Corticostriatal activity in primary motor cortex of the macaque

Although input from corticostriatal neurons (CSNs) plays a critical role in basal ganglia functions, little is known about CSN activity during behavior. We compared the properties of antidromically identified CSNs with those of antidromically identified neurons that project via the cerebral peduncle to distant targets. Both types of neurons were recorded in primary motor cortex (M1) of two monkeys as they performed a step-tracking task in which static loads opposed or assisted simple and precued movements of the elbow or wrist. Multiple lines of evidence suggested that CSNs and corticopeduncular neurons (CPNs) belong to distinct populations. No cells were activated from both striatum and peduncle. Compared with CPNs, CSNs had slow conduction velocities and low spontaneous rates, and the activity of most was unmodulated by sensory testing or within the tasks used. CSN activity resembled that described for M1-recipient striatal neurons: perimovement firing was small in magnitude, strongly directional, and rarely showed muscle-like load effects. Contrary to a previous report, perimovement activity in most CSNs began before movement onset. CSN activity was more selective than that of CPNs: CSN sensory responses and perimovement activities were often directionally specific, CSNs were often activated exclusively by sensory stimulation, active movement, or movement preparation, and a substantial fraction of CSNs (19%) was unresponsive to any task or manipulation. Thus, CSNs transmit signals distinct from those sent to spinal cord/brainstem. The highly selective activity of CSNs suggests that a discrete (i.e., sparse) code is used to signal cortical activation states to striatum.