Wei Liang’s research while affiliated with University of Chicago and other places

Propagating spatiotemporal neural patterns are widely evident across sensory, motor, and association cortical areas. However, it remains unclear whether any characteristics of neural propagation carry information about specific behavioral details. Here, we provide the first evidence for a link between the direction of cortical propagation and specific behavioral features of an upcoming movement on a trial-by-trial basis. We recorded local field potentials (LFPs) from multielectrode arrays implanted in the primary motor cortex of two rhesus macaque monkeys while they performed a 2D reach task. Propagating patterns were extracted from the information-rich high-gamma band (200 to 400 Hz) envelopes in the LFP amplitude. We found that the exact direction of propagating patterns varied systematically according to initial movement direction, enabling kinematic predictions. Furthermore, characteristics of these propagation patterns provided additional predictive capability beyond the LFP amplitude themselves, which suggests the value of including mesoscopic spatiotemporal characteristics in refining brain-machine interfaces.

The primary motor cortex (M1) is known to be spatially organized in terms of muscles and body parts, notwithstanding some overlap. However, the classical view is largely static, neglecting potential representational changes on a fast time scale. To address potential representational dynamics, we probed the mutual information between M1 signals recorded across the cortical sheet and electromyography (EMG) activity from a set of muscles while a macaque monkey performed planar reaches. Here, we demonstrated that the spatial organization of the M1 encoding was in fact quite dynamic throughout the course of a reaching movement such that a given cortical site maximally encoded different muscles at different times. Despite these rapid representational changes, a proximal-to-distal gradient of the upper limb representation was preserved particularly close to movement onset. Representation was most stable close to movement onset, with characteristic topographic maps, possibly serving functional needs. This study bridges the important gap between flexible motor encoding and static motor maps, emphasizing the importance of considering space and time together in motor representation studies.

Voluntary movement initiation involves the modulations of large groups of neurons in the primary motor cortex (M1). Yet similar modulations occur during movement planning when no movement occurs. Here, we show that a sequential spatiotemporal pattern of excitability propagates across M1 prior to the movement initiation in one of two oppositely oriented directions along the rostro-caudal axis. Using spatiotemporal patterns of intracortical microstimulation, we find that reaction time increases significantly when stimulation is delivered against, but not with, the natural propagation direction. Functional connections among M1 units emerge at movement that are oriented along the same rostro-caudal axis but not during movement planning. Finally, we show that beta amplitude profiles can more accurately decode muscle activity when they conform to the natural propagating patterns. These findings provide the first causal evidence that large-scale, propagating patterns of cortical excitability are behaviorally relevant and may be a necessary component of movement initiation.

Voluntary movement initiation involves the modulation of neurons in the primary motor cortex (M1) around movement onset. Yet, similar modulations of M1 activity occur during movement planning when no movement occurs. Here, we show that a sequential spatio-temporal pattern of excitability based on beta oscillation amplitude attenuation propagates across M1 prior to the initiation of reaching movements in one of two oppositely oriented directions along the rostro-caudal axis. Using spatiotemporal patterns of intracortical microstimulation, we find that reaction time increases significantly when stimulation is delivered against but not with the natural propagation orientation suggesting that movement initiation requires a precise recruitment pattern in M1. Functional connections among M1 units emerge at movement onset that are oriented along the same rostro-caudal axis but not during movement planning. Finally, we show that beta amplitude profiles can more accurately decode muscle activity when these patterns conform to the natural propagating patterns. These findings provide the first causal evidence that large-scale, spatially organized propagating patterns of cortical excitability and activity are behaviorally relevant and may be a necessary component of movement initiation.