The macaque monkey’s ventral intraparietal area (VIP) in the intraparietal sulcus (IPS) responds to visual, vestibular, tactile, and auditory signals and is involved in higher cognitive functions, including the processing of peripersonal space. In humans, VIP appears to have expanded into three functionally distinct regions. Macaque VIP has been divided cytoarchitonically into medial and lateral parts; however, no functional specialization has so far been associated with this anatomical division. Functional MRI suggests a functional gradient along the anterior-posterior axis of the macaque IPS: anterior VIP shows visio-tactile properties and face preference, whereas posterior VIP responds to large-field visual dynamic stimuli. This functional distinction matches with functional differences among the three human VIP regions, suggesting that a regional specialization may also exist within macaque VIP. Here, we characterized the macaque ipsilateral, whole-brain functional connectivity, assessed during awake resting state, along VIP’s anterior-posterior axis by dividing VIP into three regions of interest (ROIs). The functional connectivity profiles of the three VIP ROIs resembled anatomical connectivity profiles obtained by chemical tracing. Anterior VIP was functionally connected to regions associated with motor, tactile, and proprioceptive processing and with regions involved in reaching, grasping, and processing peripersonal space. Posterior VIP had the strongest functional connectivity to regions involved in motion processing and eye movements. These profiles are consistent with the connectivity profiles of the anterior and posterior VIP areas identified in humans. Intermediate VIP did not exhibit specific connectivity profiles. Viewed together, resting-state functional connectivity, task-related fMRI, and anatomical tracing consistently suggest specific functional specializations of macaque anterior and posterior VIP.

The pulvinar, the largest nucleus of the thalamus, is functionally heterogeneous and involved in multiple cognitive functions. It has been proposed to act as a functional hub of cortical processes due to its extensive reciprocal connectivity with the cortex. However, its role in cognition is not fully understood yet. Here, we posit that an improved understanding of its functional connectivity with the cortex is needed to better capture the cognitive functions of this nucleus. To address this question, we characterize the pulvino-cortical functional connectivity along the ventro-dorsal, antero-posterior, and medio-lateral axes, using awake resting-state data from 10 adult macaques. We first report two global cortical functional connectivity gradients along the antero-posterior and ventro-dorsal pulvinar gradients that match remarkably well the structural connectivity gradients described by anatomical approaches. In addition to these global gradients, multiple local cortical pulvinar projection fields can be identified at the sulci level such as in the lateral sulcus (LS), the intraparietal sulcus (IPS), the principal sulci (PS), and the anterior cingulate cortex (ACC). For most sulci, we show that functional pulvino-cortical projection fields follow the major anatomical axis of these different sulci (e.g., the ventro-dorsal axis for the LS and the antero-posterior axis for the IPS). Other sulci, such as the superior temporal sulcus, the posterior cingulate cortex, or the central sulcus, display multiple projection fields from the pulvinar. Although substantial inter-individual differences exist, the general functional connectivity patterns are remarkably consistent across hemispheres and individuals. Overall, we propose that these multiple pulvinar projection fields correspond to a fundamental principle of pulvino-cortical connectivity and that a better understanding of this connectional organization will shed light on the function of pulvino-cortical interactions and the role of the pulvinar in cognition at large.