Abstract
The basal ganglia are critical for the control of motor behaviors and for reinforcement learning. Here, we demonstrate in rats that primary and secondary motor areas (M1 and M2) make functional synaptic connections in the globus pallidus (GP), not usually thought of as an input site of the basal ganglia. Morphological observation revealed that the density of axonal boutons from motor cortices in the GP was 47% and 78% of that in the subthalamic nucleus (STN) from M1 and M2, respectively. Cortical excitation of GP neurons was comparable to that of STN neurons in slice preparations. FoxP2-expressing arkypallidal neurons were preferentially innervated by the motor cortex. The connection probability of cortico-pallidal innervation was higher for M2 than M1. These results suggest that cortico-pallidal innervation is an additional excitatory input to the basal ganglia, and that it can affect behaviors via the cortex-basal ganglia-thalamus motor loop.
Highlights
Parallel loops of neural connections among the cerebral cortex, basal ganglia, and thalamus contribute to multiple aspects of behavior (Alexander, DeLong, & Strick, 1986; Nambu, 2008; Wei & Wang, 2016)
Using a combination of neural tracing with immunofluorescence, we demonstrate that M1 and M2 project to different subregions of each basal ganglia nucleus, and that in the globus pallidus (GP), cortical axon collaterals and boutons have topographic distributions that depend on the cortical area of origin (Naito & Kita, 1994)
We found that 60 bi-directionally projecting GP neurons (GPBi) received cortical inputs (7/10 for M1 and 7/9 for M2; N = 3 rats for each), and most of them exhibited an optically evoked excitatory postsynaptic currents (EPSCs) (oEPSC) with small amplitude (Fig. 5C)
Summary
Parallel loops of neural connections among the cerebral cortex, basal ganglia, and thalamus contribute to multiple aspects of behavior (Alexander, DeLong, & Strick, 1986; Nambu, 2008; Wei & Wang, 2016). According to the traditional model, the direct pathway promotes the execution of desired actions, whereas the indirect pathway prevents the execution of competing actions (Friend & Kravitz, 2014; Nambu, 2007; Vicente et al, 2016), and the hyperdirect pathway emergently cancels or switches imminent movements (Frank, Samanta, Moustafa, & Sherman, 2007; Isoda & Hikosaka, 2008; Nambu et al., 2002; Schmidt, Leventhal, Mallet, Chen, & Berke, 2013) In this regard, basal ganglia activity and function are likely modulated by the cerebral cortex
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