Balanced Activity in Basal Ganglia Projection Pathways is Critical for Contraversive Movements

Overview

Journal Nat Commun

Specialty Biology

Date 2014 Jul 9

PMID 25002180

Citations 105

Authors

Fatuel Tecuapetla

Sara Matias

Guillaume P Dugue

Zachary F Mainen

Rui M Costa

Affiliations

Soon will be listed here.

Abstract

The basal ganglia, and the striatum in particular, have been implicated in the generation of contraversive movements. The striatum projects to downstream basal ganglia nuclei through two main circuits, originating in striatonigral and striatopallidal neurons, and different models postulate that the two pathways can work in opposition or synergistically. Here we show striatonigral and striatopallidal neurons are concurrently active during spontaneous contraversive movements. Furthermore, we show that unilateral optogenetic inhibition of either or both projection pathways disrupts contraversive movements. Consistently, simultaneous activation of both neuron types produces contraversive movements. Still, we also show that imbalanced activity between the pathways can result in opposing movements being driven by each projection pathway. These data show that balanced activity in both striatal projection pathways is critical for the generation of contraversive movements and highlights that imbalanced activity between the two projection pathways can result in opposing motor output.

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References

Heilman K, Bowers D, Coslett H, Whelan H, Watson R . Directional hypokinesia: prolonged reaction times for leftward movements in patients with right hemisphere lesions and neglect. Neurology. 1985; 35(6):855-9. DOI: 10.1212/wnl.35.6.855. View

Durieux P, Schiffmann S, de Kerchove dExaerde A . Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions. EMBO J. 2011; 31(3):640-53. PMC: 3273396. DOI: 10.1038/emboj.2011.400. View

Alexander G, Crutcher M . Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990; 13(7):266-71. DOI: 10.1016/0166-2236(90)90107-l. View

Nambu A . Seven problems on the basal ganglia. Curr Opin Neurobiol. 2008; 18(6):595-604. DOI: 10.1016/j.conb.2008.11.001. View

Gong S, Doughty M, Harbaugh C, Cummins A, Hatten M, Heintz N . Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci. 2007; 27(37):9817-23. PMC: 6672645. DOI: 10.1523/JNEUROSCI.2707-07.2007. View

Wichmann T, DeLong M . Functional and pathophysiological models of the basal ganglia. Curr Opin Neurobiol. 1996; 6(6):751-8. DOI: 10.1016/s0959-4388(96)80024-9. View

Aravanis A, Wang L, Zhang F, Meltzer L, Mogri M, Schneider M . An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J Neural Eng. 2007; 4(3):S143-56. DOI: 10.1088/1741-2560/4/3/S02. View

Gerfen C, Engber T, Mahan L, Susel Z, Chase T, Monsma Jr F . D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science. 1990; 250(4986):1429-32. DOI: 10.1126/science.2147780. 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

10.

Schwarcz R, Fuxe K, Agnati L, Hokfelt T, Coyle J . Rotational behaviour in rats with unilateral striatal kainic acid lesions: a behavioural model for studies on intact dopamine receptors. Brain Res. 1979; 170(3):485-95. DOI: 10.1016/0006-8993(79)90966-1. View

11.

Mink J . The Basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch Neurol. 2003; 60(10):1365-8. DOI: 10.1001/archneur.60.10.1365. View

12.

Karnath H, Himmelbach M, Rorden C . The subcortical anatomy of human spatial neglect: putamen, caudate nucleus and pulvinar. Brain. 2002; 125(Pt 2):350-60. DOI: 10.1093/brain/awf032. View

13.

Kravitz A, Freeze B, Parker P, Kay K, Thwin M, Deisseroth K . Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature. 2010; 466(7306):622-6. PMC: 3552484. DOI: 10.1038/nature09159. View

14.

Sano H, Chiken S, Hikida T, Kobayashi K, Nambu A . Signals through the striatopallidal indirect pathway stop movements by phasic excitation in the substantia nigra. J Neurosci. 2013; 33(17):7583-94. PMC: 6619573. DOI: 10.1523/JNEUROSCI.4932-12.2013. View

15.

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

16.

Brasted P, Humby T, Dunnett S, Robbins T . Unilateral lesions of the dorsal striatum in rats disrupt responding in egocentric space. J Neurosci. 1997; 17(22):8919-26. PMC: 6573075. View

17.

Thanos P, Jhamandas K, Beninger R . N-methyl-D-aspartate unilaterally injected into the dorsal striatum of rats produces contralateral circling: antagonism by 2-amino-7-phosphonoheptanoic acid and cis-flupenthixol. Brain Res. 1992; 589(1):55-61. DOI: 10.1016/0006-8993(92)91161-7. View

18.

Mallet N, Micklem B, Henny P, Brown M, Williams C, Bolam J . Dichotomous organization of the external globus pallidus. Neuron. 2012; 74(6):1075-86. PMC: 3407962. DOI: 10.1016/j.neuron.2012.04.027. View

19.

Atasoy D, Aponte Y, Su H, Sternson S . A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J Neurosci. 2008; 28(28):7025-30. PMC: 2593125. DOI: 10.1523/JNEUROSCI.1954-08.2008. View

20.

Taverna S, Ilijic E, Surmeier D . Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson's disease. J Neurosci. 2008; 28(21):5504-12. PMC: 3235738. DOI: 10.1523/JNEUROSCI.5493-07.2008. View