Disinhibition of the nucleus accumbens leads to macro-scale hyperactivity consisting of micro-scale behavioral segments encoded by striatal activity

Dorin Yael, Orel Tahary, Boris Gurovich, Katya Belelovsky, Izhar Bar-Gad

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

The striatum comprises of multiple functional territories involved with multilevel control of behavior. Disinhibition of different functional territories leads to territory-specific hyperkinetic and hyperbehavioral symptoms. The ventromedial striatum, including the nucleus accumbens (NAc) core, is typically associated with limbic input but was historically linked to high-level motor control. In this study, performed in female Long–Evans rats, we show that the NAc core directly controls motor behavior on multiple timescales. On the macro-scale, following NAc disinhibition, the animals manifested prolonged hyperactivity, expressed as excessive normal behavior, whereas on the micro-scale multiple behavior transitions occurred, generating short movement segments. The underlying striatal network displayed population-based local field potential transient deflections (LFP spikes) whose rate determined the magnitude of the hyperactivity and whose timing corresponded to unitary behavioral transition events. Individual striatal neurons preserved normal baseline activity and network interactions following the disinhibition, maintaining the normal encoding of behavioral primitives and forming a sparse link between the LFP spikes and single neuron activity. Disinhibition of this classically limbic territory leads to profound motor changes resembling hyperactivity and attention deficit. These behavioral and neuronal results highlight the direct interplay on multiple timescales between different striatal territories during normal and pathological conditions.

Original languageEnglish
Pages (from-to)5897-5909
Number of pages13
JournalJournal of Neuroscience
Volume39
Issue number30
DOIs
StatePublished - 24 Jul 2019

Bibliographical note

Publisher Copyright:
© 2019 by the authors. All rights reserved.

Funding

Received Dec. 13, 2018; revised May 14, 2019; accepted May 16, 2019. Author contributions: D.Y. and I.B.-G. designed research; D.Y. and I.B.-G. performed research; D.Y., O.T., B.G., K.B., and I.B.-G. contributed unpublished reagents/analytic tools; D.Y. and I.B.-G. analyzed data; D.Y. and I.B.-G. wrote the paper. This study was supported in part by an Israel Science Foundation Grant (297/18) and a BSF-NSF Collaborative Research in Computational Neuroscience Grant (2016744). The authors declare no competing financial interests. Correspondence should be addressed to Izhar Bar-Gad at [email protected]. https://doi.org/10.1523/JNEUROSCI.3120-18.2019 Copyright © 2019 the authors

FundersFunder number
BSF-NSF2016744
Israel Science Foundation297/18

    Keywords

    • ADHD
    • Attention deficit hyperactivity disorder
    • GABA
    • Locomotion
    • Nucleus accumbens
    • Ventral striatum

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