Literature DB >> 28871960

Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior.

Justin K O'Hare1,2, Haofang Li3, Namsoo Kim3, Erin Gaidis3, Kristen Ade1,2, Jeff Beck1, Henry Yin3, Nicole Calakos1,2.   

Abstract

Habit formation is a behavioral adaptation that automates routine actions. Habitual behavior correlates with broad reconfigurations of dorsolateral striatal (DLS) circuit properties that increase gain and shift pathway timing. The mechanism(s) for these circuit adaptations are unknown and could be responsible for habitual behavior. Here we find that a single class of interneuron, fast-spiking interneurons (FSIs), modulates all of these habit-predictive properties. Consistent with a role in habits, FSIs are more excitable in habitual mice compared to goal-directed and acute chemogenetic inhibition of FSIs in DLS prevents the expression of habitual lever pressing. In vivo recordings further reveal a previously unappreciated selective modulation of SPNs based on their firing patterns; FSIs inhibit most SPNs but paradoxically promote the activity of a subset displaying high fractions of gamma-frequency spiking. These results establish a microcircuit mechanism for habits and provide a new example of how interneurons mediate experience-dependent behavior.

Entities:  

Keywords:  fast-spiking interneuron; habit; mouse; neuroscience; striatum

Mesh:

Substances:

Year:  2017        PMID: 28871960      PMCID: PMC5584985          DOI: 10.7554/eLife.26231

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  61 in total

1.  Regulation of neuronal input transformations by tunable dendritic inhibition.

Authors:  Matthew Lovett-Barron; Gergely F Turi; Patrick Kaifosh; Peter H Lee; Frédéric Bolze; Xiao-Hua Sun; Jean-François Nicoud; Boris V Zemelman; Scott M Sternson; Attila Losonczy
Journal:  Nat Neurosci       Date:  2012-01-15       Impact factor: 24.884

2.  The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat.

Authors:  C R Gerfen
Journal:  J Comp Neurol       Date:  1985-06-22       Impact factor: 3.215

3.  Reversible online control of habitual behavior by optogenetic perturbation of medial prefrontal cortex.

Authors:  Kyle S Smith; Arti Virkud; Karl Deisseroth; Ann M Graybiel
Journal:  Proc Natl Acad Sci U S A       Date:  2012-10-29       Impact factor: 11.205

4.  Distinct roles of GABAergic interneurons in the regulation of striatal output pathways.

Authors:  Aryn H Gittis; Alexandra B Nelson; Myo T Thwin; Jorge J Palop; Anatol C Kreitzer
Journal:  J Neurosci       Date:  2010-02-10       Impact factor: 6.167

5.  Cannabinoid receptor 1-expressing neurons in the nucleus accumbens.

Authors:  Bradley D Winters; Juliane M Krüger; Xiaojie Huang; Zachary R Gallaher; Masago Ishikawa; Krzysztof Czaja; James M Krueger; Yanhua H Huang; Oliver M Schlüter; Yan Dong
Journal:  Proc Natl Acad Sci U S A       Date:  2012-09-10       Impact factor: 11.205

6.  Shift from goal-directed to habitual cocaine seeking after prolonged experience in rats.

Authors:  Agustin Zapata; Vicki L Minney; Toni S Shippenberg
Journal:  J Neurosci       Date:  2010-11-17       Impact factor: 6.167

7.  Changes in activity of the striatum during formation of a motor habit.

Authors:  Chengke Tang; Anthony P Pawlak; Volodymyr Prokopenko; Mark O West
Journal:  Eur J Neurosci       Date:  2007-02       Impact factor: 3.386

8.  Representation of the body by single neurons in the dorsolateral striatum of the awake, unrestrained rat.

Authors:  R M Carelli; M O West
Journal:  J Comp Neurol       Date:  1991-07-08       Impact factor: 3.215

9.  SK channel modulation rescues striatal plasticity and control over habit in cannabinoid tolerance.

Authors:  Cristiano Nazzaro; Barbara Greco; Milica Cerovic; Paul Baxter; Tiziana Rubino; Massimo Trusel; Daniela Parolaro; Tatiana Tkatch; Fabio Benfenati; Paola Pedarzani; Raffaella Tonini
Journal:  Nat Neurosci       Date:  2012-01-08       Impact factor: 24.884

10.  An Improved BAC Transgenic Fluorescent Reporter Line for Sensitive and Specific Identification of Striatonigral Medium Spiny Neurons.

Authors:  Kristen K Ade; Yehong Wan; Meng Chen; Bernd Gloss; Nicole Calakos
Journal:  Front Syst Neurosci       Date:  2011-06-08
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  27 in total

Review 1.  Dopaminergic modulation of striatal function and Parkinson's disease.

Authors:  Shenyu Zhai; Weixing Shen; Steven M Graves; D James Surmeier
Journal:  J Neural Transm (Vienna)       Date:  2019-04-01       Impact factor: 3.575

2.  Active Zone Proteins RIM1αβ Are Required for Normal Corticostriatal Transmission and Action Control.

Authors:  David A Kupferschmidt; Shana M Augustin; Kari A Johnson; David M Lovinger
Journal:  J Neurosci       Date:  2018-12-17       Impact factor: 6.167

3.  Loss of striatal tyrosine-hydroxylase interneurons impairs instrumental goal-directed behavior.

Authors:  Jaime Kaminer; Diego Espinoza; Shaznaan Bhimani; James M Tepper; Tibor Koos; Michael W Shiflett
Journal:  Eur J Neurosci       Date:  2019-05-02       Impact factor: 3.386

4.  Inversely Active Striatal Projection Neurons and Interneurons Selectively Delimit Useful Behavioral Sequences.

Authors:  Nuné Martiros; Alexandra A Burgess; Ann M Graybiel
Journal:  Curr Biol       Date:  2018-02-08       Impact factor: 10.834

Review 5.  Neural substrates of habit.

Authors:  Melissa Malvaez
Journal:  J Neurosci Res       Date:  2019-11-06       Impact factor: 4.164

6.  An Aplysia-like synaptic switch for rapid protection against ethanol-induced synaptic inhibition in a mammalian habit circuit.

Authors:  Mary H Patton; Katherine E Padgett; Paige N McKeon; Shao-Gang Lu; Thomas W Abrams; Brian N Mathur
Journal:  Neuropharmacology       Date:  2018-10-12       Impact factor: 5.250

7.  Opposing Influence of Sensory and Motor Cortical Input on Striatal Circuitry and Choice Behavior.

Authors:  Christian R Lee; Alex J Yonk; Joost Wiskerke; Kenneth G Paradiso; James M Tepper; David J Margolis
Journal:  Curr Biol       Date:  2019-04-11       Impact factor: 10.834

Review 8.  Excitatory extrinsic afferents to striatal interneurons and interactions with striatal microcircuitry.

Authors:  Maxime Assous; James M Tepper
Journal:  Eur J Neurosci       Date:  2018-03-25       Impact factor: 3.386

9.  Recent Insights into Corticostriatal Circuit Mechanisms underlying Habits: Invited review for Current Opinions in Behavioral Sciences.

Authors:  Justin O'Hare; Nicole Calakos; Henry H Yin
Journal:  Curr Opin Behav Sci       Date:  2017-10-27

Review 10.  Aberrant features of in vivo striatal dynamics in Parkinson's disease.

Authors:  Kwang Lee; Sotiris C Masmanidis
Journal:  J Neurosci Res       Date:  2019-09-09       Impact factor: 4.164

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