Homogeneity of intrinsic properties of sexually dimorphic vocal motoneurons in male and female zebra finches

Department of Neurobiology, Duke University Medical Center, Durham North Carolina 27710, USA.
The Journal of Comparative Neurology (Impact Factor: 3.51). 05/2007; 502(1):157-69. DOI: 10.1002/cne.21310
Source: PubMed

ABSTRACT Sex differences in behavioral repertoires are often reflected in the underlying electrophysiological and morphological properties of motor neurons. Male zebra finches produce long, spectrally complex, learned songs and short calls, whereas female finches only produce short, innate, and spectrally simple calls. In both sexes, vocalizations are produced by using syringeal muscles controlled by motoneurons within the tracheosyringeal part of the hypoglossal motor nucleus (XIIts). We asked whether the sexually dimorphic vocal repertoire of adult zebra finches is paralleled by structural and functional differences in syringeal motoneurons. By using immunohistochemical and intracellular staining methods, we describe sex differences in the morphology of XIIts and its surrounding neuropil (suprahypoglossal region; SH). Although the overall number of XIIts neurons and the proportions of somata/neuropil were not sexually dimorphic, the volumes of both XIIts and SH were larger in males, in part because male XIIts neurons had larger somata. In contrast, female XIIts motoneurons had a more complex dendritic structure than did male neurons, suggesting that the larger volume of the male XIIts is due in part to increased numbers of afferents. Intracellular recordings in brain slices revealed that the intrinsic electrophysiological properties of female XIIts neurons were similar to published values for male XIIts motoneurons. We also show that female neurons received glycinergic inputs from the brainstem respiratory premotor column, similar to those described in males. These findings indicate that male and female zebra finches produce their disparate vocal repertoires using physiologically similar motoneurons. Thus, sites upstream of the motoneuron pool may be the major determinants of sexually dimorphic vocal behaviors in this species.

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    • "The anti-parvalbumin antibody (Table 1) was characterized in Celio et al. (1988). It has since been used to detect the zebra finch isoform in immunohistochemistry to identify parvalbumin-positive neurons in song control nuclei (Wild et al., 2001, 2005, 2009; Roberts et al., 2007), as it is used in this study. "
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    ABSTRACT: Variants of the contactin associated protein-like 2 (Cntnap2) gene are risk factors for language-related disorders including autism spectrum disorder, specific language impairment, and stuttering. Songbirds are useful models for study of human speech disorders due to their shared capacity for vocal learning, which relies on similar cortico-basal ganglia circuitry and genetic factors. Here, we investigate Cntnap2 protein expression in the brain of the zebra finch, a songbird species in which males, but not females, learn their courtship songs. We hypothesize that Cntnap2 has overlapping functions in vocal learning species, and expect to find protein expression in song-related areas of the zebra finch brain. We further expect that the distribution of this membrane-bound protein may not completely mirror its mRNA distribution due to the distinct subcellular localization of the two molecular species. We find that Cntnap2 protein is enriched in several song control regions relative to surrounding tissues, particularly within the adult male, but not female, robust nucleus of the arcopallium (RA), a cortical song control region analogous to human layer 5 primary motor cortex. The onset of this sexually dimorphic expression coincides with the onset of sensorimotor learning in developing males. Enrichment in male RA appears due to expression in projection neurons within the nucleus, as well as to additional expression in nerve terminals of cortical projections to RA from the lateral magnocellular nucleus of the nidopallium. Cntnap2 protein expression in zebra finch brain supports the hypothesis that this molecule affects neural connectivity critical for vocal learning across taxonomic classes. J. Comp. Neurol., 2013. © 2013 Wiley Periodicals, Inc.
    The Journal of Comparative Neurology 01/2014; 522(1). DOI:10.1002/cne.23394 · 3.51 Impact Factor
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    • "Interestingly, the 3000 possible independent output channels in Area X is similar to the number of primary motor neurons (Roberts et al., 2007) that topographically innervate only roughly 8 muscles on each side of the vocal organ (Vicario and Nottebohm, 1988). "
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    ABSTRACT: Most of our motor skills are not innately programmed, but are learned by a combination of motor exploration and performance evaluation, suggesting that they proceed through a reinforcement learning (RL) mechanism. Songbirds have emerged as a model system to study how a complex behavioral sequence can be learned through an RL-like strategy. Interestingly, like motor sequence learning in mammals, song learning in birds requires a basal ganglia (BG)-thalamocortical loop, suggesting common neural mechanisms. Here, we outline a specific working hypothesis for how BG-forebrain circuits could utilize an internally computed reinforcement signal to direct song learning. Our model includes a number of general concepts borrowed from the mammalian BG literature, including a dopaminergic reward prediction error and dopamine-mediated plasticity at corticostriatal synapses. We also invoke a number of conceptual advances arising from recent observations in the songbird. Specifically, there is evidence for a specialized cortical circuit that adds trial-to-trial variability to stereotyped cortical motor programs, and a role for the BG in "biasing" this variability to improve behavioral performance. This BG-dependent "premotor bias" may in turn guide plasticity in downstream cortical synapses to consolidate recently learned song changes. Given the similarity between mammalian and songbird BG-thalamocortical circuits, our model for the role of the BG in this process may have broader relevance to mammalian BG function.
    Neuroscience 12/2011; 198:152-70. DOI:10.1016/j.neuroscience.2011.09.069 · 3.33 Impact Factor
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    • "Neurons in different regions, however, may differ in whether an increase in neuron size leads to an increase in the time constant of the membrane (as in this study), or a decrease in input resistance (i.e., male Xenopus laryngeal motoneurons, [Yamaguchi et al., 2003]). In at least one case, however, the steroid sex hormone induced-increase in neuron size did not affect capacitance, input resistance, or the time constant (the sexually dimorphic avian hypoglossal motoneurons studied by Roberts et al., 2007). "
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    ABSTRACT: Steroid sex hormones drive changes in the nervous system and behavior in many animal taxa, but integrating the former with the latter remains challenging. One useful model system for meeting this challenge is seasonally breeding songbirds. In these species, plasma testosterone levels rise and fall across the seasons, altering song behavior and causing dramatic growth and regression of the song-control system, a discrete set of nuclei that control song behavior. Whereas the cellular mechanisms underlying changes in nucleus volume have been studied as a model for neural growth and degeneration, it is unknown whether these changes in neural structure are accompanied by changes in electrophysiological properties other than spontaneous firing rate. Here we test the hypothesis that passive and active neuronal properties in the forebrain song-control nuclei HVC and RA change across breeding conditions. We exposed adult male Gambel's white-crowned sparrows to either short-day photoperiod or long-day photoperiod and systemic testosterone to simulate nonbreeding and breeding conditions, respectively. We made whole-cell recordings from RA and HVC neurons in acute brain slices. We found that RA projection neuron membrane time constant, capacitance, and evoked and spontaneous firing rates were all increased in the breeding condition; the measured electrophysiological properties of HVC interneurons and projection neurons were stable across breeding conditions. This combination of plastic and stable intrinsic properties could directly impact the song-control system's motor control across seasons, underlying changes in song stereotypy. These results provide a valuable framework for integrating how steroid hormones modulate cellular physiology to change behavior.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 06/2009; 29(20):6558-67. DOI:10.1523/JNEUROSCI.5571-08.2009 · 6.75 Impact Factor
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