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

Abstract

To understand how the information derived from different motor cortical areas representing different body parts is organized in the basal ganglia, we examined the neuronal responses in the subthalamic nucleus (STN), and the external (GPe) and internal (GPi) segments of the globus pallidus (input, relay and output nuclei, respectively) to stimulation of the orofacial, forelimb and hindlimb regions of the primary motor cortex (MI) and supplementary motor area (SMA) in macaque monkeys under the awake state. Most STN and GPe/GPi neurons responded exclusively to stimulation of either the MI or SMA, and one-fourth to one-third of neurons responded to both. STN neurons responding to the hindlimb, forelimb and orofacial regions of the MI were located along the medial-lateral axis in the posterolateral STN, while neurons responding to the orofacial region of the SMA were located more medially than the others in the anteromedial STN. GPe/GPi neurons responding to the hindlimb, forelimb and orofacial regions of the MI were found along the dorsal-ventral axis in the posterolateral GPe/GPi, and neurons responding to the corresponding regions of the SMA were similarly but less clearly distributed in more anteromedial regions. Moreover, neurons responding to the distal and proximal forelimb MI regions were found along the lateral-medial axis in the STN and the ventral-dorsal axis in the GPe/GPi. Most STN and GPe/GPi neurons showed kinaesthetic responses with similar somatotopic maps. These observations suggest that the somatotopically organized inputs from the MI and SMA are well preserved in the STN and GPe/GPi with partial convergence.

Weakly correlated activity of pallidal neurons in behaving monkeys

“…The response pattern was typically triphasic, that is, early excitation followed by inhibition and late excitation (Figure 2a), as reported previously (Nambu et al, 2000; Iwamuro et al, 2017). The latency and duration of these response components are shown in Table 2, and results agree with previous studies (Nambu et al, 2000; Iwamuro et al, 2017). The mean spontaneous firing rates of GPe neurons were 71 ± 29 ( Monkey H ) and 91 ± 28 ( Monkey L ) Hz, and those of GPi neurons were 75 ± 25 ( H ) and 100 ± 26 ( L ) Hz, which also agree with the previous studies.…”

“…Most of them (199/219, 91%; GPe, 123/140, 88%; GPi, 76/79, 96%) responded to both M1 and SMA stimulation. The response pattern was typically triphasic, that is, early excitation followed by inhibition and late excitation (Figure 2a), as reported previously (Nambu et al, 2000;Iwamuro et al, 2017). The latency and duration of these response components are shown in Table 2, and results agree with previous studies (Nambu et al, 2000;Iwamuro et al, 2017).…”

Transient response of basal ganglia network in healthy and low-dopamine state

“…The triphasic response is consistent with the predictions of a simple feedforward model of the BG involving the so-called direct, indirect and hyper-direct pathway (Albin et al, 1989;Jaeger and Kita, 2011). However, individual neurons in SNr (Sano and Nambu, 2019) or GPi (Iwamuro et al, 2017) can show biphasic or monophasic responses. In dopamine depleted conditions, the fraction of neurons showing biphasic and monophasic responses is changed resulting in an altered population response.…”

Cortical Projection From the Premotor or Primary Motor Cortex to the Subthalamic Nucleus in Intact and Parkinsonian Adult Macaque Monkeys: A Pilot Tracing Study

“…The majority of motor cortical inputs to the basal ganglia are directed to the striatum (e.g., Künzle, 1975;McGuire et al, 1991;Inase et al, 1996Inase et al, , 1999Takada et al, 1998a,b;Tokuno et al, 1999;Nambu et al, 2002a;Tachibana et al, 2004;Parent and Parent, 2006;Raju et al, 2008;Gerbella et al, 2016;Innocenti et al, 2017). However, other cortical projections to the basal ganglia reach the subthalamic nucleus (STN), via corticosubthalamic projections (CSTPs) originating from the primary motor cortex (M1), the supplementary motor areas (SMA-proper and pre-SMA), the premotor cortex (PM), and the cingulate motor areas, representing a hyper direct pathway parallel to the classic direct and indirect pathways (Nambu et al, 1996(Nambu et al, , 1997(Nambu et al, , 2000(Nambu et al, , 2002bInase et al, 1999;Takada et al, 2001;Miyachi et al, 2006;Degos et al, 2008;Inoue et al, 2012;Iwamuro et al, 2017;Coudé et al, 2018;Temiz et al, 2020).…”