Although input from corticostriatal neurons (CSNs) plays a critical role in
basal ganglia functions, little is known about CSN activity during behavio
r. 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 c
ortex (M1) of two monkeys as they performed a step-tracking task in which s
tatic loads opposed or assisted simple and precued movements of the elbow o
r wrist. Multiple lines of evidence suggested that CSNs and corticopeduncul
ar neurons (CPNs) belong to distinct populations. No cells were activated f
rom both striatum and peduncle. Compared with CPNs, CSNs had slow conductio
n velocities and low spontaneous rates, and the activity of most was unmodu
lated by sensory testing or within the tasks used. CSN activity resembled t
hat described for M1-recipient striatal neurons: perimovement firing was sm
all 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 C
PNs: CSN sensory responses and perimovement activities were often direction
ally specific, CSNs were often activated exclusively by sensory stimulation
, active movement, or movement preparation, and a substantial fraction of C
SNs (19%) was unresponsive to any task or manipulation. Thus, CSNs transmit
signals distinct from those sent to spinal cord/brainstem. The highly sele
ctive activity of CSNs suggests that a discrete (i.e., sparse) code is used
to signal cortical activation states to striatum.