Seasonal plasticity of song behavior relies on motor and syntactic variability induced by a basal ganglia-forebrain circuit.
Neuroscience. 2017-09-01; 359: 49-68
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Alliende J(1), Giret N(2), Pidoux L(1), Del Negro C(2), Leblois A(3).
(1)Center for Neurophysics, Physiology and Pathologies (UMR CNRS 8119), Institute for Neuroscience and Cognition, Paris Descartes University, 45 rue des Saints Pères, 75006 Paris, France.
(2)Paris-Saclay Institute of Neuroscience, UMR CNRS 9197, Paris Sud University, 91405 Orsay, France.
(3)Center for Neurophysics, Physiology and Pathologies (UMR CNRS 8119), Institute for Neuroscience and Cognition, Paris Descartes University, 45 rue des Saints Pères, 75006 Paris, France.
The plasticity of nervous systems allows animals to quickly adapt to a changing
environment. In particular, seasonal plasticity of brain structure and behavior
is often critical to survival or mating in seasonal climates. Songbirds provide
striking examples of seasonal changes in neural circuits and vocal behavior and
have emerged as a leading model for adult brain plasticity. While seasonal
plasticity and the well-characterized process of juvenile song learning may share
common neural mechanisms, the extent of their similarity remains unclear.
Especially, it is unknown whether the basal ganglia (BG)-forebrain loop which
implements song learning in juveniles by driving vocal exploration participates
in seasonal plasticity. To address this issue, we performed bilateral lesions of
the output structure of the song-related BG-forebrain circuit (the magnocellular
nucleus of the anterior nidopallium) in canaries during the breeding season, when
song is most stereotyped, and just after resuming singing in early fall, when
canaries sing their most variable songs and may produce new syllable types.
Lesions drastically reduced song acoustic variability, increased song and phrase
duration, and decreased syntax variability in early fall, reverting at least
partially seasonal changes observed between the breeding season and early fall.
On the contrary, lesions did not affect singing behavior during the breeding
season. Our results therefore indicate that the BG-forebrain pathway introduces
acoustic and syntactic variability in song when canaries resume singing in early
fall. We propose that BG-forebrain circuits actively participate in seasonal
plasticity by injecting variability in behavior during non-breeding
season.SIGNIFICANCE STATEMENT: The study of seasonal plasticity in temperate
songbirds has provided important insights into the mechanisms of structural and
functional plasticity in the central nervous system. The precise function and
mechanisms of seasonal song plasticity however remain poorly understood. We show
here that a basal ganglia-forebrain circuit involved in the acquisition and
maintenance of birdsong is actively inducing song variability outside the
breeding season, when singing is most variable, while having little effect on the
stereotyped singing during the breeding season. Our results suggest that seasonal
plasticity reflects an active song-maintenance process akin to juvenile learning,
and that basal ganglia-forebrain circuits can drive plasticity in a learned vocal
behavior during the non-injury-induced degeneration and reconstruction of the
neural circuit underlying its production.