Convergent Cortical Innervation of Striatal Projection Neurons

Overview

Journal Nat Neurosci

Date 2013 May 14

PMID 23666180

Citations 73

Authors

Geraldine J Kress

Naoki Yamawaki

David L Wokosin

Ian R Wickersham

Gordon M G Shepherd

D James Surmeier

Affiliations

Soon will be listed here.

Abstract

Anatomical studies have led to the assertion that intratelencephalic and pyramidal tract cortical neurons innervate different striatal projection neurons. To test this hypothesis, we measured the responses of mouse striatal neurons to optogenetic activation of intratelencephalic and pyramidal tract axons. Contrary to expectation, direct and indirect pathway striatal spiny projection neurons responded to both intratelencephalic and pyramidal tract activation, arguing that these cortical networks innervate both striatal projection neurons.

Citing Articles

Globus pallidus is not independent from striatal direct pathway neurons: an up-to-date review.

Fujiyama F, Karube F, Hirai Y Mol Brain. 2024; 17(1):34.

PMID: 38849935 PMC: 11157709. DOI: 10.1186/s13041-024-01107-4.

FOXP1 regulates the development of excitatory synaptic inputs onto striatal neurons and induces phenotypic reversal with reinstatement.

Khandelwal N, Kulkarni A, Ahmed N, Harper M, Konopka G, Gibson J Sci Adv. 2024; 10(18):eadm7039.

PMID: 38701209 PMC: 11068015. DOI: 10.1126/sciadv.adm7039.

Distributed dopaminergic signaling in the basal ganglia and its relationship to motor disability in Parkinson's disease.

Zhai S, Cui Q, Simmons D, Surmeier D Curr Opin Neurobiol. 2023; 83:102798.

PMID: 37866012 PMC: 10842063. DOI: 10.1016/j.conb.2023.102798.

Chronic stress promotes basal ganglia disinhibition by increasing the excitatory drive of direct-pathway neurons.

Rodrigues D, Monteiro P Neurobiol Stress. 2023; 27:100571.

PMID: 37781564 PMC: 10540042. DOI: 10.1016/j.ynstr.2023.100571.

Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways.

Rios A, Nonomura S, Kato S, Yoshida J, Matsushita N, Nambu A Commun Biol. 2023; 6(1):914.

PMID: 37673949 PMC: 10482957. DOI: 10.1038/s42003-023-05288-x.

References

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

Gerfen C, Surmeier D . Modulation of striatal projection systems by dopamine. Annu Rev Neurosci. 2011; 34:441-66. PMC: 3487690. DOI: 10.1146/annurev-neuro-061010-113641. View

Kiritani T, Wickersham I, Seung H, Shepherd G . Hierarchical connectivity and connection-specific dynamics in the corticospinal-corticostriatal microcircuit in mouse motor cortex. J Neurosci. 2012; 32(14):4992-5001. PMC: 3329752. DOI: 10.1523/JNEUROSCI.4759-11.2012. View

Apicella A, Wickersham I, Seung H, Shepherd G . Laminarly orthogonal excitation of fast-spiking and low-threshold-spiking interneurons in mouse motor cortex. J Neurosci. 2012; 32(20):7021-33. PMC: 3377057. DOI: 10.1523/JNEUROSCI.0011-12.2012. View

Wilson C . Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J Comp Neurol. 1987; 263(4):567-80. DOI: 10.1002/cne.902630408. View

Morita K, Morishima M, Sakai K, Kawaguchi Y . Reinforcement learning: computing the temporal difference of values via distinct corticostriatal pathways. Trends Neurosci. 2012; 35(8):457-67. DOI: 10.1016/j.tins.2012.04.009. View

Reiner A, Hart N, Lei W, Deng Y . Corticostriatal projection neurons - dichotomous types and dichotomous functions. Front Neuroanat. 2010; 4:142. PMC: 2982718. DOI: 10.3389/fnana.2010.00142. View

Graybiel A, Aosaki T, Flaherty A, Kimura M . The basal ganglia and adaptive motor control. Science. 1994; 265(5180):1826-31. DOI: 10.1126/science.8091209. View

Wickersham I, Sullivan H, Seung H . Production of glycoprotein-deleted rabies viruses for monosynaptic tracing and high-level gene expression in neurons. Nat Protoc. 2010; 5(3):595-606. DOI: 10.1038/nprot.2009.248. View

10.

Heintz N . BAC to the future: the use of bac transgenic mice for neuroscience research. Nat Rev Neurosci. 2001; 2(12):861-70. DOI: 10.1038/35104049. View

11.

Suter B, OConnor T, Iyer V, Petreanu L, Hooks B, Kiritani T . Ephus: multipurpose data acquisition software for neuroscience experiments. Front Neural Circuits. 2011; 4:100. PMC: 3176413. DOI: 10.3389/fncir.2010.00100. View

12.

Shepherd G . Corticostriatal connectivity and its role in disease. Nat Rev Neurosci. 2013; 14(4):278-91. PMC: 4096337. DOI: 10.1038/nrn3469. View

13.

Lei W, Jiao Y, Del Mar N, Reiner A . Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J Neurosci. 2004; 24(38):8289-99. PMC: 6729697. DOI: 10.1523/JNEUROSCI.1990-04.2004. View

14.

Ballion B, Mallet N, Bezard E, Lanciego J, Gonon F . Intratelencephalic corticostriatal neurons equally excite striatonigral and striatopallidal neurons and their discharge activity is selectively reduced in experimental parkinsonism. Eur J Neurosci. 2008; 27(9):2313-21. DOI: 10.1111/j.1460-9568.2008.06192.x. View

15.

Reiner A, Jiao Y, Del Mar N, Laverghetta A, Lei W . Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J Comp Neurol. 2003; 457(4):420-40. DOI: 10.1002/cne.10541. View

16.

Cui G, Jun S, Jin X, Pham M, Vogel S, Lovinger D . Concurrent activation of striatal direct and indirect pathways during action initiation. Nature. 2013; 494(7436):238-42. PMC: 4039389. DOI: 10.1038/nature11846. View