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

Abstract

IntroductionThe contemporary study of adult neurogenesis has it origins in work on communication behavior. In the 1980s, Fernando Nottebohm and colleagues showed that changes in the songs of canaries correlated with addition of neurons in a brain region (the high vocal center) that controls vocal behavior (Goldman and Nottebohm, 1983;Alvarez-Buylla et al., 1988). Since then, many studies in vertebrates have shown that social interaction influences cell proliferation and neurogenesis in the brain (Lieberwirth and Wang, 2012;Gheusi et al., 2009;Font et al., 2012;Almli and Wilczynski, 2009;Barnea and Pravosudov, 2011). However, given the complexity of social signaling in most species, it is often difficult to identify specific features of social interaction that are effective for influencing neurogenesis. Moreover, the brain regions that show adult neurogenesis are usually embedded in complex networks and are only indirectly connected to the production of communication signals. Thus it is difficult to describe the precise role of new neurons in contributing to behavioral change.In electric fish, however, these problems are simplified. Electric fish are unusually good models for investigating the link between the social environment and neurogenesis because brain regions controlling communication signals have single functions and their activity is closely connected to the behavioral output of the whole animal. For example, neurons in the prepacemaker nucleus (PPn), a region that controls certain electrocommunication signals, are only two synapses removed from the final effector cells that generate the communication signal. Because the PPn has only one predominant output, the behavioral relevance of new neurons added to this nucleus during adulthood can be determined with relative ease. Another advantage of electric fish is that components of social interaction can be separated readily because their primary mode of social signaling, electrocommunication signals, is relatively simple and thus easily manipulated and presented experimentally. Thus, electric fish are quite useful for dissecting out the specific components of social interaction responsible for enhanced adult neurogenesis.Here, we begin by briefly describing an electrocommunication behavior termed chirping and its neural control. Then we review our work showing that long-term social interaction (1-2weeks) between electric fish (Apteronotus leptorhynchus) increases both the production of chirps and the addition of new cells to the brain, particularly near the region that regulates chirping. By manipulating the social stimuli presented to the fish, we demonstrate that dynamic and novel social stimuli are most effective in enhancing both the rate of chirp production and cell addition. We describe experiments showing that cortisol mediates, at least in part, the effect of long-term social interaction on chirping behavior and brain cell addition. Finally, we summarize our studies of a closely related electric fish (Brachyhypopomus gauderio) demonstrating that s...

Predators inhibit brain cell proliferation in natural populations of electric fish, Brachyhypopomus occidentalis

“…Nonetheless, it offers support from natural populations that small glucocorticoid increases in unstressed conditions promote cell proliferation [2,14]. This finding is also consistent with laboratory studies of another electric fish, A. leptorhynchus, in which small elevations in basal cortisol from exogenous treatment or social interaction both promote brain cell addition [16,46], and of zebrafish, in which elevated cortisol from environmental enrichment correlates positively with brain cell proliferation [29].…”

“…In other animals, brain cell proliferation and neurogenesis depend on neural activity within the brain region, allowing for region-specific, experience-dependent responses to environmental change [1,2,45]. In another electric fish, A. leptorhynchus, an enhanced social environment increases cell addition in midbrain regions associated with electrocommunication, but not in midbrain regions less closely tied to social interaction [16,46]. However, in B. occidentalis, we did not observe such differential proliferative response by region, indicating that all three brain regions show similar neural activity or that the forebrain cell proliferation of electric fish is not activity-dependent.…”

“…Experimental exposure to predators or their odours can increase the production of glucocorticoids [9,11 -13], and exogenous glucocorticoids can inhibit the production of proliferating cells [7,14]. However, the observed relationships between predators, glucocorticoids and brain cell proliferation are not consistent or simple: in some cases, predator exposure increases glucocorticoids without affecting brain cell proliferation [15], while in other cases environmental manipulations that increase glucocorticoids can enhance brain cell proliferation [7,16]. This inconsistency is paralleled by results from natural populations: in some cases, populations exposed to high predation pressure have higher basal glucocorticoid levels or glucocorticoid responses to acute stress [17,18], while in other cases they do not [19,20].…”

Fish Neurogenesis in Context: Assessing Environmental Influences on Brain Plasticity within a Highly Labile Physiology and Morphology

“…In electric fish, i.e. A. leptorhynchus, Dunlap et al [2006Dunlap et al [ , 2013 examined the effect of same-sex dyadic interaction (7 days) after a long period of social isolation. Fish housed in pairs had ∼ 4 times more cell addition (cell birth plus 4 day survival) in the midbrain than fish that remained isolated.…”

Electric fishes: neural systems, behaviour and evolution

“…These processes demand interdisciplinary approaches and integration across different levels of biological organization. Weakly electric fishes facilitate these sorts of integrative studies, ranging from the control of electric behaviours and sensory processing by hormones and neuromodulators (Gavassa et al, 2013;Silva et al, 2013;Smith, 2013;Toscano Marquez et al, 2013;Markham, 2013) to neurogenesis (Dunlap, 2013) and tissue regeneration (Unguez, 2013). In the upcoming years we expect the experimental advantages of electric fish to be exploited to also address questions of higherorder brain function, such as those related to cognition.…”