Differential roles of nonsynaptic and synaptic plasticity in operant reward learning-induced compulsive behavior.
Current Biology. 2014-05-01; 24(9): 941-950
DOI: 10.1016/j.cub.2014.03.004
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1. Curr Biol. 2014 May 5;24(9):941-50. doi: 10.1016/j.cub.2014.03.004. Epub 2014 Apr
3.
Differential roles of nonsynaptic and synaptic plasticity in operant reward
learning-induced compulsive behavior.
Sieling F(1), Bédécarrats A(2), Simmers J(2), Prinz AA(3), Nargeot R(4).
Author information:
(1)Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA),
Université de Bordeaux, UMR 5287, 33000 Bordeaux, France; CNRS, INCIA, UMR 5287,
33000 Bordeaux, France; Wallace H. Coulter Department of Biomedical Engineering,
Georgia Institute of Technology and Emory University, Atlanta, GA 30332, USA.
(2)Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA),
Université de Bordeaux, UMR 5287, 33000 Bordeaux, France; CNRS, INCIA, UMR 5287,
33000 Bordeaux, France.
(3)Department of Biology, Emory University, Atlanta, GA 30322, USA.
(4)Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA),
Université de Bordeaux, UMR 5287, 33000 Bordeaux, France; CNRS, INCIA, UMR 5287,
33000 Bordeaux, France. Electronic address: .
BACKGROUND: Rewarding stimuli in associative learning can transform the
irregularly and infrequently generated motor patterns underlying motivated
behaviors into output for accelerated and stereotyped repetitive action. This
transition to compulsive behavioral expression is associated with modified
synaptic and membrane properties of central neurons, but establishing the causal
relationships between cellular plasticity and motor adaptation has remained a
challenge.
RESULTS: We found previously that changes in the intrinsic excitability and
electrical synapses of identified neurons in Aplysia’s central pattern-generating
network for feeding are correlated with a switch to compulsive-like motor output
expression induced by in vivo operant conditioning. Here, we used specific
computer-simulated ionic currents in vitro to selectively replicate or suppress
the membrane and synaptic plasticity resulting from this learning. In naive in
vitro preparations, such experimental manipulation of neuronal membrane
properties alone increased the frequency but not the regularity of feeding motor
output found in preparations from operantly trained animals. On the other hand,
changes in synaptic strength alone switched the regularity but not the frequency
of feeding output from naive to trained states. However, simultaneously imposed
changes in both membrane and synaptic properties reproduced both major aspects of
the motor plasticity. Conversely, in preparations from trained animals,
experimental suppression of the membrane and synaptic plasticity abolished the
increase in frequency and regularity of the learned motor output expression.
CONCLUSIONS: These data establish direct causality for the contributions of
distinct synaptic and nonsynaptic adaptive processes to complementary facets of a
compulsive behavior resulting from operant reward learning.
Copyright © 2014 Elsevier Ltd. All rights reserved.
DOI: 10.1016/j.cub.2014.03.004
PMID: 24704077 [Indexed for MEDLINE]