Elsevier

Neuroscience

Volume 359, 17 September 2017, Pages 49-68
Neuroscience

Seasonal plasticity of song behavior relies on motor and syntactic variability induced by a basal ganglia–forebrain circuit

https://doi.org/10.1016/j.neuroscience.2017.07.007Get rights and content

Highlights

  • Lesion of LMAN, output nucleus of the song-related BG–forebrain loop, reverses seasonal changes in canary song.

  • Song and phrase duration, acoustic variability and the entropy of transitions increase between the breeding season and fall.

  • These song parameters are reduced by LMAN lesion performed in early fall.

  • In contrast, canary song in breeding season is not affected by LMAN lesion.

Abstract

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.

Introduction

Nervous systems display a strong plasticity of structure and function that allows animals to rapidly adapt to changes in their environment. In particular, seasonal plasticity of neural circuits and behavior is often critical to survival or mating in seasonal climates (Jacobs, 1996). Temperate songbirds breed seasonally and display a pronounced seasonal plasticity in their singing behavior (Ball and Balthazart, 2010, Brenowitz and Larson, 2015). The song initially learned as a juvenile undergoes a pattern of yearly changes: birds produce highly stereotyped songs in the breeding season, then stop singing during the summer molt, resume singing in fall with short-duration songs of variable structure at lower rate and volume and gradually sing longer, louder and more stereotyped songs until the next breeding season (Nottebohm, 1981, Nottebohm et al., 1986, Nottebohm et al., 1987, Guttinger, 1985, Brenowitz, 1997, Voigt and Leitner, 2008). These changes in song are accompanied by large structural reorganization of neural circuits in the brain song-control regions (Nottebohm et al., 1986, Kirn et al., 1989), auditory areas (De Groof et al., 2009, Caras et al., 2012) and beyond (De Groof et al., 2008). The volume of many song-related brain regions, as well as their number of neurons and synapses, increases dramatically in anticipation of the breeding season (Nottebohm, 1981, Brenowitz, 2004), while the physiological and functional properties of their neurons are altered (Del Negro and Edeline, 2002, Del Negro et al., 2005, Meitzen et al., 2007, Meitzen et al., 2009). Songbirds have therefore emerged as a leading model for naturally occurring structural and functional plasticity in the adult central nervous system.

Seasonal changes in vocal behavior, brain structure and neuronal properties are triggered at least in part by vernal increases in circulating sex steroids (Nottebohm et al., 1987, Nowicki and Ball, 1989, Fusani and Gahr, 2006, Alward et al., 2013). Interestingly, the same endocrine signals regulate juvenile song learning in seasonal as well as non-seasonal songbird species (Marler et al., 1988, Korsia and Bottjer, 1991, Whaling et al., 1995, Alliende et al., 2010). For instance, testosterone can increase song stereotypy both in seasonal plasticity (Smith et al., 1997, Tramontin et al., 2000) and juvenile learning (Heid et al., 1985, Marler et al., 1988, Gardner et al., 2005, Sizemore and Perkel, 2011). Seasonal plasticity may therefore exploit similar mechanisms as those acting during early ontogeny in juvenile learning, an idea that dates back to Ramon y Cajál (1959). However, whether seasonal song plasticity relies on the neural circuits which implement juvenile learning remains unknown.

Basal ganglia (BG) circuits promote the acquisition and maintenance of fine motor skill in vertebrates (Hikosaka et al., 2002, Grillner et al., 2005). In particular, songbirds have a specialized BG–forebrain circuit required for juvenile song learning (Fig.1A; Bottjer et al., 1984, Scharff and Nottebohm, 1991) which generates song variability underlying vocal experimentation (Olveczky et al., 2005, Kao et al., 2005, Aronov et al., 2008). This circuit undergoes important seasonal morphological changes in seasonal songbirds (Brenowitz et al., 1998, De Groof et al., 2008), and is a target of sex-steroids (Arnold et al., 1976, Brenowitz and Arnold, 1985, Livingston and Mooney, 2001). Whether the BG–forebrain circuit is actively involved in seasonal song remodeling, possibly injecting variability in song as in the juvenile learning process, remains however unknown. Alternatively, transient song degradation outside breeding season may rather express alteration of the motor pathway which experiences large morphological and physiological changes with seasons (Smith et al., 1997, Del Negro and Edeline, 2002, Del Negro et al., 2005, Thompson et al., 2007, Meitzen et al., 2007, Meitzen et al., 2009), and is an important target of brain sex steroids (Ball and Balthazart, 2010, Brenowitz, 2015).

Here, we sought to determine whether seasonal song plasticity relies on the song-related BG–forebrain circuit. We compared the temporal, acoustic and sequencing properties of canary song between 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 add new syllables to their repertoire. We then assessed how lesions of the output of the song-related BG–forebrain circuit, the magnocellular nucleus of the anterior nidopallium (LMAN), interfere with seasonal changes. While having no effect on song during the breeding season, LMAN 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.

Section snippets

Animals

Fourteen adult domesticated male canaries (Serinus canaria), 1–3 years of age, were used for this experiment. All canaries were reared in the laboratory and belonged to an outbreed form of the common canary with a heterogeneous genetic background. Birds had constant access to seeds (mainly canary grass, Phalaris canariensis, and rape, Brassica rapa), crushed oyster shell and water. Seeds supplemented with fresh food and water were provided daily. The birds were housed on a natural photoperiod

Song structure and repertoire

The canary has a fairly complex song structure (Güttinger, 1979, Del Negro et al., 2005, Markowitz et al., 2013). Canary song consists of a series of phrases, where each phrase is composed of the repetition of a syllable generally formed of 1 or 2 notes (Fig.2A). A male canary has a repertoire of around 20–30 distinct phrases (range 12–40 in the breeding season). Only a part of the repertoire (on average, 8–10 phrases) is present in each song, and phrases may be recombined in different ways.

Discussion

We report here that the output nucleus LMAN of the song-related BG–forebrain circuit is essential for the expression of seasonal changes undergone by canary song in early fall, namely its increased variability and decreased duration compared to the breeding season song. Indeed, LMAN lesions performed in early fall induced a season-specific decrease in song acoustic and syntactic variability and an increase in song and phrase duration, reverting to a great extent observed seasonal changes. Our

Acknowledgments

We are grateful to William E Wood for valuable discussions, to Pascale Le Blanc for technical assistance, and to John Meitzen for his comment on the manuscripts. This work was supported by the Agence National pour la Recherche (ANR, program “Retour Post-Doc”, Grant number ANR-10-PDOC-0016) and by the city of Paris (program “Emergence”, Grant number DDEEES 2014-166).

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