The dynamics of statistical learning in visual search and its interaction with salience processing: An EEG study.

Visual attention can be guided by statistical regularities in the environment, that people implicitly learn from past experiences (statistical learning, SL). Moreover, a perceptually salient element can automatically capture attention, gaining processing priority through a bottom-up attentional control mechanism. The aim of our study was to investigate the dynamics of SL and if it shapes attentional target selection additively with salience processing, or whether these mechanisms interact, e.g. one gates the other. In a visual search task, we therefore manipulated target frequency (high vs. low) across locations while, in some trials, the target was salient in terms of colour. Additionally, halfway through the experiment, the high-frequency location changed to the opposite hemifield. EEG activity was simultaneously recorded, with a specific interest in two markers related to target selection and post-selection processing, respectively: N2pc and SPCN. Our results revealed that both SL and saliency significantly enhanced behavioural performance, but also interacted with each other, with an attenuated saliency effect at the high-frequency target location, and a smaller SL effect for salient targets. Concerning processing dynamics, the benefit of salience processing was more evident during the early stage of target selection and processing, as indexed by a larger N2pc and early-SPCN, whereas SL modulated the underlying neural activity particularly later on, as revealed by larger late-SPCN. Furthermore, we showed that SL was rapidly acquired and adjusted when the spatial imbalance changed. Overall, our findings suggest that SL is flexible to changes and, combined with salience processing, jointly contributes to establishing attentional priority.

Macaque claustrum, pulvinar and putative dorsolateral amygdala support the cross-modal association of social audio-visual stimuli based on meaning.

Social communication draws on several cognitive functions such as perception, emotion recognition and attention. The association of audio-visual information is essential to the processing of species-specific communication signals. In this study, we use functional magnetic resonance imaging in order to identify the subcortical areas involved in the cross-modal association of visual and auditory information based on their common social meaning. We identified three subcortical regions involved in audio-visual processing of species-specific communicative signals: the dorsolateral amygdala, the claustrum and the pulvinar. These regions responded to visual, auditory congruent and audio-visual stimulations. However, none of them was significantly activated when the auditory stimuli were semantically incongruent with the visual context, thus showing an influence of visual context on auditory processing. For example, positive vocalization (coos) activated the three subcortical regions when presented in the context of positive facial expression (lipsmacks) but not when presented in the context of negative facial expression (aggressive faces). In addition, the medial pulvinar and the amygdala presented multisensory integration such that audiovisual stimuli resulted in activations that were significantly higher than those observed for the highest unimodal response. Last, the pulvinar responded in a task-dependent manner, along a specific spatial sensory gradient. We propose that the dorsolateral amygdala, the claustrum and the pulvinar belong to a multisensory network that modulates the perception of visual socioemotional information and vocalizations as a function of the relevance of the stimuli in the social context. SIGNIFICANCE STATEMENT: Understanding and correctly associating socioemotional information across sensory modalities, such that happy faces predict laughter and escape scenes predict screams, is essential when living in complex social groups. With the use of functional magnetic imaging in the awake macaque, we identify three subcortical structures-dorsolateral amygdala, claustrum and pulvinar-that only respond to auditory information that matches the ongoing visual socioemotional context, such as hearing positively valenced coo calls and seeing positively valenced mutual grooming monkeys. We additionally describe task-dependent activations in the pulvinar, organizing along a specific spatial sensory gradient, supporting its role as a network regulator.

Prefrontal Control of Proactive and Reactive Mechanisms of Visual Suppression.

In everyday life, we are continuously struggling at focusing on our current goals while at the same time avoiding distractions. Attention is the neuro-cognitive process devoted to the selection of behaviorally relevant sensory information while at the same time preventing distraction by irrelevant information. Distraction can be prevented proactively, by strategically prioritizing task-relevant information at the expense of irrelevant information, or reactively, by suppressing the ongoing processing of distractors. The distinctive neuronal signature of these suppressive mechanisms is still largely unknown. Thanks to machine-learning decoding methods applied to prefrontal cortical activity, we monitor the dynamic spatial attention with an unprecedented spatial and temporal resolution. We first identify independent behavioral and neuronal signatures for long-term (learning-based spatial prioritization) and short-term (dynamic spatial attention) mechanisms. We then identify distinct behavioral and neuronal signatures for proactive and reactive suppression mechanisms. We find that while distracting task-relevant information is suppressed proactively, task-irrelevant information is suppressed reactively. Critically, we show that distractor suppression, whether proactive or reactive, strongly depends on the implementation of both long-term and short-term mechanisms of selection. Overall, we provide a unified neuro-cognitive framework describing how the prefrontal cortex deals with distractors in order to flexibly optimize behavior in dynamic environments.

The neural bases of spatial attention and perceptual rhythms.

Attentional processes allow the brain to overcome its processing capacities limitations by enhancing relevant visual information and suppressing irrelevant information. Thus attention plays a critical role, shaping our perception of the world. Several models have been proposed to describe the neuronal bases of attention and its mechanistic underlyings. Recent electrophysiological evidence show that attentional processes rely on oscillatory brain activities that correlate with rhythmic changes in cognitive performance. In the present review, we first take a historical perspective on how attention is viewed, from the initial spotlight theory of attention to the recent dynamic view of attention selection and we review their supporting psychophysical evidence. Based on recent prefrontal electrophysiological evidence, we refine the most recent models of attention sampling by proposing a rhythmic and continuous model of attentional sampling. In particular, we show that attention involves a continuous exploration of space, shifting within and across visual hemifield at specific alpha and theta rhythms, independently of the current attentional load. In addition, we show that this prefrontal attentional spotlight implements conjointly selection and suppression mechanisms, and is captured by salient incoming items. Last, we argue that this attention spotlight implements a highly flexible alternation of attentional exploration and exploitation epochs, depending on ongoing task contingencies. In a last part, we review the local and network oscillatory mechanisms that correlate with rhythmic attentional sampling, describing multiple rhythmic generators and complex network interactions.

Strengths and challenges of longitudinal non-human primate neuroimaging.

Longitudinal non-human primate neuroimaging has the potential to greatly enhance our understanding of primate brain structure and function. Here we describe its specific strengths, compared to both cross-sectional non-human primate neuroimaging and longitudinal human neuroimaging, but also its associated challenges. We elaborate on factors guiding the use of different analytical tools, subject-specific versus age-specific templates for analyses, and issues related to statistical power.

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 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.

High-resolution 3D diffusion tensor MRI of anesthetized rhesus macaque brain at 3T.

Diffusion Magnetic Resonance Imaging (dMRI) has been widely used to investigate human brain microstructure and connectivity and its abnormalities in a variety of brain deficits, whether acute, neurodevelopmental or neurodegenerative. However, the biological interpretation and validation of dMRI data modelling is still a crucial challenge in the field. In this respect, achieving high spatial resolution in-vivo dMRI in the non-human primate to compare these observations both with human dMRI on the one hand and 'ground truth' microstructural and histological data on the other hand is of outmost importance. Here, we developed a dMRI pulse sequence based on 3D-multishot Echo Planar Imaging (3D-msEPI) on a 3T human clinical scanner. We demonstrate the feasibility of cerebral dMRI at an isotropic resolution of 0.5 mm in 4 anesthetized macaque monkeys. The added value of the high-resolution dMRI is illustrated by focusing on two aspects. First, we show an enhanced descriptive power of the fine substructure of the hippocampus. Second, we show a more physiological description of the interface between cortex grey matter, superficial and deep white matter. Overall, the high spatial resolution dMRI acquisition method proposed in this study is a significant achievement with respect to the state of the art of dMRI on anesthetized monkeys. This study highlights also the potential of very high-resolution dMRI to precisely capture the microstructure of thin cerebral structures such as the hippocampus and superficial white matter.

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.

Differential dynamics of spatial attention, position, and color coding within the parietofrontal network.

Despite an ever growing knowledge on how parietal and prefrontal neurons encode low-level spatial and color information or higher-level information, such as spatial attention, an understanding of how these cortical regions process neuronal information at the population level is still missing. A simple assumption would be that the function and temporal response profiles of these neuronal populations match that of its constituting individual cells. However, several recent studies suggest that this is not necessarily the case and that the single-cell approach overlooks dynamic changes in how information is distributed over the neuronal population. Here, we use a time-resolved population pattern analysis to explore how spatial position, spatial attention and color information are differentially encoded and maintained in the macaque monkey prefrontal (frontal eye fields) and parietal cortex (lateral intraparietal area). Overall, our work brings about three novel observations. First, we show that parietal and prefrontal populations operate in two distinct population regimens for the encoding of sensory and cognitive information: a stationary mode and a dynamic mode. Second, we show that the temporal dynamics of a heterogeneous neuronal population brings about complementary information to that of its functional subpopulations. Thus, both need to be investigated in parallel. Last, we show that identifying the neuronal configuration in which a neuronal population encodes given information can serve to reveal this same information in a different context. All together, this work challenges common views on neural coding in the parietofrontal network.

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.

A functional hierarchy within the parietofrontal network in stimulus selection and attention control.

Although we are confronted with an ever-changing environment, we do not have the capacity to analyze all incoming sensory information. Perception is selective and is guided both by salient events occurring in our visual field and by cognitive premises about what needs our attention. Although the lateral intraparietal area (LIP) and frontal eye field (FEF) are known to represent the position of visual attention, their respective contributions to its control are still unclear. Here, we report LIP and FEF neuronal activities recorded while monkeys performed a voluntary attention-orientation target-detection task. We show that both encode behaviorally significant events, but that the FEF plays a specific role in mapping abstract cue instructions onto a spatial priority map to voluntarily guide attention. On the basis of a latency analysis, we show that the coding of stimulus identity and position precedes the emergence of an explicit attentional signal within the FEF. We also describe dynamic temporal hierarchies between LIP and FEF: stimuli carrying the highest intrinsic saliency are signaled by LIP before FEF, whereas stimuli carrying the highest extrinsic saliency are signaled in FEF before LIP. This suggests that whereas the parietofrontal attentional network most probably processes visual information in a recurrent way, exogenous processing predominates in the parietal cortex and the endogenous control of attention takes place in the FEF.

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.

Fluoxetine degrades luminance perceptual thresholds while enhancing motivation and reward sensitivity.

Selective serotonin reuptake inhibitors (SSRIs) increase serotonin activity in the brain. While they are mostly known for their antidepressant properties, they have been shown to improve visual functions in amblyopia and impact cognitive functions ranging from attention to motivation and sensitivity to reward. Yet, a clear understanding of the specific action of serotonin to each of bottom-up sensory and top-down cognitive control components and their interaction is still missing. To address this question, we characterize, in two adult male macaques, the behavioral effects of fluoxetine, a specific SSRI, on visual perception under varying bottom-up (luminosity, distractors) and top-down (uncertainty, reward biases) constraints while they are performing three different visual tasks. We first manipulate target luminosity in a visual detection task, and we show that fluoxetine degrades luminance perceptual thresholds. We then use a target detection task in the presence of spatial distractors, and we show that under fluoxetine, monkeys display both more liberal responses as well as a degraded perceptual spatial resolution. In a last target selection task, involving free choice in the presence of reward biases, we show that monkeys display an increased sensitivity to reward outcome under fluoxetine. In addition, we report that monkeys produce, under fluoxetine, more trials and less aborts, increased pupil size, shorter blink durations, as well as task-dependent changes in reaction times. Overall, while low level vision appears to be degraded by fluoxetine, performances in the visual tasks are maintained under fluoxetine due to enhanced top-down control based on task outcome and reward maximization.

Effects of top-down and bottom-up attention on post-selection posterior contralateral negativity.

We examined the effect of combined top-down and bottom-up attentional control sources in easy and difficult visual search tasks. Applying a new analysis on previously acquired data, we focused on the sustained posterior contralateral negativity (SPCN) and the response-locked posterior contralateral negativity (RLpcN), to better understand processes following target selection. We used the signed-area approach to measure the negative area, where the signal was either locked to the target or the response onsets. We further split the RLpcN into an early and a late segment to capture the dynamics of selection and post-selection processes. In Experiment 1, participants reported the orientation of a uniquely tilted target. In Experiment 2, participants reported the position of a small gap within the uniquely tilted target. In both experiments, endogenous cues manipulated top-down attention (valid vs. neutral), and salient color singletons (either the target or a distractor) manipulated bottom-up attention. We hypothesized that the SPCN and the later segment of the RLpcN would be modulated by task difficulty and target salience, as they are associated with post-selection processes, such as response selection and working memory. The early segment of the RLpcN was hypothesized to be modulated by the cueing manipulation and presence of a salient distractor, as they affect target selection. An effect of distractor presence was observed on the early segment of the RLpcN, and our results further supported the hypotheses regarding the SPCN and the later segment of the RLpcN, providing novel insights into post-selection processes in visual search.

Integrated effects of top-down attention and statistical learning during visual search: An EEG study.

The present study aims to investigate how the competition between visual elements is solved by top-down and/or statistical learning (SL) attentional control (AC) mechanisms when active together. We hypothesized that the "winner" element that will undergo further processing is selected either by one AC mechanism that prevails over the other, or by the joint activity of both mechanisms. To test these hypotheses, we conducted a visual search experiment that combined an endogenous cueing protocol (valid vs. neutral cue) and an imbalance of target frequency distribution across locations (high- vs. low-frequency location). The unique and combined effects of top-down control and SL mechanisms were measured on behaviour and amplitudes of three evoked-response potential (ERP) components (i.e., N2pc, P1, CNV) related to attentional processing. Our behavioural results showed better performance for validly cued targets and for targets in the high-frequency location. The two factors were found to interact, so that SL effects emerged only in the absence of top-down guidance. Whereas the CNV and P1 only displayed a main effect of cueing, for the N2pc we observed an interaction between cueing and SL, revealing a cueing effect for targets in the low-frequency condition, but not in the high-frequency condition. Thus, our data support the view that top-down control and SL work in a conjoint, integrated manner during target selection. In particular, SL mechanisms are reduced or even absent when a fully reliable top-down guidance of attention is at play.