Elsevier

Hormones and Behavior

Volume 60, Issue 5, November 2011, Pages 529-539
Hormones and Behavior

Individual differences in the motivation to communicate relate to levels of midbrain and striatal catecholamine markers in male European starlings

https://doi.org/10.1016/j.yhbeh.2011.08.001Get rights and content

Abstract

Individuals display dramatic differences in social communication even within similar social contexts. Across vertebrates dopaminergic projections from the ventral tegmental area (VTA) and midbrain central gray (GCt) strongly influence motivated, reward-directed behaviors. Norepinephrine is also rich in these areas and may alter dopamine neuronal activity. The present study was designed to provide insight into the roles of dopamine and norepinephrine in VTA and GCt and their efferent striatal target, song control region area X, in the regulation of individual differences in the motivation to sing. We used high pressure liquid chromatography with electrochemical detection to measure dopamine, norepinephrine and their metabolites in micropunched samples from VTA, GCt, and area X in male European starlings (Sturnus vulgaris). We categorized males as sexually motivated or non-sexually motivated based on individual differences in song produced in response to a female. Dopamine markers and norepinephrine in VTA and dopamine in area X correlated positively with sexually-motivated song. Norepinephrine in area X correlated negatively with non-sexually-motivated song. Dopamine in GCt correlated negatively with sexually-motivated song, and the metabolite DOPAC correlated positively with non-sexually-motivated song. Results highlight a role for evolutionarily conserved dopaminergic projections from VTA to striatum in the motivation to communicate and highlight novel patterns of catecholamine activity in area X, VTA, and GCt associated with individual differences in sexually-motivated and non-sexually-motivated communication. Correlations between dopamine and norepinephrine markers also suggest that norepinephrine may contribute to individual differences in communication by modifying dopamine neuronal activity in VTA and GCt.

Highlights

► Individual male starlings increased (sexually motivated) or decreased (non-sexually motivated) song in response to a female. ► Dopamine markers and norepinephrine in VTA and dopamine in area X correlated positively with sexually-motivated song. ► Norepinephrine in area X correlated negatively with non-sexually-motivated song. ► Dopamine markers in GCt correlated negatively with sexually-motivated song and positively with non-sexually-motivated song. ► Individual differences in catecholamine activity in VTA, GCt, and area X may underlie individual differences in song.

Introduction

Vocal communication is central to successful social interactions, yet dramatic differences can be observed across individuals in the motivation to communicate even within similar social contexts. In male songbirds, song production plays a crucial role in mate attraction (Catchpole and Slater, 2008). Males with elevated concentrations of the steroid hormone testosterone respond to the introduction of a female conspecific with a dramatic increase in singing behavior; whereas males with low testosterone do not (Pinxten et al., 2002, Riters et al., 2000). Interestingly however even in males with similarly elevated concentrations of testosterone a subset of males fails to respond to females with an increase in singing and courtship behavior (e.g., (Goodson et al., 2009, Riters et al., 2000)). This suggests that interactions between steroid hormones and other neurochemical systems are likely critical for the production of male courtship song. Although aspects of vocal production in songbirds such as song learning, production, and sensorimotor processing have been relatively well studied (for recent reviews see (Ball et al., 2008, Brainard, 2008, Brenowitz, 2008, Gentner, 2008, Nordeen and Nordeen, 2008, Theunissen et al., 2008, Wild, 2008)), little is known about the neural basis of individual differences in the motivation to sing during conspecific interactions.

Across vertebrates, dopaminergic projections from the midbrain to striatal brain regions strongly influence multiple anticipatory, motivated, reward-directed behaviors (reviewed in (Berridge, 2007, Fibiger et al., 1992, Panksepp and Moskal, 2008, Schultz, 2010, Wise, 2005)), including sexually-motivated behaviors (e.g., (Hull et al., 1990, Pfaus et al., 1995)). In male songbirds, peripheral injections of an indirect dopamine receptor agonist (GBR-12909) stimulate, whereas antagonists (a D1/D2 antagonist cis-flupenthixol and a D1 antagonist SCH-23390) inhibit sexually-motivated, female-directed singing behavior (Rauceo et al., 2008, Schroeder and Riters, 2006). Tract-tracing studies identify the midbrain ventral tegmental area (VTA) and mesencephalic central gray (GCt) as primary sources of catecholaminergic inputs to song control regions, including area X of the avian striatum (Fig. 1) (Appeltants et al., 2000, Appeltants et al., 2002, Bottjer et al., 1989, Castelino et al., 2007, Lewis et al., 1981). In male European starlings immunolabeling for tyrosine hydroxylase (TH; the rate limiting enzyme for catecholamine synthesis) and autoradiography for dopamine receptors suggest that dopamine in VTA and GCt is more tightly coupled to sexually-motivated song compared to song produced in non-breeding condition males (Heimovics et al., 2009, Heimovics and Riters, 2008). The combined results of several additional studies in starlings and zebra finches using immunolabeling for immediate early genes (IEGs), IEG/TH double labeling, and electrophysiological recording also highlight roles for dopamine neurons in both VTA and GCt in the regulation of sexually-motivated male song production (Bharati and Goodson, 2006, Goodson et al., 2009, Hara et al., 2007, Heimovics and Riters, 2005, Yanagihara and Hessler, 2006).

Of the song control regions to which VTA and GCt project (Fig. 1), area X shows among the most consistent and extreme differences in song-associated activity or gene expression across social contexts (e.g., (Hessler and Doupe, 1999, Jarvis et al., 1998, Riters et al., 2004, Teramitsu et al., 2010)). Area X is a component of the songbird basal ganglia circuit that underlies song learning and context-appropriate song variability in adults (Doupe et al., 2005, Leblois et al., 2010, Scharff and Nottebohm, 1991). Dopamine receptor stimulation influences neuronal activity in area X (Ding et al., 2003, Ding and Perkel, 2002); and dopamine levels in area X measured using microdialysis are higher during female-directed than undirected singing (Sasaki et al., 2006). Differential patterns of D1 and D2 receptor dopamine subtype colocalization with the IEG egr1 (referred to in birds by the acronym ZENK (Mello et al., 1992)) are also observed during directed and undirected singing in male zebra finches (Kubikova et al., 2010). Furthermore, pharmacological blockade of dopamine D1 receptors in area X disrupts context-dependent changes in song variability in male zebra finches singing female-directed compared to undirected song (Leblois et al., 2010).

Although VTA and GCt are sources of dopaminergic projections to area X (Fig. 1), both of these regions are also rich in noradrenergic alpha-2 receptors and the norepinephrine synthesizing enzyme dopamine beta hydroxylase (DBH; (Heimovics et al., 2011, Heimovics and Riters, 2008, Mello et al., 1998, Waterman and Harding, 2008)). DBH immunolabeled fibers in both GCt and VTA are found in close apposition to area X projecting neurons (Castelino et al., 2007). Past data demonstrate that norepinephrine depletion using the noradrenergic specific neurotoxin DSP-4 disrupts female-directed song production and reduces norepinephrine levels in area X (Barclay et al., 1996). DSP-4 also abolishes context-dependent differences observed in IEG activation in area X associated with female-directed compared to undirected song (Castelino and Ball, 2005). These findings suggest that norepinephrine may modulate individual differences in sexually-motivated singing behavior by acting directly in area X or indirectly by acting in part on dopamine neurons within VTA and GCt.

In the present study we used high pressure liquid chromatography to examine levels of dopamine, norepinephrine, and their metabolites in micropunched samples from area X, VTA, and GCt in male European starlings (Sturnus vulgaris) singing in the presence of a female. Courtship in male starlings typically involves a male flying (often away from a female) to a nesting territory from which he produces high rates of song (rates above those observed when a female is not present (Eens, 1997, Riters et al., 2000)). Within a group of breeding condition male starlings however, some males respond to a female with a reduction in song production (e.g., (Heimovics et al., 2009, Heimovics and Riters, 2007, Riters et al., 2000)). Given that song in response to a female functions to attract mates (Eens et al., 1990, Eens et al., 1993), our assumption is that males that elevate song production in response to a female are sexually motivated. In contrast, we assume that males that reduce song in response to a female are less or non-sexually motivated (or perhaps sexually inhibited by competing males). The goal of the present study was to use these naturally occurring individual differences in the motivation to sing in male starlings to provide further insight into the role of catecholamines in the motivation to communicate.

Section snippets

Material and methods

All protocols were approved by the University of Wisconsin Institutional Animal Care and Use Committee and adhered to methods approved by the National Institutes of Health Guide for the Care and Use of Laboratory Animals.

Sexually-motivated and non-sexually-motivated males

Fourteen males produced greater than 50% of their total song when a female was present compared to when no female was present and were assigned to the sexually-motivated group. Ten males produced greater than 50% of total song when a female was absent compared to when a female was present and were assigned to the non-sexually-motivated group. A repeated measures ANOVA revealed a significant interaction (F1,22 = 33.49, p = 0.000008; Figs. 3A and B) but no significant main effects for singing

Discussion

Little is known about the neural regulation of the motivation to communicate in any vertebrate species. In male songbirds the steroid hormone testosterone clearly plays a role in sexually-motivated-song production (Ball et al., 2004, Pinxten et al., 2002, Riters et al., 2000), yet as observed in the present and past studies (e.g., (Heimovics et al., 2009, Heimovics and Riters, 2007, Riters et al., 2000)) even with similarly high testosterone concentrations some males do not sing in response to

Conclusions

The results of this study indicate that naturally occurring individual variation in the motivation to sing in response to a female is reflected in catecholamine activity in projections from midbrain dopaminergic brain regions to the striatum. Midbrain dopamine systems are central for the production of multiple incentively-motivated, reward-directed behaviors. The present results suggest that the evolutionarily conserved role for dopamine projections from VTA to the striatum in motivated

Acknowledgments

The data presented in this paper are based upon work supported by grants from NIH to LVR (R01 MH080225) and KWS (R01 NS055125) and a graduate research fellowship from NSF to SAH. We gratefully acknowledge Kate Skogen, Jeff Alexander, Chris Elliot, and John Irwin for help with starling capture and animal care and Bill Feeny for assistance with illustrations. We thank Dr. Richard B. Mailman and Stan B. Southerland for providing and helping with the HPLC system in Chapel Hill.

References (71)

  • J. Grenhoff et al.

    Prazosin modulates the firing pattern of dopamine neurons in rat ventral tegmental area

    Eur. J. Pharmacol.

    (1993)
  • S.A. Heimovics et al.

    ZENK labeling within social behavior brain regions reveals breeding context-dependent patterns of neural activity associated with song in male European starlings (Sturnus vulgaris)

    Behav. Brain Res.

    (2007)
  • S.A. Heimovics et al.

    Evidence that dopamine within motivation and song control brain regions regulates birdsong context-dependently

    Physiol. Behav.

    (2008)
  • S.A. Heimovics et al.

    D1-like dopamine receptor density in nuclei involved in social behavior correlates with song in a context-dependent fashion in male European starlings

    Neuroscience

    (2009)
  • E.M. Hull et al.

    Dopamine receptors in the ventral tegmental area modulate male sexual behavior in rats

    Brain Res.

    (1990)
  • E.D. Jarvis et al.

    For whom the bird sings: context-dependent gene expression

    Neuron

    (1998)
  • C.D. Kilts et al.

    Simultaneous quantification of dopamine, 5-hydroxytryptamine and four metabolically related compounds by means of reversed-phase high-performance liquid chromatography with electrochemical detection

    J. Chromatogr.

    (1981)
  • K.S. Lynch et al.

    Catecholaminergic cell groups and vocal communication in male songbirds

    Physiol. Behav.

    (2008)
  • J.G. Pfaus et al.

    Sexual activity increases dopamine transmission in the nucleus accumbens and striatum of female rats

    Brain Res.

    (1995)
  • R. Pinxten et al.

    Context-dependent effects of castration and testosterone treatment on song in male European starlings

    Horm. Behav.

    (2002)
  • S. Rauceo et al.

    Dopaminergic modulation of reproductive behavior and activity in male zebra finches

    Behav. Brain Res.

    (2008)
  • L.V. Riters et al.

    Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris)

    Horm. Behav.

    (2000)
  • L.V. Riters et al.

    Vocal production in different social contexts relates to variation in immediate early gene immunoreactivity within and outside of the song control system

    Behav. Brain Res.

    (2004)
  • M.B. Schroeder et al.

    Pharmacological manipulations of dopamine and opioids have differential effects on sexually motivated song production in male European starlings

    Physiol. Behav.

    (2006)
  • S.A. Waterman et al.

    Neurotoxic effects of DSP-4 on the central noradrenergic system in male zebra finches

    Behav. Brain Res.

    (2008)
  • D. Appeltants et al.

    The origin of catecholaminergic inputs to the song control nucleus RA in canaries

    Neuroreport

    (2002)
  • G.F. Ball et al.

    Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior

    Ann. N. Y. Acad. Sci.

    (2004)
  • G.F. Ball et al.

    Sex differences in brain and behavior and the neuroendocrine control of the motivation to sing

  • K.C. Berridge

    The debate over dopamine's role in reward: the case for incentive salience

    Psychopharmacol. (Berl.)

    (2007)
  • S.W. Bottjer et al.

    Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches

    J. Comp. Neurol.

    (1989)
  • M.S. Brainard

    The anterior forebrain pathway and vocal plasticity

  • E.A. Brenowitz

    Plasticity of the song control system in adult birds

  • C.B. Castelino et al.

    A role for norepinephrine in the regulation of context-dependent ZENK expression in male zebra finches (Taeniopygia guttata)

    Eur. J. Neurosci.

    (2005)
  • C.B. Castelino et al.

    Noradrenergic projections to the song control nucleus area X of the medial striatum in male zebra finches (Taeniopygia guttata)

    J. Comp. Neurol.

    (2007)
  • C.K. Catchpole et al.

    Bird Song: Biological Themes and Variations

    (2008)
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    1

    Present addresses: Dept of Psychology, University of British Columbia, Vancouver, BC, Canada.

    2

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