Striatal dopamine signals are region specific and temporally stable across action-sequence habit formation

Wouter van Elzelingen; Pascal Warnaar; João Matos; Wieneke Bastet; Roos Jonkman; Dyonne Smulders; Jessica Goedhoop; Damiaan Denys; Tara Arbab; Ingo Willuhn

doi:10.1016/j.cub.2021.12.027

Striatal dopamine signals are region specific and temporally stable across action-sequence habit formation

Wouter van Elzelingen, Pascal Warnaar, João Matos, Wieneke Bastet, Roos Jonkman, Dyonne Smulders, Jessica Goedhoop, Damiaan Denys, Tara Arbab, Ingo Willuhn

Netherlands Institute for Neuroscience (NIN)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

29 Citations (Scopus)

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Abstract

Habits are automatic, inflexible behaviors that develop slowly with repeated performance. Striatal dopamine signaling instantiates this habit-formation process, presumably region specifically and via ventral-to-dorsal and medial-to-lateral signal shifts. Here, we quantify dopamine release in regions implicated in these presumed shifts (ventromedial striatum [VMS], dorsomedial striatum [DMS], and dorsolateral striatum [DLS]) in rats performing an action-sequence task and characterize habit development throughout a 10-week training. Surprisingly, all regions exhibited stable dopamine dynamics throughout habit development. VMS and DLS signals did not differ between habitual and non-habitual animals, but DMS dopamine release increased during action-sequence initiation and decreased during action-sequence completion in habitual rats, whereas non-habitual rats showed opposite effects. Consistently, optogenetic stimulation of DMS dopamine release accelerated habit formation. Thus, we demonstrate that dopamine signals do not shift regionally during habit formation and that dopamine in DMS, but not VMS or DLS, determines habit bias, attributing "habit functions" to a region previously associated exclusively with non-habitual behavior.

Original language	English
Pages (from-to)	1163-1174.E6
Journal	Current Biology
Volume	32
DOIs	https://doi.org/10.1016/j.cub.2021.12.027
Publication status	Published - 07 Feb 2022

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Elzelingen2022Final published version, 2.66 MBLicence: CC BY-NC-ND

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title = "Striatal dopamine signals are region specific and temporally stable across action-sequence habit formation",

abstract = "Habits are automatic, inflexible behaviors that develop slowly with repeated performance. Striatal dopamine signaling instantiates this habit-formation process, presumably region specifically and via ventral-to-dorsal and medial-to-lateral signal shifts. Here, we quantify dopamine release in regions implicated in these presumed shifts (ventromedial striatum [VMS], dorsomedial striatum [DMS], and dorsolateral striatum [DLS]) in rats performing an action-sequence task and characterize habit development throughout a 10-week training. Surprisingly, all regions exhibited stable dopamine dynamics throughout habit development. VMS and DLS signals did not differ between habitual and non-habitual animals, but DMS dopamine release increased during action-sequence initiation and decreased during action-sequence completion in habitual rats, whereas non-habitual rats showed opposite effects. Consistently, optogenetic stimulation of DMS dopamine release accelerated habit formation. Thus, we demonstrate that dopamine signals do not shift regionally during habit formation and that dopamine in DMS, but not VMS or DLS, determines habit bias, attributing {"}habit functions{"} to a region previously associated exclusively with non-habitual behavior.",

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T1 - Striatal dopamine signals are region specific and temporally stable across action-sequence habit formation

AU - van Elzelingen, Wouter

AU - Warnaar, Pascal

AU - Matos, João

AU - Bastet, Wieneke

AU - Jonkman, Roos

AU - Smulders, Dyonne

AU - Goedhoop, Jessica

AU - Denys, Damiaan

AU - Arbab, Tara

AU - Willuhn, Ingo

PY - 2022/2/7

Y1 - 2022/2/7

N2 - Habits are automatic, inflexible behaviors that develop slowly with repeated performance. Striatal dopamine signaling instantiates this habit-formation process, presumably region specifically and via ventral-to-dorsal and medial-to-lateral signal shifts. Here, we quantify dopamine release in regions implicated in these presumed shifts (ventromedial striatum [VMS], dorsomedial striatum [DMS], and dorsolateral striatum [DLS]) in rats performing an action-sequence task and characterize habit development throughout a 10-week training. Surprisingly, all regions exhibited stable dopamine dynamics throughout habit development. VMS and DLS signals did not differ between habitual and non-habitual animals, but DMS dopamine release increased during action-sequence initiation and decreased during action-sequence completion in habitual rats, whereas non-habitual rats showed opposite effects. Consistently, optogenetic stimulation of DMS dopamine release accelerated habit formation. Thus, we demonstrate that dopamine signals do not shift regionally during habit formation and that dopamine in DMS, but not VMS or DLS, determines habit bias, attributing "habit functions" to a region previously associated exclusively with non-habitual behavior.

AB - Habits are automatic, inflexible behaviors that develop slowly with repeated performance. Striatal dopamine signaling instantiates this habit-formation process, presumably region specifically and via ventral-to-dorsal and medial-to-lateral signal shifts. Here, we quantify dopamine release in regions implicated in these presumed shifts (ventromedial striatum [VMS], dorsomedial striatum [DMS], and dorsolateral striatum [DLS]) in rats performing an action-sequence task and characterize habit development throughout a 10-week training. Surprisingly, all regions exhibited stable dopamine dynamics throughout habit development. VMS and DLS signals did not differ between habitual and non-habitual animals, but DMS dopamine release increased during action-sequence initiation and decreased during action-sequence completion in habitual rats, whereas non-habitual rats showed opposite effects. Consistently, optogenetic stimulation of DMS dopamine release accelerated habit formation. Thus, we demonstrate that dopamine signals do not shift regionally during habit formation and that dopamine in DMS, but not VMS or DLS, determines habit bias, attributing "habit functions" to a region previously associated exclusively with non-habitual behavior.

U2 - 10.1016/j.cub.2021.12.027

DO - 10.1016/j.cub.2021.12.027

M3 - Article

C2 - 35134325

SN - 0960-9822

VL - 32

SP - 1163-1174.E6

JO - Current Biology

JF - Current Biology

ER -

Striatal dopamine signals are region specific and temporally stable across action-sequence habit formation

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