Local vasotocin modulation of the pacemaker nucleus resembles distinct electric behaviors in two species of weakly electric fish

Perrone, Rossana; Migliaro, Adriana; Comas, Virginia; Quintana, Laura; Borde, Michel; Silva, Ana C.

doi:10.1016/j.jphysparis.2014.07.007

Cited by 21 publications

(24 citation statements)

References 60 publications

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“…Previous studies demonstrated that AVT differentially modulates EOD-BR in the two study species [Perrone et al, 2010;Perrone et al, 2014]. These differences are also evident at the medullary PN in which AVT induces a large persistent increase in firing rate in B. gauderio but a small transient one in G. omarorum [Perrone et al, 2010[Perrone et al, , 2014. Interestingly, these differences resemble the species differences in the dynamics of the nocturnal increase presented in this study.…”

Section: Discussionsupporting

confidence: 81%

“…Identifying differences in electric behavior among species with different sociality prompted us to explore whether differences in the system of hypothalamic neuropeptides contribute to their control. Previous studies demonstrated that AVT differentially modulates EOD-BR in the two study species [Perrone et al, 2010;Perrone et al, 2014]. These differences are also evident at the medullary PN in which AVT induces a large persistent increase in firing rate in B. gauderio but a small transient one in G. omarorum [Perrone et al, 2010[Perrone et al, , 2014.…”

Section: Discussionmentioning

confidence: 77%

“…Furthermore, endogenous AVT does not seem to regulate daytime EOD-BR, since MC does not affect EOD-BR during the light phase in either species. This lack of an MC effect, in species in which its blocking efficacy has already been demonstrated, was surprising given the consistent stimulatory effect of AVT on EOD-BR and the proven robustness of MC antagonist action [Perrone et al, 2010[Perrone et al, , 2014.…”

Section: Discussionmentioning

confidence: 95%

“…Multiple circadian clocks, central and peripheral, as well as multiple melatonin targets are observed in fish [Hurd et al, 1998;Falcon et al, 2010]. Interestingly, the preoptic area of the hypothalamus in teleosts has been reported as both an endogenous clock and a melatonin target [Falcon et al, 2010], as well as the location of AVT neurons [Dewan et al, 2008;Maruska, 2009;Perrone et al, 2014]. The reported difference in the distribution of the AVTergic system between G. omarorum and B. gauderio [Perrone et al, 2014] might represent the basis of how these species integrate circadian and social information to shape daily changes in behavior.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies in electric fish revealed a differential effect of AVT on the electric behavior of G. omarorum and B. gauderio . In freely behaving, nonbreeding adults, AVT induces a large prolonged increase in EOD-BR during the day in B. gauderio , but only a transient small effect in G. omarorum [Perrone et al, 2010[Perrone et al, , 2014. In addition, AVT regulates the socially dependent modulation of electric behavior in B. gauderio .…”

Section: Introductionmentioning

confidence: 93%

See 4 more Smart Citations

Melatonin Regulates Daily Variations in Electric Behavior Arousal in Two Species of Weakly Electric Fish with Different Social Structures

Migliaro

Silva²

2016

Brain Behav Evol

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Timing is crucial for social interactions. Animal behavior is synchronized with biotic and abiotic environment variables ensuring that the activity phase of conspecifics occurs during the same period of the day. As biological rhythms are embedded in the complex integrative control of the brain, it is fundamental to explore its interaction with environmental and social factors. This approach will unravel the link between external stimuli carrying information on environmental cycles and the neural commands for behavior, including social behavior, associated with precise phases of those cycles. Arousal in the solitary Gymnotus omarorum and in the gregarious Brachyhypopomus gauderio is characterized by a nocturnal increase in the basal discharge rate of electric behavior, which is mild and transient in G. omarorum and large and persistent in B. gauderio. In this study, we show that the major integrator of social behavior, AVT (arginine vasotocin), is not involved in the nocturnal increase of electric behavior basal rate in isolated animals of either species. On the other hand, endogenous melatonin, the major modulator of the circadian system, is responsible for the nocturnal increase in electric behavior in isolated individuals of both species.

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Section: Discussionsupporting

confidence: 81%

Section: Discussionmentioning

confidence: 77%

Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 93%

See 3 more Smart Citations

Melatonin Regulates Daily Variations in Electric Behavior Arousal in Two Species of Weakly Electric Fish with Different Social Structures

Migliaro

Silva²

2016

Brain Behav Evol

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Hormone‐mediated modulation of the electromotor CPG in pulse‐type weakly electric fish. Commonalities and differences across species

Borde

Quintana

Comas

et al. 2020

Developmental Neurobiology

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Like stomatogastric activity in crustaceans, vocalization in teleosts and frogs, and locomotion in mammals, the electric organ discharge (EOD) of weakly electric fish is a rhythmic and stereotyped electromotor pattern. The EOD, which functions in both perception and communication, is controlled by a two‐layered central pattern generator (CPG), the electromotor CPG, which modifies its basal output in response to environmental and social challenges. Despite major anatomo‐functional commonalities in the electromotor CPG across electric fish species, we show that Gymnotus omarorum and Brachyhypopomus gauderio have evolved divergent neural processes to transiently modify the CPG outputs through descending fast neurotransmitter inputs to generate communication signals. We also present two examples of electric behavioral displays in which it is possible to separately analyze the effects of neuropeptides (mid‐term modulation) and gonadal steroid hormones (long‐term modulation) upon the CPG. First, the nonbreeding territorial aggression of G. omarorum has been an advantageous model to analyze the status‐dependent modulation of the excitability of CPG neuronal components by vasotocin. Second, the seasonal and sexually dimorphic courtship signals of B. gauderio have been useful to understand the effects of sex steroids on the responses to glutamatergic inputs in the CPG. Overall, the electromotor CPG functions in a regime that safeguards the EOD waveform. However, prepacemaker influences and hormonal modulation enable an enormous versatility and allows the EOD to adapt its functional state in a species‐, sex‐, and social context‐specific manners.

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Genes linked to species diversity in a sexually dimorphic communication signal in electric fish

et al. 2017

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Sexually dimorphic behaviors are often regulated by androgens and estrogens. Steroid receptors and metabolism are control points for evolutionary changes in sexual dimorphism. Electric communication signals of South American knifefishes are a model for understanding the evolution and physiology of sexually dimorphic behavior. These signals are regulated by gonadal steroids and controlled by a simple neural circuit. Sexual dimorphism of the signals varies across species. We used transcriptomics to examine mechanisms for sex differences in electric organ discharges (EODs) of two closely related species, Apteronotus leptorhynchus and Apteronotus albifrons, with reversed sexual dimorphism in their EODs. The pacemaker nucleus (Pn), which controls EOD frequency (EODf), expressed transcripts for steroid receptors and metabolizing enzymes, including androgen receptors, estrogen receptors, aromatase, and 5α-reductase. The Pn expressed mRNA for ion channels likely to regulate the high-frequency activity of Pn neurons and for neuromodulator and neurotransmitter receptors that may regulate EOD modulations used in aggression and courtship. Expression of several ion channel genes, including those for Kir3.1 inward-rectifying potassium channels and sodium channel β1 subunits, was sex-biased or correlated with EODf in ways consistent with EODf sex differences. Our findings provide a basis for future studies to characterize neurogenomic mechanisms by which sex differences evolve.

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Local vasotocin modulation of the pacemaker nucleus resembles distinct electric behaviors in two species of weakly electric fish

Cited by 21 publications

References 60 publications

Melatonin Regulates Daily Variations in Electric Behavior Arousal in Two Species of Weakly Electric Fish with Different Social Structures

Melatonin Regulates Daily Variations in Electric Behavior Arousal in Two Species of Weakly Electric Fish with Different Social Structures

Hormone‐mediated modulation of the electromotor CPG in pulse‐type weakly electric fish. Commonalities and differences across species

Genes linked to species diversity in a sexually dimorphic communication signal in electric fish

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