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.

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.

The relevance of the unique anatomy of the human prefrontal operculum to the emergence of speech.

Identifying the evolutionary origins of human speech remains a topic of intense scientific interest. Here we describe a unique feature of adult human neuroanatomy compared to chimpanzees and other primates that may provide an explanation of changes that occurred to enable the capacity for speech. That feature is the Prefrontal extent of the Frontal Operculum (PFOp) region, which is located in the ventrolateral prefrontal cortex, adjacent and ventromedial to the classical Broca's area. We also show that, in chimpanzees, individuals with the most human-like PFOp, particularly in the left hemisphere, have greater oro-facial and vocal motor control abilities. This critical discovery, when combined with recent paleontological evidence, suggests that the PFOp is a recently evolved feature of human cortical structure (perhaps limited to the genus Homo) that emerged in response to increasing selection for cognitive and motor functions evident in modern speech abilities.

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.

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.

A revised perspective on the evolution of the lateral frontal cortex in primates.

Detailed neuroscientific data from macaque monkeys have been essential in advancing understanding of human frontal cortex function, particularly for regions of frontal cortex without homologs in other model species. However, precise transfer of this knowledge for direct use in human applications requires an understanding of monkey to hominid homologies, particularly whether and how sulci and cytoarchitectonic regions in the frontal cortex of macaques relate to those in hominids. We combine sulcal pattern analysis with resting-state functional magnetic resonance imaging and cytoarchitectonic analysis to show that old-world monkey brains have the same principles of organization as hominid brains, with the notable exception of sulci in the frontopolar cortex. This essential comparative framework provides insights into primate brain evolution and a key tool to drive translation from invasive research in monkeys to human applications.

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.

Beyond the brain-computer interface: Decoding brain activity as a tool to understand neuronal mechanisms subtending cognition and behavior.

One of the major challenges in system neurosciences consists in developing techniques for estimating the cognitive information content in brain activity. This has an enormous potential in different domains spanning from clinical applications, cognitive enhancement to a better understanding of the neural bases of cognition. In this context, the inclusion of machine learning techniques to decode different aspects of human cognition and behavior and its use to develop brain-computer interfaces for applications in neuroprosthetics has supported a genuine revolution in the field. However, while these approaches have been shown quite successful for the study of the motor and sensory functions, success is still far from being reached when it comes to covert cognitive functions such as attention, motivation and decision making. While improvement in this field of BCIs is growing fast, a new research focus has emerged from the development of strategies for decoding neural activity. In this review, we aim at exploring how the advanced in decoding of brain activity is becoming a major neuroscience tool moving forward our understanding of brain functions, providing a robust theoretical framework to test predictions on the relationship between brain activity and cognition and behavior.

Distractibility and impulsivity neural states are distinct from selective attention and modulate the implementation of spatial attention.

In the context of visual attention, it has been classically assumed that missing the response to a target or erroneously selecting a distractor occurs as a consequence of the (miss)allocation of attention in space. In the present paper, we challenge this view and provide evidence that, in addition to encoding spatial attention, prefrontal neurons also encode a distractibility-to-impulsivity state. Using supervised dimensionality reduction techniques in prefrontal neuronal recordings in monkeys, we identify two partially overlapping neuronal subpopulations associated either with the focus of attention or overt behaviour. The degree of overlap accounts for the behavioral gain associated with the good allocation of attention. We further describe the neural variability accounting for distractibility-to-impulsivity behaviour by a two dimensional state associated with optimality in task and responsiveness. Overall, we thus show that behavioral performance arises from the integration of task-specific neuronal processes and pre-existing neuronal states describing task-independent behavioral states.

Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain.

Social interactions rely on the interpretation of semantic and emotional information, often from multiple sensory modalities. Nonhuman primates send and receive auditory and visual communicative signals. However, the neural mechanisms underlying the association of visual and auditory information based on their common social meaning are unknown. Using heart rate estimates and functional neuroimaging, we show that in the lateral and superior temporal sulcus of the macaque monkey, neural responses are enhanced in response to species-specific vocalisations paired with a matching visual context, or when vocalisations follow, in time, visual information, but inhibited when vocalisation are incongruent with the visual context. For example, responses to affiliative vocalisations are enhanced when paired with affiliative contexts but inhibited when paired with aggressive or escape contexts. Overall, we propose that the identified neural network represents social meaning irrespective of sensory modality.

An evolutionary gap in primate default mode network organization.

The human default mode network (DMN) is engaged at rest and in cognitive states such as self-directed thoughts. Interconnected homologous cortical areas in primates constitute a network considered as the equivalent. Here, based on a cross-species comparison of the DMN between humans and non-hominoid primates (macaques, marmosets, and mouse lemurs), we report major dissimilarities in connectivity profiles. Most importantly, the medial prefrontal cortex (mPFC) of non-hominoid primates is poorly engaged with the posterior cingulate cortex (PCC), though strong correlated activity between the human PCC and the mPFC is a key feature of the human DMN. Instead, a fronto-temporal resting-state network involving the mPFC was detected consistently across non-hominoid primate species. These common functional features shared between non-hominoid primates but not with humans suggest a substantial gap in the organization of the primate's DMN and its associated cognitive functions.

An EEG study of the combined effects of top-down and bottom-up attentional selection under varying task difficulty.

We examined the effect of combined top-down and bottom-up attentional control sources, using known attention-related EEG components that are thought to reflect target selection (N2pc) and distractor suppression (PD ). We used endogenous cues (valid vs. neutral) for top-down attentional control, and salience in the form of color singletons (either the target or a distractor) for bottom-up attentional control in visual search. Crucially, in two experiments, the task was of increasing difficulty, reporting the orientation of a tilted target (Experiment 1), or the position of a small gap within the target among tilted non-targets (Experiment 2). Our results showed strong cueing effects on RT and accuracy in both experiments, demonstrating a general facilitation of responses to validly cued targets. Whereas the processing of salient targets was not improved compared with non-salient targets, the presence of a salient distractor consistently worsened performance. The N2pc and PD were only observed in trials where targets were preceded by neutral cues in Experiment 1, and for validly cued targets and salient neutrally cued targets in Experiment 2. A cueing effect was found on the PD in Experiment 1, showing an amplitude reduction in trials where the target was validly cued. These results support the idea that bottom-up attentional allocation occurs only when top-down allocation of attention is absent or inefficient. Therefore, these results indicate that attentional selection and suppression during visual search are both influenced by top-down cueing and give support to theories that focus on the interaction between the two types of attention.

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.

The macaque ventral intraparietal area has expanded into three homologue human parietal areas.

The macaque ventral intraparietal area (VIP) in the fundus of the intraparietal sulcus has been implicated in a diverse range of sensorimotor and cognitive functions such as motion processing, multisensory integration, processing of head peripersonal space, defensive behavior, and numerosity coding. Here, we exhaustively review macaque VIP function, cytoarchitectonics, and anatomical connectivity and integrate it with human studies that have attempted to identify a potential human VIP homologue. We show that human VIP research has consistently identified three, rather than one, bilateral parietal areas that each appear to subsume some, but not all, of the macaque area's functionality. Available evidence suggests that this human "VIP complex" has evolved as an expansion of the macaque area, but that some precursory specialization within macaque VIP has been previously overlooked. The three human areas are dominated, roughly, by coding the head or self in the environment, visual heading direction, and the peripersonal environment around the head, respectively. A unifying functional principle may be best described as prediction in space and time, linking VIP to state estimation as a key parietal sensorimotor function. VIP's expansive differentiation of head and self-related processing may have been key in the emergence of human bodily self-consciousness.

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.

Early social adversity modulates the relation between attention biases and socioemotional behaviour in juvenile macaques.

Affect-biased attention may play a fundamental role in early socioemotional development, but factors influencing its emergence and associations with typical versus pathological outcomes remain unclear. Here, we adopted a nonhuman primate model of early social adversity (ESA) to: (1) establish whether juvenile, pre-adolescent macaques demonstrate attention biases to both threatening and reward-related dynamic facial gestures; (2) examine the effects of early social experience on such biases; and (3) investigate how this relation may be linked to socioemotional behaviour. Two groups of juvenile macaques (ESA exposed and non-ESA exposed) were presented with pairs of dynamic facial gestures comprising two conditions: neutral-threat and neutral-lipsmacking. Attention biases to threat and lipsmacking were calculated as the proportion of gaze to the affective versus neutral gesture. Measures of anxiety and social engagement were also acquired from videos of the subjects in their everyday social environment. Results revealed that while both groups demonstrated an attention bias towards threatening facial gestures, a greater bias linked to anxiety was demonstrated by the ESA group only. Only the non-ESA group demonstrated a significant attention bias towards lipsmacking, and the degree of this positive bias was related to duration and frequency of social engagement in this group. These findings offer important insights into the effects of early social experience on affect-biased attention and related socioemotional behaviour in nonhuman primates, and demonstrate the utility of this model for future investigations into the neural and learning mechanisms underlying this relationship across development.

Revisiting Persistent Neuronal Activity During Covert Spatial Attention.

Persistent activity has been observed in the prefrontal cortex (PFC), in particular during the delay periods of visual attention tasks. Classical approaches based on the average activity over multiple trials have revealed that such an activity encodes the information about the attentional instruction provided in such tasks. However, single-trial approaches have shown that activity in this area is rather sparse than persistent and highly heterogeneous not only within the trials but also between the different trials. Thus, this observation raised the question of how persistent the actually persistent attention-related prefrontal activity is and how it contributes to spatial attention. In this paper, we review recent evidence of precisely deconstructing the persistence of the neural activity in the PFC in the context of attention orienting. The inclusion of machine-learning methods for decoding the information reveals that attention orienting is a highly dynamic process, possessing intrinsic oscillatory dynamics working at multiple timescales spanning from milliseconds to minutes. Dimensionality reduction methods further show that this persistent activity dynamically incorporates multiple sources of information. This novel framework reflects a high complexity in the neural representation of the attention-related information in the PFC, and how its computational organization predicts behavior.

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.