Decoding Grasping Movements from the Parieto-Frontal Reaching Circuit in the Nonhuman Primate

Abstract

Prehension movements typically include a reaching phase, guiding the hand toward the object, and a grip phase, shaping the hand around it. The dominant view posits that these components rely upon largely independent parieto-frontal circuits: a dorso-medial circuit involved in reaching and a dorso-lateral circuit involved in grasping. However, mounting evidence suggests a more complex arrangement, with dorso-medial areas contributing to both reaching and grasping. To investigate the role of the dorso-medial reaching circuit in grasping, we trained monkeys to reach-and-grasp different objects in the dark and determined if hand configurations could be decoded from functional magnetic resonance imaging (MRI) responses obtained from the reaching and grasping circuits. Indicative of their established role in grasping, object-specific grasp decoding was found in anterior intraparietal (AIP) area, inferior parietal lobule area PFG and ventral premotor region F5 of the lateral grasping circuit, and primary motor cortex. Importantly, the medial reaching circuit also conveyed robust grasp-specific information, as evidenced by significant decoding in parietal reach regions (particular V6A) and dorsal premotor region F2. These data support the proposed role of dorso-medial "reach" regions in controlling aspects of grasping and demonstrate the value of complementing univariate with more sensitive multivariate analyses of functional MRI (fMRI) data in uncovering information coding in the brain.

Preparatory activity for purposeful arm movements in the dorsomedial parietal area V6A: Beyond the online guidance of movement

“…Interestingly, a very recent study using magneto-encephalography (MEG) in humans has demonstrated that both the dorsolateral (putative grasping) and the dorsomedial (putative reaching) stream play a critical role in planning of non-visually guided reaching vs. grasping actions 72 . Once again, this notion corroborates the hypothesis that grasping information is coded within both pathways, in line with multiple recent evidence collected both in human 40 , 54 , 73 – 75 and monkey studies 4 , 19 , 42 , 76 , 77 .…”

“…While some neurons showed a strong preference for reach-to-grasp movements, others showed a strong preference for reach-to-press movements. In line with increasing evidence for a significant role of area V6A and, more generally, of the dorsomedial visual pathway in the encoding of grasping movements 4 , 19 , 41 , 42 , the majority of cells with significant task-related activity showed a preference for the Reach-to-Grasp task. Accordingly, the entire population of cells showing task effects showed higher activation while the monkey was preparing the execution of a reach-to-grasp action (see Fig.…”

“…In essence, activity measured in aSPOC before movement execution seems to selectively encode specific motor programs that require planning of arm direction, hand preshaping and grip selection 38 , 40 , in other words movement preparation. Along these lines, recent studies in the macaque monkey have demonstrated that information for grasping, notably differentiating grip configurations, is reliably decoded from population neural activity acquired from macaque area V6A in a pre-movement phase (as well as during other task epochs) of a grasping task 41 , 42 .…”

Action Categorization in Rhesus Monkeys: discrimination of grasping from non-grasping manual motor acts

“…The monkey subjects were accustomed to sitting in a sphinx position in a plastic monkey chair, directly facing a liquid crystal display (LCD) screen (60 Hz frame rate), which was positioned at 57 cm from the monkeys‘ eyes 28 , 29 . During initial training, they were required to maintain fixation within a 2° × 2° window centered on a red fixation target (size: 0.18° × 0.18°) in the middle of the screen.…”

Corticocortical Systems Underlying High-Order Motor Control

“…These convey the outflow of parietofrontal operations to subcortical centers and to the spinal cord. The analysis of the functional properties of cells in the many reach-related parietal and frontal areas and the study of their connections indicate that fast reaching and its online control are primarily encoded by a DRS (Caminiti et al, 2017), which also incorporate a grasping-related component (Filippini et al, 2017;Breveglieri et al, 2018;Nelissen et al, 2018), probably subserving an early coordination of reaching and grasping. This view on the DRS is also supported by the effects of reversible inactivation in monkeys, which mimics the defective online control of eye and arm movement (Battaglia-Mayer et al, 2013) typical of patients with parietal lesions resulting in optic ataxia (Balint, 1909;Pisella et al, 2000;Gréa et al, 2002;Buiatti et al, 2013).…”