Pheromones enhance somatosensory processing in newt brains through a vasotocin-dependent mechanism

Thompson, Ronald G.; Dickinson, Patsy S.; Rose, James D.; Dakin, Kelly Anne; Civiello, G.M; Segerdahl, Andrew R.; Bartlett, R. P.

doi:10.1098/rspb.2008.0207

Cited by 18 publications

(5 citation statements)

References 38 publications

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“…Given that social contact is not affected by infusions of V 1a and OT antagonists into the lateral ventricle and/or LS (Goodson et al, 2009c), the antisense effect on contact time is unlikely to be mediated via BSTm projections to the LS, and may reflect VT actions in areas outside of the forebrain altogether (i.e., in areas distal to the ventricular antagonist infusions). Interestingly, endogenous VT inhibits social approach in goldfish via a cascade that includes descending parvocellular projections to autonomic hindbrain nuclei, activation of substance P vagal efferents, and feedback to the brain from peripheral body state (Thompson et al, 2008a). However, although these descending projections are strongly conserved across all vertebrate taxa (DeVries et al, 1985; Caffe et al, 1989; Panzica et al, 1999; Thompson et al, 2008b; Thompson and Walton, 2009), they appear to primarily arise from parvocellular neurons in the preoptic area (in anamniotes) and homologous neurons in the PVN of amniotes (De Vries and Buijs, 1983; Goodson et al, 2003; Thompson and Walton, 2009), not the BSTm cell group, which is lacking in fish altogether (Goodson et al, 2003; Greenwood et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty

Kelly

Kingsbury

Hoffbuhr

et al. 2011

Hormones and Behavior

119

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Previous comparisons of territorial and gregarious finches (family Estrildidae) suggest the hypothesis that arginine vasotocin (VT) neurons in the medial bed nucleus of the stria terminalis (BSTm) and V 1a -like receptors in the lateral septum (LS) promote flocking behavior. Consistent with this hypothesis, we now show that intraseptal infusions of a V 1a antagonist in male zebra finches (Taeniopygia guttata) reduce gregariousness (preference for a group of 10 versus 2 conspecific males), but have no effect on the amount of time that subjects spend in close proximity to other birds ("contact time"). The antagonist also produces a profound increase in anxiety-like behavior, as exhibited by an increased latency to feed in a novelty-suppressed feeding test. Bilateral knockdown of VT production in the BSTm using LNA-modified antisense oligonucleotides likewise produces increases in anxiety-like behavior and a potent reduction in gregariousness, relative to subjects receiving scrambled oligonucleotides. The antisense oligonucleotides also produced a modest increase in contact time (irrespective of group size). Together, these combined experiments provide clear evidence that endogenous VT promotes preferences for larger flock sizes, and does so in a manner that is coupled to general anxiolysis. Given that homologous peptide circuitry of the BSTm-LS is found across all tetrapod vertebrate classes, these findings may be predictive for other highly gregarious species.Central nonapeptide circuits play phylogenetically widespread roles in the modulation of social behaviors and stress responses and often exert their effects in a species-specific manner (Engelmann et al., 2004;De Vries and Panzica, 2006;Donaldson and Young, 2008;Veenema and Neumann, 2008;Choleris et al., 2009;Goodson and Thompson, 2010). These circuits arise primarily from magnocellular and parvocellular neurons in the preoptic area and hypothalamus that produce either arginine vasotocin (VT; in nonmammalian vertebrates) or arginine vasopressin (VP; in mammals), plus a single oxytocin-like peptide form in any given species. In addition to these cell groups, virtually all tetrapods, including humans, exhibit VT/VP neurons in the medial extended amygdala, primarily within the medial bed nucleus of the stria terminalis (BSTm) (De Vries and Panzica, 2006;Goodson and Thompson, 2010). Unlike the various hypothalamic VT/VP cell groups, the BSTm neurons and their projections to basal forebrain sites such as the lateral septum (LS), medial preoptic area and habenula Absil et al., 2002) are typically sexually

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Section: Discussionmentioning

confidence: 99%

Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty

Kelly

Kingsbury

Hoffbuhr

et al. 2011

Hormones and Behavior

119

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“…Alternatively, or in addition, AD could activate AVT cells that project to the optic tectum in goldfish [Thompson and Walton, 2009] and thus directly modulate the processing of visual stimuli in ways that lead to decreased social approach. A similar mechanism by which AVT mediates cross-modal sensorimotor integration has been shown in male roughskin newts, in which female sex pheromones enhance the processing of somatosensory stimuli involved in the regulation of courtship clasping [Thompson et al, 2008a]. …”

Section: Discussionmentioning

confidence: 82%

Pheromone Exposure Influences Preoptic Arginine Vasotocin Gene Expression and Inhibits Social Approach Behavior in Response to Rivals but Not Potential Mates

Mangiamele

Keeney²,

D’Agostino

et al. 2013

Brain Behav Evol

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The nonapeptides arginine vasotocin (AVT) and vasopressin mediate a variety of social behaviors in vertebrates. However, the effects of these peptides on behavior can vary considerably both between and within species. AVT, in particular, stimulates aggressive and courtship responses typical of dominant males in several species, although it can also inhibit social interactions in some cases. Such differential effects may depend upon AVT influences within brain circuits that differ among species or between males that adopt alternative reproductive phenotypes and/or upon the differential activation of those circuits in different social contexts. However, to date, very little is known about how social stimuli that promote alternative behavioral responses influence AVT circuits within the brain. To address this issue, we exposed adult male goldfish to androstenedione (AD), a pheromonal signal that is released by both males and females during the breeding season, and measured social approach responses of males towards same- and other-sex individuals before and after AD exposure. In a second experiment, we measured AD-induced AVT gene expression using in situ hybridization. We found that brief exposure to AD induces social avoidance in response to rival males, but does not affect the level of sociality exhibited in response to sexually receptive females. Exposure to AD also increases AVT gene expression in the preoptic area of male goldfish, particularly in the parvocellular population of the preoptic nucleus. Together, these data suggest that AD is part of a social signaling system that induces social withdrawal specifically during male-male interactions by activating AVT neurons.

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“…It is possible that VT mediates social spacing during the breeding season, which is dependent on social signals indicative of whether a female is ovulating and ready to spawn. Indeed, social stimuli have been shown to activate VT/VP cells and/or drive peptide release in numerous species (Beiderbeck et al, 2007; Ebner et al, 2005; Gobrogge et al, 2007; Goodson and Evans, 2004; Goodson and Wang, 2006; Greenwood et al, 2008; Lim and Young, 2004; Thompson et al, 2008a). Male and female goldfish both excrete androstenedione (AD) at particular times during the reproductive season; males excrete high levels when exposed to female sexual stimuli (Sorensen et al, 2005), whereas females excrete high levels early in their ovulatory cycle before they are ready to spawn (Scott and Sorensen, 1994).…”

Section: Discussionmentioning

confidence: 99%

Behavioral effects of hindbrain vasotocin in goldfish are seasonally variable but not sexually dimorphic

et al. 2010

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We have previously demonstrated that centrally administered vasotocin (VT) inhibits social approach toward same-sex conspecifics in male and female goldfish, and that this behavioral effect is dependent upon VT projections to the hindbrain. We now show that there are no sex differences in sensitivity to the behavioral effects of VT, though differences do exist in responsiveness across seasons in both sexes. A central dose of 1 µg, but not 200 ng, inhibited social approach in goldfish in non-reproductive condition, whereas a dose as low as 40 ng inhibited social approach in fish in full reproductive condition. In males and females in full reproductive condition, social approach behavior was facilitated by central administration of 500 ng of a V1A specific antagonist. In addition, the behavioral effects of exogenously administered central VT were blocked by central administration of 1 µg of a V1A antagonist. These results demonstrate that the propensity to approach a conspecific, a simple behavior underlying many social interactions, is controlled by a V1A-like receptor, and that VT’s behavioral effects depend on reproductive context. Quantitative real-time PCR showed that the seasonal changes in behavioral responsiveness to VT are associated with changes in the expression of a V1A-like receptor in the hindbrain, but not the mid- or forebrain, indicating that the seasonal regulation of social approach behavior likely depends on the local modulation of the expression of this receptor within a primitive peptide circuit in this species.

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Pheromones enhance somatosensory processing in newt brains through a vasotocin-dependent mechanism

Cited by 18 publications

References 38 publications

Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty

Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty

Pheromone Exposure Influences Preoptic Arginine Vasotocin Gene Expression and Inhibits Social Approach Behavior in Response to Rivals but Not Potential Mates

Behavioral effects of hindbrain vasotocin in goldfish are seasonally variable but not sexually dimorphic

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