Region-specific testosterone modulation of the vasotocin-immunoreactive system in male dark-eyed junco, Junco hyemalis

Plumari, L.; Plateroti, S.; Deviche, Pierre; Panzica, Giancarlo

doi:10.1016/j.brainres.2003.10.037

Cited by 24 publications

(15 citation statements)

References 38 publications

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“…The number of VT͞VP neurons in the BSTm is sexually dimorphic (males Ͼ females) and steroid-dependent in most vertebrate species thus far examined (4,5,30), including songbirds (31,32). In contrast, zebra finches have not been consistently found to exhibit sexually dimorphic or testosterone-dependent immunostaining (33,34), and we here found no evidence for sex differences in any of the estrildid species examined, either in their numbers of VT-ir neurons or Fos responses to social stimuli.…”

Section: Discussioncontrasting

confidence: 38%

Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species

Goodson

Wang

2006

Proc. Natl. Acad. Sci. U.S.A.

121

160

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The medial bed nucleus of the stria terminalis (BSTm) influences both social approach and social aversion, suggesting that this structure may play an important role in generating motivational and behavioral differences between gregarious and asocial species. However, no specific neurons have been identified within the BSTm that influence species-typical levels of sociality or that mediate approach and avoidance. Using five songbird species that differ selectively in their species-typical group sizes, we now demonstrate that vasotocin-immunoreactive (VT-ir) neurons of the BSTm exhibit very different immediate early gene responses to same-sex stimuli in gregarious and asocial species. Exposure to a same-sex conspecific increases VT-Fos colocalization in gregarious species while decreasing colocalization in relatively asocial species. We additionally demonstrate that these neurons are selectively activated by social stimuli that normally elicit affiliation (positively valenced social stimuli) but not by stimuli that elicit aversion (negatively valenced social stimuli). Constitutive Fos activity of the VT-ir neurons is also significantly greater in the gregarious species, and the two most social species express significantly more VT-ir neurons. These findings demonstrate that the properties of valence-sensitive neurons evolve in relation to sociality and indicate that gregarious species accentuate positive stimulus properties during social interactions.amygdala ͉ sociality ͉ vasopressin ͉ vasotocin T he medial bed nucleus of the stria terminalis (BSTm) is anatomically and functionally conserved in the land vertebrate classes (1-3), and in virtually all species, a subpopulation of BSTm neurons produce vasotocin (VT) or its mammalian homologue vasopressin (VP) (4, 5) (see Fig. 1). These neurons project to multiple areas of the basal forebrain [e.g., ventral pallidum and lateral septum (5, 6)], where VT͞VP influences a variety of social behaviors, sometimes in a potent and highly species-specific manner (4,7,8). For instance, differential expression of V 1a receptors in the ventral pallidum is both necessary and sufficient to account for species differences in monogamous pair-bonding (9), and V 1a receptors in the lateral septum are both necessary and sufficient for the display of social recognition in mice (10). However, despite the vast literature on VT͞VP functions, receptor distributions, sexual dimorphisms, and steroid sensitivities (4,5,7,8), almost nothing is known about BSTm VT͞VP neuronal activity as it relates to stimulus parameters, social context, and species-specific aspects of social structure. Indeed, to our knowledge, the only relevant data come from monogamous male voles, in which VP mRNA increases in the BSTm after cohabitation with a female (11).The present experiments were therefore conducted to test the hypotheses that (i) VT-immunoreactive (VT-ir) neurons in the BSTm are responsive to stimuli that elicit affiliation, and (ii) responses of these neurons evolve in relation to sociality. These hypoth...

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Section: Discussioncontrasting

confidence: 38%

Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species

Goodson

Wang

2006

Proc. Natl. Acad. Sci. U.S.A.

121

160

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“…Notably, recent studies have provided much-needed information on various behavioral functions of the avian PAG and adjacent tegmentum (Shaw, 2000;Maney and Ball, 2003;Charlier et al, 2005). These tracings and functional studies have been conducted concomitantly with a large number of immunocytochemical studies, particularly focused on the distribution of neuropeptides and/or their regulation by sex steroids (Aste et al, 1991(Aste et al, , 1995(Aste et al, , 1997(Aste et al, , 1998aPanzica et al, 1998Panzica et al, , 1999bGoodson et al, 2004a;Plumari et al, 2004). Overall, the data strongly support the proposal that birds possess a "social behavior network" that is homologous to the network identified for mammals (Goodson, 2005; for a more general consideration of the avian forebrain, see Reiner et al, 2004).…”

Section: Steroid-sensitive Circuits Of the Basal Forebrain And Midbramentioning

confidence: 99%

“…As in mammals (which express a homologous neuropeptide, arginine vasopressin), the AVT neuronal population of the BSTm is often sexually dimorphic and innervates the LS in a male-biased fashion (Viglietti-Panzica et al, 1992, 1994Jurkevich et al, 1999). In most species examined, this system is strongly regulated by testosterone (T) (Voorhuis et al, 1988;Viglietti-Panzica et al, 1992;Aste et al, 1997;Panzica et al, 1999a;Plumari et al, 2004), and data from Japanese quail (Coturnix japonica) show that T regulates AVT primarily via its aromatization to estradiol (E 2 ) (Viglietti- Panzica et al, 2001). Also similar to mammals, AVT acts within the septum to modulate stress responsivity and agonistic behavior (Goodson, 1998a;Goodson and Evans, 2004).…”

Section: Vasotocin Sex Steroids and Aggressionmentioning

confidence: 99%

“…The accompanying rise in circulating T coordinates a variety of processes in the brain, many of which require that T be aromatized to E 2 . These include, but are not limited to, increased expression of neuropeptides (e.g., AVT within the BSTm-LS system) (Viglietti- Panzica et al, 2001;Plumari et al, 2004), dramatic restructuring and growth of telencephalic song nuclei (Tramontin & Brenowitz, 2000;Nottebohm, 2004), and an increase in aromatase activity within the VMH and POA (Vockel et al, 1990).…”

Section: Multi-system Integration: Birdsong and Neuroendocrine Cascadesmentioning

confidence: 99%

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Recent advances in behavioral neuroendocrinology: Insights from studies on birds

Goodson

Saldanha

Hahn

et al. 2005

Hormones and Behavior

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Ever since investigations in the field of behavioral endocrinology were hatched with experiments on roosters, birds have provided original insights into issues of fundamental importance for all vertebrate groups. Here we focus on more recent advances that continue this tradition, including 1) environmental regulation of neuroendocrine and behavioral systems, 2) steroidogenic enzyme functions that are related to intracrine processes and de novo production of neurosteroids, and 3) hormonal regulation of neuroplasticity. We also review recent findings on the anatomical and functional organization of steroid-sensitive circuits in the basal forebrain and midbrain. A burgeoning body of data now demonstrates that these circuits comprise an evolutionarily conserved network, thus numerous novel insights obtained from birds can be used (in a relatively straightforward manner) to generate predictions for other taxa as well. We close by using birdsong as an example that links these areas together, thereby highlighting the exceptional opportunities that birds offer for integrative studies of behavioral neuroendocrinology, and behavioral biology in general. Keywords aggression; reproduction; song; limbic system; vasotocin; photoperiod; neurosteroid; DHEA; aromatase; adult neurogenesis; estrogen; testosterone; thyroxin; hypothalamus; hippocampus; HVC; septum; GnRH; SCN; season; neuroplasticity Birds offer excellent opportunities for behavioral and neuroendocrine experiments in both the field and the laboratory, and studies conducted at this interface have historically placed avian models on the cutting edge of research (Konishi et al., 1989; also see Wingfield, this issue). Indeed, wild birds offer a combination of accessibility (being diurnal and terrestrial) and diversity (social and ecological) that makes them invaluable models for studying mechanistic and evolutionary questions that are not as tractable in other vertebrate groups. This diversity can be studied within the context of neural and endocrine systems that share many features with those of other taxa (thereby increasing the general relevance of avian studies) (Goodson, 2005), although these features are often more pronounced in birds. Such examples include exceptionally robust and widespread neural aromatase activity, and adult neurogenesis in the forebrain, both of which are considered further below (also see Ball and Balthazart, 2004;

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“…Although the AVT and AVP systems have a range of homeostatic functions, including stress responsiveness and osmoregulation (Simon-Oppermann et al, 1980;Madison et al, 2008), this peptide acts within several nodes of the social behavior network to regulate sex and species-typical behaviors (Santangelo and Bass, 2006;Goodson et al, 2009a;Kabelik et al, 2009). In birds, AVT expressing cell bodies in the bed nucleus of the stria terminalis (BSTm) are selectively responsive to social stimuli and are implicated in regulating male territorial aggression, while AVT in the PVN is involved in homeostatic function (Kiss et al, 1987;Panzica et al, 1999;Plumari et al, 2004;Goodson and Wang, 2006;Goodson et al, 2009b;Fokidis and Deviche, 2012). Therefore, we also examined whether AVT expression differed within the BSTm and PVN of male song sparrows living in rural and urban habitats.…”

Section: Introductionmentioning

confidence: 99%

Two Neural Measures Differ between Urban and Rural Song Sparrows after Conspecific Song Playback

Sewall

Davies

2017

Front. Ecol. Evol.

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Urbanization is a critical form of environmental change that can affect the physiology and behavior of wild animals and, notably, birds. One behavioral difference between birds living in urban and rural habitats is that urban males show elevated boldness or territorial aggression in response to simulated social challenge. This pattern has been described in several populations of song sparrow, Melospiza melodia. Such behavioral differences must be underpinned by differences in the brain, yet little work has explored how urbanization and neural function may be interrelated. We explored the relationship between urbanization and neural activation within a network of brain regions, collectively called the social behavior network, which contributes to the regulation of territorial aggression. Specifically, we captured free-living, territorial male song sparrows by playing them conspecific songs for 6-11 min, and then collected their brains. We estimated recent neural activation, as indicated by the immediate early gene FOS, and measured levels of a neuropeptide, arginine vasotocin (AVT), which is involved in the regulation of social behavior. Based on previous studies we expected urban males, which are generally more territorially aggressive, to have lower FOS expression in a node of the social behavior network implicated in regulating territoriality, the lateral septum (LS). Additionally, we expected urban males to have lower AVT expression in a brain region involved in the regulation of sociality, the medial bed nucleus of the stria terminalis (BSTm). We found that, compared to rural males, urban male song sparrows did have lower FOS expression in the LS. This pattern suggests that lower neural activation in the LS could contribute to behavioral adjustments to urbanization in male song sparrows. Additionally, counter to our predictions, urban male song sparrows had higher AVT-like immunoreactivity in the BSTm. Future work building upon these findings is needed to determine the causal role of such neural differences across rural and urban habitats. Understanding the mechanisms impacted by urbanization will inform our understanding of the reversibility and consequences of this form of habitat change.

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Region-specific testosterone modulation of the vasotocin-immunoreactive system in male dark-eyed junco, Junco hyemalis

Cited by 24 publications

References 38 publications

Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species

Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species

Recent advances in behavioral neuroendocrinology: Insights from studies on birds

Two Neural Measures Differ between Urban and Rural Song Sparrows after Conspecific Song Playback

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