Motor Cortex Can Directly Drive the Globus Pallidus Neurons in a Projection Neuron Type-dependent Manner in the Rat

Overview

Journal Elife

Specialty Biology

Date 2019 Nov 13

PMID 31711567

Citations 27

Authors

Fuyuki Karube

Susumu Takahashi

Kenta Kobayashi

Fumino Fujiyama

Affiliations

Soon will be listed here.

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.

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References

Arkadir D, Morris G, Vaadia E, Bergman H . Independent coding of movement direction and reward prediction by single pallidal neurons. J Neurosci. 2004; 24(45):10047-56. PMC: 6730185. DOI: 10.1523/JNEUROSCI.2583-04.2004. View

Bevan M, Magill P, Hallworth N, Bolam J, Wilson C . Regulation of the timing and pattern of action potential generation in rat subthalamic neurons in vitro by GABA-A IPSPs. J Neurophysiol. 2002; 87(3):1348-62. DOI: 10.1152/jn.00582.2001. View

DeLong M . Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990; 13(7):281-5. DOI: 10.1016/0166-2236(90)90110-v. View

Ueta Y, Otsuka T, Morishima M, Ushimaru M, Kawaguchi Y . Multiple layer 5 pyramidal cell subtypes relay cortical feedback from secondary to primary motor areas in rats. Cereb Cortex. 2013; 24(9):2362-76. DOI: 10.1093/cercor/bht088. View

Mink J, Thach W . Basal ganglia motor control. I. Nonexclusive relation of pallidal discharge to five movement modes. J Neurophysiol. 1991; 65(2):273-300. DOI: 10.1152/jn.1991.65.2.273. View

Calabresi P, Picconi B, Tozzi A, Ghiglieri V, Di Filippo M . Direct and indirect pathways of basal ganglia: a critical reappraisal. Nat Neurosci. 2014; 17(8):1022-30. DOI: 10.1038/nn.3743. View

Albin R, Young A, Penney J . The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989; 12(10):366-75. DOI: 10.1016/0166-2236(89)90074-x. View

Hanson J, Smith Y, Jaeger D . Sodium channels and dendritic spike initiation at excitatory synapses in globus pallidus neurons. J Neurosci. 2004; 24(2):329-40. PMC: 6729996. DOI: 10.1523/JNEUROSCI.3937-03.2004. View

Mailly P, Aliane V, Groenewegen H, Haber S, Deniau J . The rat prefrontostriatal system analyzed in 3D: evidence for multiple interacting functional units. J Neurosci. 2013; 33(13):5718-27. PMC: 6705071. DOI: 10.1523/JNEUROSCI.5248-12.2013. View

10.

Ebrahimi A, Pochet R, Roger M . Topographical organization of the projections from physiologically identified areas of the motor cortex to the striatum in the rat. Neurosci Res. 1992; 14(1):39-60. DOI: 10.1016/s0168-0102(05)80005-7. View

11.

Li N, Chen T, Guo Z, Gerfen C, Svoboda K . A motor cortex circuit for motor planning and movement. Nature. 2015; 519(7541):51-6. DOI: 10.1038/nature14178. View

12.

Shibata K, Tanaka T, Hioki H, Furuta T . Projection Patterns of Corticofugal Neurons Associated with Vibrissa Movement. eNeuro. 2018; 5(5). PMC: 6220590. DOI: 10.1523/ENEURO.0190-18.2018. View

13.

Petreanu L, Mao T, Sternson S, Svoboda K . The subcellular organization of neocortical excitatory connections. Nature. 2009; 457(7233):1142-5. PMC: 2745650. DOI: 10.1038/nature07709. View

14.

Middleton F, Strick P . Basal-ganglia 'projections' to the prefrontal cortex of the primate. Cereb Cortex. 2002; 12(9):926-35. DOI: 10.1093/cercor/12.9.926. View

15.

Susaki E, Tainaka K, Perrin D, Yukinaga H, Kuno A, Ueda H . Advanced CUBIC protocols for whole-brain and whole-body clearing and imaging. Nat Protoc. 2015; 10(11):1709-27. DOI: 10.1038/nprot.2015.085. View

16.

Isomura Y, Takekawa T, Harukuni R, Handa T, Aizawa H, Takada M . Reward-modulated motor information in identified striatum neurons. J Neurosci. 2013; 33(25):10209-20. PMC: 6618603. DOI: 10.1523/JNEUROSCI.0381-13.2013. View

17.

Goldberg J, Kats S, Jaeger D . Globus pallidus discharge is coincident with striatal activity during global slow wave activity in the rat. J Neurosci. 2003; 23(31):10058-63. PMC: 6740869. View

18.

Isoda M, Hikosaka O . Role for subthalamic nucleus neurons in switching from automatic to controlled eye movement. J Neurosci. 2008; 28(28):7209-18. PMC: 2667154. DOI: 10.1523/JNEUROSCI.0487-08.2008. View

19.

Dodson P, Larvin J, Duffell J, Garas F, Doig N, Kessaris N . Distinct developmental origins manifest in the specialized encoding of movement by adult neurons of the external globus pallidus. Neuron. 2015; 86(2):501-13. PMC: 4416107. DOI: 10.1016/j.neuron.2015.03.007. View

20.

Abdi A, Mallet N, Mohamed F, Sharott A, Dodson P, Nakamura K . Prototypic and arkypallidal neurons in the dopamine-intact external globus pallidus. J Neurosci. 2015; 35(17):6667-88. PMC: 4412890. DOI: 10.1523/JNEUROSCI.4662-14.2015. View