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Cover ArticleResearch Articles, Systems/Circuits

The Tail of the Mouse Striatum Contains a Novel Large Type of GABAergic Neuron Incorporated in a Unique Disinhibitory Pathway That Relays Auditory Signals to Subcortical Nuclei

Shigeru Ogata, Yuta Miyamoto, Naoki Shigematsu, Shigeyuki Esumi and Takaichi Fukuda
Journal of Neuroscience 26 October 2022, 42 (43) 8078-8094; DOI: https://doi.org/10.1523/JNEUROSCI.2236-21.2022
Shigeru Ogata
Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto 860-8556, Japan
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Yuta Miyamoto
Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto 860-8556, Japan
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Naoki Shigematsu
Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto 860-8556, Japan
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Shigeyuki Esumi
Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto 860-8556, Japan
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Takaichi Fukuda
Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto 860-8556, Japan
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Abstract

The most caudal part of the striatum in rodents, the tail of the striatum (TS), has many features that distinguish it from the rostral striatum, such as its biased distributions of dopamine receptor subtypes, lack of striosomes and matrix compartmentalization, and involvement in sound-driven behaviors. However, information regarding the TS is still limited. We demonstrate in this article that the TS of the male mouse contains GABAergic neurons of a novel type that were detected immunohistochemically with the neurofilament marker SMI-32. Their somata were larger than cholinergic giant aspiny neurons, were located in a narrow space adjacent to the globus pallidus (GP), and extended long dendrites laterally toward the intermediate division (ID) of the trilaminar part of the TS, the region targeted by axons from the primary auditory cortex (A1). Although vesicular glutamate transporter 1-positive cortical axon terminals rarely contacted these TS large (TSL) neurons, glutamic acid decarboxylase-immunoreactive and enkephalin-immunoreactive boutons densely covered somata and dendrites of TSL neurons, forming symmetrical synapses. Analyses of GAD67-CrePR knock-in mice revealed that these axonal boutons originated from nearby medium spiny neurons (MSNs) in the ID. All MSNs examined in the ID in turn received inputs from the A1. Retrograde tracers injected into the rostral zona incerta and ventral medial nucleus of the thalamus labeled somata of TSL neurons. TSL neurons share many morphological features with GP neurons, but their strategically located dendrites receive inputs from closely located MSNs in the ID, suggesting faster responses than distant GP neurons to facilitate auditory-evoked, prompt disinhibition in their targets.

SIGNIFICANCE STATEMENT This study describes a newly found population of neurons in the mouse striatum, the brain region responsible for appropriate behaviors. They are large GABAergic neurons located in the most caudal part of the striatum [tail of the striatum (TS)]. These TS large (TSL) neurons extended dendrites toward a particular region of the TS where axons from the primary auditory cortex (A1) terminated. These dendrites received direct synaptic inputs heavily from nearby GABAergic neurons of the striatum that in turn received inputs from the A1. TSL neurons sent axons to two subcortical regions outside basal ganglia, one of which is related to arousal. Specialized connectivity of TSL neurons suggests prompt disinhibitory actions on their targets to facilitate sound-evoked characteristic behaviors.

  • auditory
  • basal ganglia
  • enkephalin
  • GABA
  • parvalbumin
  • striatum

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The Journal of Neuroscience: 42 (43)
Journal of Neuroscience
Vol. 42, Issue 43
26 Oct 2022
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The Tail of the Mouse Striatum Contains a Novel Large Type of GABAergic Neuron Incorporated in a Unique Disinhibitory Pathway That Relays Auditory Signals to Subcortical Nuclei
Shigeru Ogata, Yuta Miyamoto, Naoki Shigematsu, Shigeyuki Esumi, Takaichi Fukuda
Journal of Neuroscience 26 October 2022, 42 (43) 8078-8094; DOI: 10.1523/JNEUROSCI.2236-21.2022

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The Tail of the Mouse Striatum Contains a Novel Large Type of GABAergic Neuron Incorporated in a Unique Disinhibitory Pathway That Relays Auditory Signals to Subcortical Nuclei
Shigeru Ogata, Yuta Miyamoto, Naoki Shigematsu, Shigeyuki Esumi, Takaichi Fukuda
Journal of Neuroscience 26 October 2022, 42 (43) 8078-8094; DOI: 10.1523/JNEUROSCI.2236-21.2022
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Keywords

  • auditory
  • basal ganglia
  • enkephalin
  • GABA
  • parvalbumin
  • striatum

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