Sensory feedback from electroreceptors to electromotor pacemaker centers in gymnotids

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...

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

“…During social interactions, they modulate the continuous electric organ discharge (EOD) by briefly (10-100ms) increasing the frequency of their EOD to produce signals termed 'chirps' (Larimer and MacDonald, 1968;Hagedorn and Heiligenberg, 1985;Zupanc and Maler, 1993). The precise communicatory function of chirps is not fully understood, but they are emitted at particularly high rates when male fish engage in agonistic interactions with other male fish of similar EOD frequency (within ~100Hz) (Dunlap, 2002;Hupé and Lewis, 2008;Triefenbach and Zakon, 2008).…”

Section: Introductionmentioning

confidence: 99%

Chirping response of weakly electric knife fish (Apteronotus leptorhynchus) to low-frequency electric signals and to heterospecific electric fish

Dunlap

DiBenedictis

Banever

2010

SUMMARYBrown ghost knife fish (Apteronotus leptorhynchus) can briefly increase their electric organ discharge (EOD) frequency to produce electrocommunication signals termed chirps. The chirp rate increases when fish are presented with conspecific fish or high-frequency (700-1100Hz) electric signals that mimic conspecific fish. We examined whether A. leptorhynchus also chirps in response to artificial low-frequency electric signals and to heterospecific electric fish whose EOD contains low-frequency components. Fish chirped at rates above background when presented with low-frequency (10-300Hz) sine-wave stimuli; at 30 and 150Hz, the threshold amplitude for response was 1mVcm -1 . Low-frequency (30Hz) stimuli also potentiated the chirp response to high-frequency (~900Hz) stimuli. Fish increased their chirp rate when presented with two heterospecific electric fish, Sternopygus macrurus and Brachyhypopomus gauderio, but did not respond to the presence of the non-electric fish Carassius auratus. Fish chirped to low-frequency (150Hz) signals that mimic those of S. macrurus and to EOD playbacks of B. gauderio. The response to the B. gauderio playback was reduced when the low-frequency component (<150Hz) was experimentally filtered out. Thus, A. leptorhynchus appears to chirp specifically to the electric signals of heterospecific electric fish, and the low-frequency components of heterospecific EODs significantly influence chirp rate. These results raise the possibility that chirps function to communicate to conspecifics about the presence of a heterospecific fish or to communicate directly to heterospecific fish.

“…Wave-type EODs are continuously emitted at precise frequencies that can indicate species, sex and/or rank. When fish interact, however, they can also transiently modulate the frequency and/or amplitude of their EODs to produce different types of signals known as chirps, gradual frequency rises (GFRs) and interruptions (Dye, 1987;Hagedorn and Heiligenberg, 1985;Hopkins, 1974b;Larimer and MacDonald, 1968). In A. leptorhynchus, chirping is highly sexually dimorphic, with males chirping more than females Kolodziejski et al, 2005;Zupanc and Maler, 1993).…”

Section: Introductionmentioning

confidence: 99%

Structure and sexual dimorphism of the electrocommunication signals of the weakly electric fish,Adontosternarchus devenanzii

Zhou

Smith

2006

Reproductive and agonistic communication signals are among the most conspicuous and diverse of animal behaviors. These signals vary both across and within species, are often highly sexually dimorphic and can therefore serve as models for understanding the evolution of behavioral diversity and the mechanisms that regulate sex differences in behavior.The electrocommunication signals of weakly electric fish provide an opportunity to study the mechanisms and evolution of diversity in sexually dimorphic communication. Both African mormyriform and Neotropical gymnotiform fishes possess electric organs whose weak electrical discharges function in electrolocation and communication. The properties of electric organ discharges (EODs) differ between species and can also vary as a function of sex, reproductive condition and/or social rank (Bass, 1986;Carlson et al., 2000;Dunlap and Larkins-Ford, 2003;Franchina et al., 2001;Hagedorn and Heiligenberg, 1985;Hopkins, 1988;Kramer et al., 1980;Zakon and Smith, 2002). Each species produces one of two types of discharge: pulse-type or wave-type EODs. In pulse-type EODs, the duration of each discharge is much shorter than the time between discharges, whereas the duration of each discharge for wave-type EODs is approximately the same as the time between discharges, resulting in a quasi-sinusoidal signal (reviewed by Hopkins, 1988;Moller, 1995).In species that produce wave-type EODs, the frequency of the discharge (i.e. number of discharges per second) often differs between the sexes. In most of the wave-type gymnotiform fish that have been studied, males emit lower frequency EODs than females Hagedorn and Heiligenberg, 1985;Hopkins, 1974b). Interestingly, however, in the most speciose gymnotiform family, the Apteronotidae, sex differences in EOD frequency have been studied in only three species in a single genus, and Electrocommunication signals of electric fish vary across species, sexes and individuals. The diversity of these signals and the relative simplicity of the neural circuits controlling them make them a model well-suited for studying the mechanisms, evolution and sexual differentiation of behavior. In most wave-type gymnotiform knifefishes, electric organ discharge (EOD) frequency and EOD modulations known as chirps are sexually dimorphic. In the most speciose gymnotiform family, the Apteronotidae, EOD frequency is higher in males than females in some species, but lower in males than females in others. Sex differences in EOD frequency and chirping, however, have been examined in only three apteronotid species in a single genus, Apteronotus. To understand the diversity of electrocommunication signals, we characterized these behaviors in another genus, Adontosternarchus. Electrocommunication signals of Adontosternarchus devenanzii differed from those of Apteronotus in several ways. Unlike in Apteronotus, EOD frequency was not sexually dimorphic in A. devenanzii.Furthermore, although A. devenanzii chirped in response to playbacks simulating conspecific EODs, the number of chi...