Vasotocin Immunoreactivity in Goldfish Brains: Characterizing Primitive Circuits Associated with Social Regulation

Thompson, Ronald G.; Walton, James C.

doi:10.1159/000219485

Cited by 29 publications

(28 citation statements)

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“…However, both AVT and IT are also present in quantifiable levels in all major brain areas, therefore confirming the ubiquitous presence of these neuropeptides in the teleost fish brain as suggested by previous ICC and ISH studies Dewan et al, 2008Goodson and Bass, 2001;Goodson et al, 2003;Holmqvist and Ekstrom, 1995;Saito et al, 2004;Thompson and Walton, 2009) and supporting their role as central neuromodulators (Goodson, 2008;Goodson and Thompson, 2010). In this respect it is particularly interesting the finding of significantly high levels of AVT in the olfactory bulbs, which was by far the brain region with the highest concentration of this peptide.…”

Section: Discussionsupporting

confidence: 83%

“…In fish these nonapeptides are produced by neurons localized in the parvocellular and magnocellular nuclei of the preoptic area, that project both to the neurohypophysis, where AVT/IT are released in the systemic circulation, and to multiple extrahypothalamic regions, namely the ventral telencephalon, the thalamus and the mesencephalon (Goodson and Bass, 2001;Goodson et al, 2003;Holmqvist and Ekstrom, 1995;Thompson and Walton, 2009). The functionality of the wide extrahypothalamic projections is confirmed by the presence of AVT/IT receptors in most brain regions, in particular the AVT V1a receptor (Hausmann et al, 1995;Kline et al, 2011;Lema, 2010;Lema et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Brain levels of arginine–vasotocin and isotocin in dominant and subordinate males of a cichlid fish

Almeida

Gozdowska

Kulczykowska

et al. 2012

Hormones and Behavior

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The nonapeptides arginine-vasotocin (AVT) and isotocin (IT), which are the teleost homologues of argininevasopressin and oxytocin in mammals, have well established peripheral effects on osmoregulation and stress response, and central effects on social behavior. However, all studies that have looked so far into the relationship between these nonapeptides and social behavior have used indirect measures of AVT/IT activity (i.e. immunohistochemistry of AVT/IT immunoreactive neurons, or AVT/IT or their receptors mRNA expression with in situ hybridization or qPCR) and therefore direct measures of peptide levels in relation to social behavior are still lacking. Here we use a recently developed high-performance liquid chromatography analysis with fluorescence detection (HPLC-FL) method to quantify the levels of both AVT and IT in macro-dissected brain areas [i.e. olfactory bulbs, telencephalon, diencephalon, optic tectum, cerebellum, and hindbrain (= rhombencephalon minus cerebellum)] and pituitary of dominant and subordinate male cichlid fish (Oreochromis mossambicus). The pituitary shows higher levels of both peptides than any of the brain macroareas, and the olfactory bulbs have the highest AVT among all brain areas. Except for IT in the telencephalon there is a lack of correlations between central levels and pituitary peptide levels, suggesting an independent control of hypophysial and CNS nonapeptide secretion. There were also no correlations between AVT and IT levels either for each brain region or for the pituitary gland, suggesting a decoupled activity of the AVT and IT systems at the CNS level. Subordinate AVT pituitary levels are significantly higher than those of dominants, and dominant hindbrain IT levels are significantly higher than those of subordinates, suggesting a potential involvement of AVT in social stress in subordinate fish and of IT in the regulation of dominant behavior at the level of the hindbrain. Since in this species dominant males use urine to communicate social status and since AVT is known to have an antidiuretic effect, we have also investigated the effect of social status on urine storage. As predicted, dominant males stored significantly more urine than subordinates. Given these results we suggest that AVT/IT play a key role in orchestrating social phenotypes, acting both as central neuromodulators that promote behavioral plasticity and as peripheral hormones that promote integrated physiological changes.

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Section: Discussionsupporting

confidence: 83%

Section: Introductionmentioning

confidence: 99%

Brain levels of arginine–vasotocin and isotocin in dominant and subordinate males of a cichlid fish

Almeida

Gozdowska

Kulczykowska

et al. 2012

Hormones and Behavior

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“…Although we did not see a correlation between pre-optic AVT-ir fiber density and courtship levels, such a correlation may exist for one or more distant targets of AVT-ir axons in the telencephalon, diencephalon, midbrain and hindbrain [see Goodson et al, 2003;Dewan et al, 2008;Thompson and Walton, 2009]. The involvement of multiple brain regions in mediating AVT's effects on social behaviors would be consistent with reports for tetrapods.…”

Section: Courtshipsupporting

confidence: 80%

Individual Behavioral and Neuronal Phenotypes for Arginine Vasotocin Mediated Courtship and Aggression in a Territorial Teleost

Santangelo

Bass

2010

Brain Behav Evol

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The neuropeptide arginine vasotocin (AVT) is well known to modulate both aggression and affiliation, yet few studies relate individual behavioral state to a quantitative assessment of AVT distribution in the brain. Here, using a wild population of beaugregory damselfish, Stegastes leucostictus, we assess: (1) the effect of AVT on courtship, and (2) with reference to our previous study on AVT modulation of aggression in this species, the relationship between AVT-like immunoreactive (ir) fiber distribution in the forebrain’s preoptic area and individual courtship and aggression levels. Exogenous AVT did not affect courtship, yet Manning compound, an arginine vasopressin (AVP) V1a receptor antagonist, significantly lowered but did not eradicate courtship. Consistent with AVT’s known facilitation of aggression in this species, the density of AVT-ir fibers in the preoptic area was significantly negatively correlated to aggression. Our findings match similar behavioral and immunoreactive patterns of neuropeptide secretion in other taxa. Unlike aggression, preoptic AVT-ir fiber density was not significantly correlated to individual courtship levels. The results suggest a differential involvement of preoptic AVT neurons and/or their receptors in supporting the expression of aggression and courtship.

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“…Three populations of AVT neurons in fish brains are distributed along the third ventricle in the ventral portion of the preoptic area in the anterior hypothalamus (Lema and Nevitt, 2004a;Dewan et al, 2008;Thompson and Walton, 2009). The parvocellular AVT neuron population (homologous to the supraoptic nucleus in tetrapods) is located at the rostral and ventral portion of the preoptic area; magnocellular and gigantocellular AVT neuron groups (homologous to the paraventricular nucleus in tetrapods) are found more caudally and dorsally (Kapsimali et al, 2001;Urano and Ando, 2011;Godwin and Thompson, 2012).…”

Section: Differential Avt Modulation Of Two Types Of Aggressionmentioning

confidence: 99%

Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression

Silva

Perrone

Zubizarreta

et al. 2013

Journal of Experimental Biology

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SummaryAgonistic behavior has shaped sociality across evolution. Though extremely diverse in types of displays and timing, agonistic encounters always follow the same conserved phases (evaluation, contest and post-resolution) and depend on homologous neural circuits modulated by the same neuroendocrine mediators across vertebrates. Among neuromodulators, serotonin (5-HT) is the main inhibitor of aggression, and arginine vasotocin (AVT) underlies sexual, individual and social context differences in behavior across vertebrate taxa. We aim to demonstrate that a distinct spatio-temporal pattern of activation of the social behavior network characterizes each type of aggression by exploring its modulation by both the 5-HT and AVT systems. We analyze the neuromodulation of aggression between the intermale reproduction-related aggression displayed by the gregarious Brachyhypopomus gauderio and the non-breeding intrasexual and intersexual territorial aggression displayed by the solitary Gymnotus omarorum. Differences in the telencephalic activity of 5-HT between species were paralleled by a differential serotonergic modulation through 1A receptors that inhibited aggression in the territorial aggression of G. omarorum but not in the reproduction-related aggression of B. gauderio. AVT injection increased the motivation towards aggression in the territorial aggression of G. omarorum but not in the reproduction-related aggression of B. gauderio, whereas the electric submission and dominance observed in G. omarorum and B. gauderio, respectively, were both AVT-dependent in a distinctive way. The advantages of our model species allowed us to identify precise target areas and mechanisms of the neuromodulation of two types of aggression that may represent more general and conserved strategies of the control of social behavior among vertebrates.

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Vasotocin Immunoreactivity in Goldfish Brains: Characterizing Primitive Circuits Associated with Social Regulation

Cited by 29 publications

References 100 publications

Brain levels of arginine–vasotocin and isotocin in dominant and subordinate males of a cichlid fish

Brain levels of arginine–vasotocin and isotocin in dominant and subordinate males of a cichlid fish

Individual Behavioral and Neuronal Phenotypes for Arginine Vasotocin Mediated Courtship and Aggression in a Territorial Teleost

Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression

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