Human somatosensory cortex is modulated during motor planning

• Published in: The Journal of neuroscience Vol. 41; no. 27; pp. 5909 - 5922
• Main Authors: Gale, Daniel J, Flanagan, J Randall, Gallivan, Jason P
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 07-07-2021
• Subjects: Activity patterns; Control theory; Cortex (motor); Feedback; Feedback control; Functional magnetic resonance imaging; Hemispheres; Information processing; Motor task performance; Predictive control; Sensory feedback; Sensory integration; Somatosensory cortex; Somatosensory system
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.0342-21.2021

Recent data and motor control theory argues that movement planning involves preparing the neural state of primary motor cortex (M1) for forthcoming action execution. Theories related to internal models, feedback control, and predictive coding also emphasize the importance of sensory prediction (and processing) prior to (and during) the movement itself, explaining why motor-related deficits can arise from damage to primary somatosensory cortex (S1). Motivated by this work, here we examined whether motor planning, in addition to changing the neural state of M1, changes the neural state of S1, preparing it for the sensory feedback that arises during action. We tested this idea in two human functional MRI studies (N=31, 16 female) involving delayed object manipulation tasks, focusing our analysis on pre-movement activity patterns in M1 and S1. We found that the motor effector to be used in the upcoming action could be decoded, well before movement, from neural activity in M1 in both studies. Critically, we found that this effector information was also present, well before movement, in S1. In particular, we found that the encoding of effector information in area 3b (S1 proper) was linked to the contralateral hand, similarly to that found in M1, whereas in areas 1 and 2 this encoding was present in both the contralateral and ipsilateral hemispheres. Together, these findings suggest that motor planning not only prepares the motor system for movement, but also changes the neural state of the somatosensory system, presumably allowing it to anticipate the sensory information received during movement.
Whereas recent work on motor cortex has emphasized the critical role of movement planning in preparing neural activity for movement generation, it has not investigated the extent to which planning also modulates the activity in adjacent primary somatosensory cortex (S1). This reflects a key gap in knowledge, given that recent motor control theories emphasize the importance of sensory feedback processing in effective movement generation. Here we find, through a convergence of experiments and analyses, that the planning of object manipulation tasks, in addition to modulating the activity in motor cortex, changes the state of neural activity in different subfields of human S1. We suggest that this modulation prepares S1 for the sensory information it will receive during action execution.