visuospatial attentional task. Surprisingly, when referring to a simple target detection task in which there is no need to refrain from reacting to avoid inappropriate responses, we found no consistent evidence of facilitation of target detection at the attended location. Instead, we observed a cost at the unattended location. Departing from the classical view, our results suggest that reaction time measures of visuospatial attention probably relie on the attenuation of elementary processes involved in visual target detection and saccade initiation away from the attended location rather than on facilitation at the attended location. This highlights the need to use proper control conditions in experimental designs to disambiguate relative from absolute cueing benefits on target detection reaction times, both in psychophysical and neurophysiological studies.