A central pacemaker that underlies the production of seasonal and sexually dimorphic social signals: anatomical and electrophysiological aspects

Abstract

Our long-term goal is to approach the understanding of the anatomical and physiological bases for communication signal diversity in gymnotiform fishes as a model for vertebrate motor pattern generation. Brachyhypopomus gauderio emits, in addition to its electric organ discharge (EOD) at basal rate, a rich repertoire of rate modulations. We examined the structure of the pacemaker nucleus, responsible for the EOD rate, to explore whether its high output signal diversity was correlated to complexity in its neural components or regional organization. We confirm the existence of only two neuron types and show that the previously reported dorsal-caudal segregation of these neurons is accompanied by rostral-caudal regionalization. Pacemaker cells are grouped dorsally in the rostral half of the nucleus, and relay cells are mainly ventral and more abundant in the caudal half. Relay cells are loosely distributed from the center to the periphery of the nucleus in correlation to somata size. Our findings support the hypothesis that regional organization enables a higher diversity of rate modulations, possibly offering distinct target areas to modulatory inputs. Since no anatomical or electrophysiological seasonal or sexual differences were found, we explored these aspects from a functional point of view in a companion article.

Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression

“…As the pattern of emission of the electromotor output in electric fish is itself a social display [as it signals species, sex, season, status, male quality and social context (Silva et al, 2007;Perrone et al, 2009;Gavassa et al, 2012)], which relies on the activity of a well-known and accessible medullary medial nucleus (the PN) (Pouso et al, 2010;Quintana et al, 2011a;Quintana et al, 2011b), electric fish appear as a good model system to target specific brain areas of AVT actions. In a previous study, Perrone et al (Perrone et al, 2010) demonstrated that AVT induced a long-lasting and progressive increase of EOD rate in isolated B. gauderio, but had no effects in G. omarorum.…”

Environmental complexity, seasonality and brain cell proliferation in a weakly electric fish, Brachyhypopomus gauderio

“…The Pn drives the production of electric signals for electrocommunication and reproductive signaling and, in B. gauderio, its activity is modulated by social interactions and breeding conditions Quintana et al, 2010;Silva et al, 2007). For example, the nocturnal EOD rate of males is greater during the breeding season than during the non-breeding season and is further elevated when males are housed with females (Silva et al, 2007).…”

A JAR of Chirps: The Gymnotiform Chirp Can Function as Both a Communication Signal and a Jamming Avoidance Response

“…The neuronal network (Figure 10) controlling the modulations of the EOD rate in Gymnotiformes is well characterized generally (Dye and Meyer, 1986; Metzner, 1999; Caputi et al, 2005) and consists of an unpaired medullary pacemaker nucleus (PN) containing two cell types: pacemaker (P) and relay cells (R). Apteronotid species also have a third PN cell type, but this has not been found in other gymnotiforms (Quintana et al, 2011). P-cells are smaller (50–100 μm) and have an intrinsically rhythmic activity (Bennett, 1968).…”

“…It is well known that P cells are electronically coupled via gap junctions, but relay cells are often also inter-connected with gap junctions, albeit with large and mostly unexplored species differences (Bennett et al, 1967). A more recent anatomical study (Quintana et al, 2011) of B. gauderio also suggested that there may be multiple populations of relay cells, allowing for network specializations that increase the diversity of outputs (rate changes). Relay cell differentiation might also be important for the coordination of electrocyte sub-populations in patterned activation patterns (e.g., Caputi, 1999).…”

“…Amplitude reduction of EODs may occur from a breakdown in synchrony between R cells. An important topic for future study is the question of R cell subpopulations and possible intra-PN mechanisms of regulating EOD amplitude during chirps (see Quintana et al, 2011). These mechanisms may lead to motivational coding in chirp expression, i.e., greater AMPA activation is specifically correlated to R cell desynchronization.…”