Functional specialization of macaque premotor F5 subfields with respect to hand and mouth movements: A comparison of task and resting-state fMRI

Abstract

Based on architectonic, tract-tracing or functional criteria, the rostral portion of ventral premotor cortex in the macaque monkey, also termed area F5, has been divided into several subfields. Cytoarchitectonical investigations suggest the existence of three subfields, F5c (convexity), F5p (posterior) and F5a (anterior). Electrophysiological investigations have suggested a gradual dorso-ventral transition from hand-to mouth-dominated motor fields, with F5p and ventral F5c strictly related to hand movements and mouth movements, respectively. The involvement of F5a in this respect, however, has received much less attention. Recently, data-driven resting-state fMRI approaches have also been used to examine the presence of distinct functional fields in macaque ventral premotor cortex. Although these studies have suggested several functional clusters in/near macaque F5, so far the parcellation schemes derived from these clustering methods do not completely retrieve the same level of F5 specialization as suggested by aforementioned invasive techniques. Here, using seed-based resting-state fMRI analyses, we examined the functional connectivity of different F5 seeds with key regions of the hand and face/ mouth parieto-frontal-insular motor networks. In addition, we trained monkeys to perform either hand grasping or ingestive mouth movements in the scanner in order to compare resting-state with task-derived functional hand and mouth motor networks. In line with previous single-cell investigations, task-fMRI suggests involvement of F5p, dorsal F5c and F5a in the execution of hand grasping movements, while non-communicative mouth movements yielded particularly pronounced responses in ventral F5c. Corroborating with anatomical tracing data of macaque F5 subfields, seed-based resting-state fMRI suggests a transition from predominant functional correlations with the hand-motor network in F5p to mostly mouth-motor network functional correlations in ventral F5c. Dorsal F5c yielded robust functional correlations with both hand-and mouth-motor networks. In addition, the deepest part of the fundus of the inferior arcuate, corresponding to area 44, displayed a strikingly different functional connectivity profile compared to neighboring F5a, suggesting a different functional specialization for these two neighboring regions.

Statistical Learning Signals for Complex Visual Images in Macaque Early Visual Cortex

“…Only in a single hemisphere of M2 did we observe activations in the frontal cortex (Figures 3, 4). A closer examination of these activations showed an overlap with the ventral premotor and the frontal operculum (insular) areas that show orofacial and gustatory responses (Maranesi et al, 2012;Kaskan et al, 2019;Sharma et al, 2019). Such responses in our setup can obviously be related to reward delivery or reward anticipation since the monkey worked for juice reward during the scanning.…”

Cross-species Functional Alignment Reveals Evolutionary Hierarchy Within the Connectome

“…In addition, while the present work addressed issues regarding the reproducibility of findings by replicating analyses in independent samples, our understanding of their functional significance is based on a meta-analysis and so the precise functional meaning of the observed differences remains largely a matter of conjecture 54,79 . In order to fully appreciate the significance of these cross species differences in brain organization for human cognition, it will be necessary to understand how these patterns change across contexts, and, if possible, during active tasks states 80,81 . Understanding how functional patterns change across a common embedded space during periods of task engagement, could provide invaluable insight into how evolution has shaped many important aspects of human cognition 24 .…”

Reproducing macaque lateral grasping and oculomotor networks using resting state functional connectivity and diffusion tractography

“…In most cases, these networks included mostly neighbouring regions, rather than anatomically connected zones, as well as very few distant regions, except for homologous contralateral areas. Sharma and colleagues ( 2019 ) describe different patterns of rs-FC of F5 subdivisions using a contrast agent for enhancing signals in awake macaque monkeys. Their results appear to be very similar to those we observed.…”

“…The previously described limitations appear to be a common problem of rs-FC in macaques, even when different approaches are used (Mars et al 2011;Neubert et al 2014;Hutchison et al 2015;Sharma et al 2019). Using a different rs-FC analysis, not requiring a priori seed definition, Hutchinson and colleagues (2011) defined eleven different networks across the entire macaque cortex.…”