Differential activity patterns of putaminal neurons with inputs from the primary motor cortex and supplementary motor area in behaving monkeys

Abstract

Takara S, Hatanaka N, Takada M, Nambu A. Differential activity patterns of putaminal neurons with inputs from the primary motor cortex and supplementary motor area in behaving monkeys. J Neurophysiol 106: 1203-1217, 2011. First published June 8, 2011 doi:10.1152/jn.00768.2010.-Activity patterns of projection neurons in the putamen were investigated in behaving monkeys. Stimulating electrodes were implanted chronically into the proximal (MI proximal ) and distal (MI distal ) forelimb regions of the primary motor cortex (MI) and the forelimb region of the supplementary motor area (SMA). Cortical inputs to putaminal neurons were identified by excitatory orthodromic responses to stimulation of these motor cortices. Then, neuronal activity was recorded during the performance of a goaldirected reaching task with delay. Putaminal neurons with inputs from the MI and SMA showed different activity patterns, i.e., movementand delay-related activity, during task performance. MI-recipient neurons increased activity in response to arm-reach movements, whereas SMA-recipient neurons increased activity during delay periods, as well as during movements. The activity pattern of MI ϩ SMA-recipient neurons was of an intermediate type between those of MI-and SMA-recipient neurons. Approximately one-half of MI proximal -, SMA-, and MI ϩ SMA-recipient neurons changed activities before the onset of movements, whereas a smaller number of MI distal -and MI proximal ϩ distal -recipient neurons did. Movementrelated activity of MI-recipient neurons was modulated by target directions, whereas SMA-and MI ϩ SMA-recipient neurons had a lower directional selectivity. MI-recipient neurons were located mainly in the ventrolateral part of the caudal aspect of the putamen, whereas SMA-recipient neurons were located in the dorsomedial part. MI ϩ SMA-recipient neurons were found in between. The present results suggest that a subpopulation of putaminal neurons displays specific activity patterns depending on motor cortical inputs. Each subpopulation receives convergent or nonconvergent inputs from the MI and SMA, retains specific motor information, and sends it to the globus pallidus and the substantia nigra through the direct and indirect pathways of the basal ganglia. basal ganglia; striatum; motor control; single-unit recording THE PRIMATE STRIATUM, composed of the putamen, the caudate nucleus, and the ventral striatum, is a main input station of the basal ganglia and receives neural signals from wide areas of the cerebral cortex. Every single striatal projection neuron is estimated to receive diverse inputs from ϳ750 to 7,500 cortical neurons (Bennet and Wilson 2000), and thus cortical information is massively integrated within the striatum. The activity of striatal projection neurons is strongly modulated by local interneurons that also receive cortical inputs (Tepper et al. 2008). The projection neurons finally send processed signals to the external and internal segments of the globus pallidus and the substantia nigra pars reticulata through the ...

Information processing from the motor cortices to the subthalamic nucleus and globus pallidus and their somatotopic organizations revealed electrophysiologically in monkeys

“…Cortical stimulation (300‐μs duration, single pulse, 0.7‐mA strength, at 0.7 Hz) was delivered via the stimulating electrodes implanted in the MI and SMA. These stimulation parameters were determined by a series of our previous studies (Nambu et al ., , ; Kita et al ., , ; Tachibana et al ., ; Takara et al ., ). Neuronal responses to cortical stimulation were examined and stored on the computer with constructing peristimulus time histograms (PSTHs; bin width of 1 ms; sum of 100 times).…”

“…The lesions made by current injection and traces of electrode tracks were identified. The recording sites were reconstructed according to histological data as well as MRI images (Nambu et al ., , ; Tachibana et al ., ; Takara et al ., ). The positions of the cortical stimulating electrodes were also histologically confirmed.…”

“…Another key concept of basal ganglia circuitry is somatotopic organization. Somatotopy in the striatum has been confirmed by both anatomical and electrophysiological studies (Künzle, ; Alexander & DeLong, ; Alexander & Crutcher, ; Flaherty & Graybiel, ; Takada et al ., ; Nambu et al ., ; Takara et al ., ). Somatotopy in the STN has also been revealed by anatomical and electrophysiological studies (Monakow et al ., ; DeLong et al ., ; Wichmann et al ., ; Nambu et al ., ).…”

Functional Circuitry of the Basal Ganglia

“…The somatotopy in the putamen is also confi rmed by electrophysiological methods. PANs in the somatomotor territories are activated by active and/or passive movements of the corresponding body parts on the contralateral side (Nambu et al 2002b ;Takara et al 2011 ), while TANs respond to novel acoustic and visual stimuli (Aosaki et al 1995 ). Microstimulation in the somatomotor territories of the putamen produces movements of the corresponding body parts A. Nambu (Alexander and DeLong 1985 ;Nambu et al 2002b ).…”