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

Abstract

It is generally supposed that primary motor cortex (M1) receives somatosensory input predominantly via primary somatosensory cortex (S1). However, a growing body of evidence indicates that M1 also receives direct sensory input from the thalamus, independent of S1; such direct input is particularly evident at early ages before M1 contributes to motor control. Here, recording extracellularly from the forelimb regions of S1 and M1 in unanesthetized rats at postnatal day (P)8 and P12, we compared S1 and M1 responses to self-generated (i.e., reafferent) forelimb movements during active sleep and wake, and to other-generated (i.e., exafferent) forelimb movements. At both ages, reafferent responses were processed in parallel by S1 and M1; in contrast, exafferent responses were processed in parallel at P8 but serially, from S1 to M1, at P12. To further assess this developmental difference in processing, we compared exafferent responses to proprioceptive and tactile stimulation. At both P8 and P12, proprioceptive stimulation evoked parallel responses in S1 and M1, whereas tactile stimulation evoked parallel responses at P8 and serial responses at P12. Independent of the submodality of exafferent stimulation, pairs of S1-M1 units exhibited greater coactivation during active sleep than wake. These results indicate that S1 and M1 independently develop somatotopy before establishing the interactive relationship that typifies their functionality in adults.

Identification of a developmental switch in information transfer between whisker S1 and S2 cortex in mice

“…Based on these findings, and recent ones showing the activation of wS2-projecting wS1 neurons upon a whisker touch and the acquisition of texture discrimination, more functional experiments are required in awake behaving mice to determine the direct impact of wS1 activity to wS2 in adulthood. Interestingly, published work has provided some insights into the development of parallel versus sequential activation between somatosensory paw area S1 (pS1) and paw primary motor cortex (pM1) of rat (Gómez et al 2021). The work proposes that at P8, paw sensory stimulation reaches pS1 and pM1 through parallel streams, potentially from the thalamus, whereas at P12 it reaches pM1 via pS1 through a serial activation scheme.…”

“…Furthermore, wS2-projecting wS1 neurons have also been found to be 4 involved in the goal-directed sensorimotor transformation of a whisker touch to licking motor output (Yamashita and Petersen 2016) and show higher choice-related activity than other neurons in layer 2/3 (Kwon et al 2016). Despite of several studies about the development of sensorimotor processing (Dooley and Blumberg 2018;Gómez et al 2021;Khazipov et al 2004), little is known about the developmental stage that wS2 begins processing sensory information coming directly from the thalamus or indirectly via wS1, which would signify the beginning of higher-order representation of tactile stimuli in mammals. One informed hypothesis is that this occurs at the end of the second postnatal week.…”

Developmental onset of a cerebellar-dependent forward model of movement in motor thalamus

“…1D, gray). Although such responses are presumed to arise from thalamus, the thalamic source of sensory inputs to M1, particularly in early development, remains unclear (Gómez et al, 2021). As with M1, neurons in VP and VL also showed increased activity in response to twitches and wake-movements at all three ages (Fig.…”

Neurophysiology of the Developing Cerebral Cortex: What We Have Learned and What We Need to Know

“…Sensory feedback from passive stimulation by littermates trigger cortical activity (Akhmetshina et al, 2016 ). Furthermore, spontaneous self-generated movements (myoclonic twitches) can be already observed very early and play an important role in the development of the sensorimotor system (Inacio et al, 2016 ; Dooley et al, 2020 ; Gomez et al, 2021 ). Head-fixation of newborn rodents allows simultaneous recordings of large-scale neuronal activity and spontaneous movements of the animal's snout including the whiskers, the forelimbs, hindlimbs, and the tail using electromyography (EMG) or multiple video camera monitoring (Dooley and Blumberg, 2018 ; Glanz et al, 2021 ; Gomez et al, 2021 ).…”