The relative contributions of different sensory afferent and corticocortical projections on the motor cortex during skilled motor behaviour

Abstract

The motor system is required to perform an endless number of movements. To do this, general motor plans are created for similar groups of movements that can be adjusted for specific iterations of each movement. To ensure that the motor plan is accurate to the specific iteration of the movement, sensory information from a variety of modalities is integrated into the plan via corticocortical connections to the motor cortex. Shorter sensorimotor loops will also project to various cortical areas involved in generating the motor plan to modulate this process with updated sensory afference. However, it is still unclear exactly how these circuits interact with each other during the planning and execution of skilled motor behaviour. The current study used two transcranial magnetic stimulation paradigms to investigate these interactions. Short-interval intracortical inhibition (SICI) probes the longer corticocortical loops, while short-latency afferent inhibition (SAI) probes the shorter sensory afferent circuits. Performing both techniques during a waveform tracking task involving a planning phase and movement execution phase, the current study could investigate interactions between corticocortical and sensory afferent projections during skilled motor behaviour. Twenty-three healthy individuals completed two sessions where SICI and SAI were quantified in the first dorsal interosseous muscle during a waveform tracking task. SICI was assessed using an unbalanced transcranial magnetic stimulus that induced a posterior-anterior current in the underlying tissue with a positive phase lasting 70 µs (PA70). SAI was assessed using a stimulus that induced a posterior-anterior current in the underlying tissue with a positive phase lasting 120 µs (PA120) or a stimulus that induced an anterior-posterior current in the underlying tissue with a positive phase lasting 30 µs (AP30). TMS stimuli were delivered at seven different time points during the task: one baseline time point where the waveform was hidden from participants, two planning time points (-0.5s and -0.25s from movement onset), a time point at the onset of the movement, and three time points during the movement (1s, 2s, 3s after movement onset). Results showed that the effect of the conditioning stimulus was stronger for SICI than SAI across each of the time points during the task. We also found that the magnitude of difference in the weighting of SICI and SAI changed across the time point. These findings suggest that a variety of sensorimotor loops converge on the corticospinal neuron in the primary motor cortex to shape motor output. The corticocortical connections probed by SICI play a dominant role consistent with setting the initial motor plan. In contrast, the sensory afferent projections probed by SAI play a modulatory role updating the initial plan to reflect current sensory states and providing feedback. The interactions between corticocortical and sensory afferent circuits are important for healthy motor control and explain how the motor system is able to perform a seemingly endless number of movements.