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Influence of long-term social interaction on chirping behavior, steroid levels and neurogenesis in weakly electric fish.

ABSTRACT: Social interactions dramatically affect the brain and behavior of animals. Studies in birds and mammals indicate that socially induced changes in adult neurogenesis participate in the regulation of social behavior, but little is known about this relationship in fish. Here, we review studies in electric fish (Apteronotus leptorhychus) that link social stimulation, changes in electrocommunication behavior and adult neurogenesis in brain regions associated with electrocommunication. Compared with isolated fish, fish living in pairs have greater production of chirps, an electrocommunication signal, during dyadic interactions and in response to standardized artificial social stimuli. Social interaction also promotes neurogenesis in the periventricular zone, which contributes born cells to the prepacemaker nucleus, the brain region that regulates chirping. Both long-term chirp rate and periventricular cell addition depend on the signal dynamics (amplitude and waveform variation), modulations (chirps) and novelty of the stimuli from the partner fish. Socially elevated cortisol levels and cortisol binding to glucocorticoid receptors mediate, at least in part, the effect of social interaction on chirping behavior and brain cell addition. In a closely related electric fish (Brachyhypopomus gauderio), social interaction enhances cell proliferation specifically in brain regions for electrocommunication and only during the breeding season, when social signaling is most elaborate. Together, these studies demonstrate a consistent correlation between brain cell addition and environmentally regulated chirping behavior across many social and steroidal treatments and suggest a causal relationship.

SUBMITTER: Dunlap KD

PROVIDER: S-EPMC3680506 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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Influence of long-term social interaction on chirping behavior, steroid levels and neurogenesis in weakly electric fish.

Dunlap Kent D KD Chung Michael M Castellano James F JF

The Journal of experimental biology 20130701 Pt 13

Social interactions dramatically affect the brain and behavior of animals. Studies in birds and mammals indicate that socially induced changes in adult neurogenesis participate in the regulation of social behavior, but little is known about this relationship in fish. Here, we review studies in electric fish (Apteronotus leptorhychus) that link social stimulation, changes in electrocommunication behavior and adult neurogenesis in brain regions associated with electrocommunication. Compared with i ...[more]

PMID: 23761468

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Project description:Mormyrid weakly electric fish produce short, pulse-type electric organ discharges for actively probing their environment and to communicate with conspecifics. Animals emit sequences of pulse-trains that vary in overall frequency and temporal patterning and can lead to time-locked interactions with the discharge activity of other individuals. Both active electrolocation and electrocommunication are additionally accompanied by stereotypical locomotor patterns. However, the concrete roles of electrical and locomotor patterns during social interactions in mormyrids are not well understood. Here we used a mobile fish dummy that was emitting different types of electrical playback sequences to study following behavior and interaction patterns (electrical and locomotor) between individuals of weakly electric fish. We confronted single individuals of Mormyrus rume proboscirostris with a mobile dummy fish designed to attract fish from a shelter and recruit them into an open area by emitting electrical playbacks of natural discharge sequences. We found that fish were reliably recruited by the mobile dummy if it emitted electrical signals and followed it largely independently of the presented playback patterns. While following the dummy, fish interacted with it spatially by displaying stereotypical motor patterns, as well as electrically, e.g. through discharge regularizations and by synchronizing their own discharge activity to the playback. However, the overall emission frequencies of the dummy were not adopted by the following fish. Instead, social signals based on different temporal patterns were emitted depending on the type of playback. In particular, double pulses were displayed in response to electrical signaling of the dummy and their expression was positively correlated with an animals' rank in the dominance hierarchy. Based on additional analysis of swimming trajectories and stereotypical locomotor behavior patterns, we conclude that the reception and emission of electrical communication signals play a crucial role in mediating social interactions in mormyrid weakly electric fish.

Project description:Adult neurogenesis, an essential mechanism of brain plasticity, enables brain development along postnatal life, constant addition of new neurons, neuronal turnover, and/or regeneration. It is amply distributed but negatively modulated during development and along evolution. Widespread cell proliferation, high neurogenic, and regenerative capacities are considered characteristics of teleost brains during adulthood. These anamniotes are promising models to depict factors that modulate cell proliferation, migration, and neurogenesis, and might be intervened to promote brain plasticity in mammals. Nevertheless, the migration path of derived cells to their final destination was not studied in various teleosts, including most weakly electric fish. In this group adult brain morphology is attributed to sensory specialization, involving the concerted evolution of peripheral electroreceptors and electric organs, encompassed by the evolution of neural networks involved in electrosensory information processing. In wave type gymnotids adult brain morphology is proposed to result from lifelong region specific cell proliferation and neurogenesis. Consistently, pulse type weakly electric gymnotids and mormyrids show widespread distribution of proliferation zones that persists in adulthood, but their neurogenic potential is still unknown. Here we studied the migration process and differentiation of newborn cells into the neuronal phenotype in the pulse type gymnotid Gymnotus omarorum. Pulse labeling of S-phase cells with 5-Chloro-2'-deoxyuridine thymidine followed by 1 to 180 day survivals evidenced long distance migration of newborn cells from the rostralmost telencephalic ventricle to the olfactory bulb, and between layers of all cerebellar divisions. Shorter migration appeared in the tectum opticum and torus semicircularis. In many brain regions, derived cells expressed early neuronal markers doublecortin (chase: 1-30 days) and HuC/HuD (chase: 7-180 days). Some newborn cells expressed the mature neuronal marker tyrosine hydroxylase in the subpallium (chase: 90 days) and olfactory bulb (chase: 180 days), indicating the acquisition of a mature neuronal phenotype. Long term CldU labeled newborn cells of the granular layer of the corpus cerebelli were also retrogradely labeled "in vivo," suggesting their insertion into the neural networks. These findings evidence the neurogenic capacity of telencephalic, mesencephalic, and rhombencephalic brain proliferation zones in G. omarorum, supporting the phylogenetic conserved feature of adult neurogenesis and its functional significance.

Dataset Information

Influence of long-term social interaction on chirping behavior, steroid levels and neurogenesis in weakly electric fish.

Publications

Influence of long-term social interaction on chirping behavior, steroid levels and neurogenesis in weakly electric fish.

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