Electric interactions through chirping behavior in the weakly electric fish, Apteronotus leptorhynchus

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.

Section: Introductioncontrasting

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

“…When two fish are in close enough proximity so that their electric fields interact (within approximately 1m), the interactions of the electric fields continuously produce amplitude and phase modulations (Heiligenberg, 1991;Tan et al, 2005;Stamper et al, 2010). In Apteronotus, fish can also produce rapid, intermittent transients in their electric field (Zupanc et al, 2006;Dunlap et al, 2010), especially during agonistic encounters . In the ELL, the cancellation of the predictable amplitude modulations that result from the mixing of electric organ discharges (EODs) from nearby fish also induces a concomitant enhancement of the responses to unpredictable chirp signals (Marsat and Maler, 2011).…”

Section: Tail Bending Contributes To Sensory Processingmentioning

confidence: 99%

Active sensing via movement shapes spatiotemporal patterns of sensory feedback

Stamper

Roth

Cowan

et al. 2012

107

SUMMARYPrevious work has shown that animals alter their locomotor behavior to increase sensing volumes. However, an animalʼs own movement also determines the spatial and temporal dynamics of sensory feedback. Because each sensory modality has unique spatiotemporal properties, movement has differential and potentially independent effects on each sensory system. Here we show that weakly electric fish dramatically adjust their locomotor behavior in relation to changes of modality-specific information in a task in which increasing sensory volume is irrelevant. We varied sensory information during a refuge-tracking task by changing illumination (vision) and conductivity (electroreception). The gain between refuge movement stimuli and fish tracking responses was functionally identical across all sensory conditions. However, there was a significant increase in the tracking error in the dark (no visual cues). This was a result of spontaneous whole-body oscillations (0.1 to 1Hz) produced by the fish. These movements were costly: in the dark, fish swam over three times further when tracking and produced more net positive mechanical work. The magnitudes of these oscillations increased as electrosensory salience was degraded via increases in conductivity. In addition, tail bending (1.5 to 2.35Hz), which has been reported to enhance electrosensory perception, occurred only during trials in the dark. These data show that both categories of movements -whole-body oscillations and tail bends -actively shape the spatiotemporal dynamics of electrosensory feedback. Supplementary material available online at

“…olfactory signal) in the stimulus fish. However, in short-term interactions, chirping of the focal fish is quantitatively correlated (Dunlap, 2002) and temporally structured in an 'echo' pattern (Zupanc et al, 2006; with chirping in a stimulus fish. Thus it is likely that pharmacological manipulation of the stimulus fish decreased long-term chirp rates in focal fish by decreasing chirp stimuli from the stimulus fish.…”

Section: Chirping During Dyadic Interactionsmentioning

confidence: 99%

“…Chirp rate is also influenced strongly by stimulus amplitude (Bastian et al, 2001;Dunlap et al, 1998), and, because EOD amplitude attenuates drastically through the water, the distance between fish determines chirp production (Dunlap and Larkins-Ford, 2003;Zupanc et al, 2006): higher stimulus amplitudes and shorter distances between fish elicit higher chirp rates. In both dyadic interactions and chirp chambers, chirp rate habituates relatively quickly after the onset of stimulus, with chirp rates declining to half-maximal values after ~10min of stimulation (Dunlap, 2002;Harvey-Girard et al, 2010).…”

Section: Introduction To Chirping Behavior and Its Neural Controlmentioning

confidence: 99%

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

Dunlap

Chung

Castellano

2013

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...