Distributed Motor Control of Limb Movements in Rat Motor and Somatosensory Cortex: The Sensorimotor Amalgam Revisited

Abstract

Which areas of the neocortex are involved in the control of movement, and how is motor cortex organized across species? Recent studies using long-train intracortical microstimulation demonstrate that in addition to M1, movements can be elicited from somatosensory regions in multiple species. In the rat, M1 hindlimb and forelimb movement representations have long been thought to overlap with somatosensory representations of the hindlimb and forelimb in S1, forming a partial sensorimotor amalgam. Here we use long-train intracortical microstimulation to characterize the movements elicited across frontal and parietal cortex. We found that movements of the hindlimb, forelimb, and face can be elicited from both M1 and histologically defined S1 and that representations of limb movement types are different in these two areas. Stimulation of S1 generates retraction of the contralateral forelimb, while stimulation of M1 evokes forelimb elevation movements that are often bilateral, including a rostral region of digit grasping. Hindlimb movement representations include distinct regions of hip flexion and hindlimb retraction evoked from S1 and hip extension evoked from M1. Our data indicate that both S1 and M1 are involved in the generation of movement types exhibited during natural behavior. We draw on these results to reconsider how sensorimotor cortex evolved.

Cortical connections of the functional domain for climbing or running in posterior parietal cortex of galagos

“…A lateral to medial progression of domains in motor and premotor cortex reflects a crude somatotopic pattern from the face to hindlimbs in all stimulated primates, as has long been observed in short‐train stimulation studies (for review, see Graziano, 2009). Microstimulation of PPC and motor cortex in non‐primate mammals reveal similar results of movement representation from face to limbs in lateral to medial sequences, indicating that those features emerged in mammalian evolution before the emergence of primates (Baldwin, Cooke, & Krubitzer, 2017; Halley, Baldwin, Cooke, Englund, & Krubitzer, 2020).…”

Evolution of behavioural control from chordates to primates

“…Figure 6a shows a simplified schematic of the forebrain organization in the putative last common ancestor of mammals. The parcellation of neocortical regions is based on studies in marsupials [158][159][160][161] and their comparison with monotremes [162,163] and placentals [164][165][166]. In particular, note the central 'core' island of neocortex (light tan), bordered on the medial side by agranular mesocortical regions (dark tan) corresponding to infra/pre-limbic, anterior cingulate, mid-cingulate and retrosplenial cortex, and on the lateral side by regions derived from the LPall (violet) including the agranular orbital, agranular insular and perirhinal cortex [74,151].…”

Parallel and Serial Sensory Processing in Developing Primary Somatosensory and Motor Cortex

“…For example, S1 sends excitatory axonal projections to M1 (Hooks et al, 2011;Mao et al, 2011;Rocco-Donovan et al, 2011), ablating S1 reduces or abolishes activity in M1 (Goldring et al, 1970;Farkas et al, 1999), silencing S1 impairs motor adaptation (Sakamoto et al, 1989;Mathis et al, 2017), and the latency of evoked and spontaneous sensory responses is typically shorter in S1 than M1 (Ferezou et al, 2007;Chakrabarti et al, 2008;McVea et al, 2012;An et al, 2014). However, the existence of short-latency sensory responses in M1 (Asanuma et al, 1979;Horne and Tracey, 1979;Lemon and van der Burg, 1979;Tracey et al, 1980;Herman et al, 1985;Asanuma and Mackel, 1989) and evidence of S1's role in motor control (Sasaki and Gemba, 1984;Matyas et al, 2010;Halley et al, 2020) suggest that the conventional division of S1 and M1 into distinct sensory and motor areas, respectively, is questionable (Hatsopoulos and Suminski, 2011;Ebbesen et al, 2018).…”