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

Nat Commun 13, 4886 (2022). 

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.

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

Nat Commun 13, 4796 (2022). 

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.

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

Progress in Neurobiology Volume 209, 102185 (2022). 

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.

A multisensory perspective onto primate pulvinar functions

Neuroscience & Biobehavioral Reviews. Volume 125, June 2021, Pages 231-243. 

Perception in ambiguous environments relies on the combination of sensory information from various sources. Most associative and primary sensory cortical areas are involved in this multisensory active integration process. As a result, the entire cortex appears as heavily multisensory. In this review, we focus on the contribution of the pulvinar to multisensory integration. This subcortical thalamic nucleus plays a central role in visual detection and selection at a fast time scale, as well as in the regulation of visual processes, at a much slower time scale. However, the pulvinar is also densely connected to cortical areas involved in multisensory integration. In spite of this, little is known about its multisensory properties and its contribution to multisensory perception. Here, we review the anatomical and functional organization of multisensory input to the pulvinar. We describe how visual, auditory, somatosensory, pain, proprioceptive and olfactory projections are differentially organized across the main subdivisions of the pulvinar and we show that topography is central to the organization of this complex nucleus. We propose that the pulvinar combines multiple sources of sensory information to enhance fast responses to the environment, while also playing the role of a general regulation hub for adaptive and flexible cognition.

Prefrontal attentional saccades explore space rhythmically

Nat Commun 11, 925 (2020). 

Recent studies suggest that attention samples space rhythmically through oscillatory interactions in the frontoparietal network. How these attentional fluctuations coincide with spatial exploration/displacement and exploitation/selection by a dynamic attentional spotlight under top-down control is unclear. Here, we show a direct contribution of prefrontal attention selection mechanisms to a continuous space exploration. Specifically, we provide a direct high spatio-temporal resolution prefrontal population decoding of the covert attentional spotlight. We show that it continuously explores space at a 7–12 Hz rhythm. Sensory encoding and behavioral reports are increased at a specific optimal phase w/ to this rhythm. We propose that this prefrontal neuronal rhythm reflects an alpha-clocked sampling of the visual environment in the absence of eye movements. These attentional explorations are highly flexible, how they spatially unfold depending both on within-trial and across-task contingencies. These results are discussed in the context of exploration-exploitation strategies and prefrontal top-down attentional control.

Direct Two-Dimensional Access to the Spatial Location of Covert Attention in Macaque Prefrontal Cortex

Current Biology. Volume 26: 13, 1699-1704, 2016.   

Direct access to motor cortical information now enables tetraplegic patients to precisely control neuroprostheses and recover some autonomy. In contrast, explicit access to higher cortical cognitive functions, such as covert attention, has been missing. Indeed, this cognitive information, known only to the subject, can solely be inferred by an observer from the subject’s overt behavior. Here, we present direct two-dimensional real-time access to where monkeys are covertly paying attention, using machine-learning decoding methods applied to their ongoing prefrontal cortical activity. Decoded attention was highly predictive of overt behavior in a cued target-detection task. Indeed, monkeys had a higher probability of detecting a visual stimulus as the distance between decoded attention and stimulus location decreased. This was true whether the visual stimulus was presented at the cued target location or at another distractor location. In error trials, in which the animals failed to detect the cued target stimulus, both the locations of attention and visual cue were misencoded. This misencoding coincided with a specific state of the prefrontal cortical population in which the shared variability between its different neurons (or noise correlations) was high, even before trial onset. This observation strongly suggests a functional link between high noise-correlation states and attentional failure. Overall, this real-time access to the attentional spotlight, as well as the identification of a neural signature of attentional lapses, open new perspectives both to the study of the neural bases of attention and to the remediation or enhancement of the attentional function using neurofeedback.