12 Active Electroreception and Electrocommunication

Vielka L. Salazar

CONTENTS

12.1 Introduction to Electroreception and Electrogenesis

12.2 Classification of Electric Fishes Based on Electric Signal Type

12.3 Electrocommunication

12.4 Generalized Anatomy of the Electro-Sensory-Motor Pathways in Gymnotiform Weakly Electric Fishes

12.5 Structural Organization and Premotor Neural Regulation of the Pacemaker Nucleus

12.6 Endocrine Regulation and Neuromodulation of the Premotor and Motor Brain Centers

12.7 Endocrine Regulation of the Peripheral Electric Organ

12.8 Conclusion

Acknowledgements

References

12.1 Introduction to Electroreception and Electrogenesis

Electroreception, an ancestral vertebrate trait, refers to the ability of an organism to sense electrical stimuli from its environment. Electroreceptive organisms can detect electrical stimuli passively or actively. In fishes, passive electroreception is more common and involves using ampullary electroreceptors (with the exception of the marine uranoscopid stargazers) to detect weak, low-frequency electric sources (Moller, 1995). The usual electric sources in the surrounding environment are bioelectric outputs from surrounding living organisms, such as muscle contraction during swimming and feeding. Passive electroreception was lost in the ancestor of all teleost fishes but independently re-evolved in the ancestor of the lineages Notopteridae and Mormyroidea and in the ancestor to the lineage Siluriphysi (which includes the orders Siluriformes and Gymnotiformes) (Crampton, 2019).

Active electroreception is less common; it involves organisms emitting an electric field that interacts with the surrounding environment and then detecting the distortions that the environment causes to this electric field (Lissmann, 1951) (Figure 12.1). To achieve this, active electroreceptive fishes activate an electric organ (EO) that discharges the electric field (electrogenesis) and use specialized tuberous electroreceptors to detect this electric field (Heiligenberg and Bastian, 1984). Subtraction of their own field composition from the distorted field allows these electric fishes to produce an electric image of their surroundings (Lissmann and Machin, 1958) (Figure 12.1). In teleost fishes, active electroreception and electrogenesis evolved independently in two freshwater fish groups: one Osteoglossiformes clade, the African superfamily Mormyroidea (known as mormyroids), which includes the families Mormyridae (elephant nose fish) and Gymnarchidae, and one Ostariophysi clade, the Neotropical order Gymnotiformes (known as gymnotiforms or knifefish) (Crampton, 2019).

FIGURE 12.1 Snapshot representation of the electric field of a weakly electric fish. (a) The electric organ (EO) (horizontal black line within the fish’s silhouette) generates an electric signal due to the separation of positive (+) and negative charges (−) along the fish’s body (lines of current flow). The fish can emit a continuous, non-propagating electric field (equipotential lines) for several centimeters away from its body and use this electric field to navigate its environment or locate objects in the dark. (b) A close-up showing how the conductive properties of objects distort the fish’s own electric signal differently. The current lines are attracted and concentrated by a conductive object (gray circle) and are repelled by a nonconductive object (black circle). These electrical differences can be detected by the tuberous electroreceptors in the skin surface closest to the object.
(Based on Lissmann, H.W., J. Exp. Biol., 35, 156–191, 1958; Lissmann, H.W. and Machin, K.E., J. Exp. Biol., 35, 451–486, 1958.)

12.2 Classification of Electric Fishes Based on Electric Signal Type

Electric fishes can be subdivided on the basis of voltage output (field strength) into strongly and weakly electric fishes (Moller, 1995). Strongly electric fishes can generate episodic bouts of high-voltage electric signals up to 860 V and include some marine torpediniform electric rays, marine uranoscopid stargazers, the African freshwater malapterurid electric catfishes, and three species of freshwater gymnotiform electric eels in the genus Electrophorus (Moller, 1995; Crampton, 2019; de Santana et al., 2019). These fishes use their large voltage discharges mainly to hunt prey and protect themselves (Moller, 1995). Weakly electric fishes produce low-voltage (lower than 10 V), continuous electric organ discharges (EODs) that project the electric field for several centimeters around the fish’s body (Bullock, 1982) (Figure 12.1). Although skates, stingrays, electric rays, and some catfishes generate weak electric signals, only gymnotiforms and mormyroids use their weak electric signals for active electroreception. Since many of these weakly electric fishes are nocturnal or live in murky waters, active electroreception is believed to be advantageous by acting to complement or even replace the visual system (Carr, 1990). With the exception of the gymnotiform electric eels (Electrophorus), all gymnotiforms and mormyroids generate only weak electric signals. The gymnotiform genus Electrophorus is the only active electroreceptive clade that produces both strong and weak electric signals due to the segregation of function of its three EOs (Figure 12.2). Electric eels activate the main organ and the anterior portion of the Hunter’s organ to produce strong electric signals, while activation of the Sach’s organ and the posterior portion of the Hunter’s organ generates weak electric signals (de Santana et al., 2019) (Figure 12.2).

FIGURE 12.2 Summary of the most recent proposed phylogenetic relationships for the order Gymnotiformes, also showing the outgroup Siluriformes (catfishes). The gymnotiform fish clade is composed of five families: Apteronotidae, Sternopygidae, Gymnotidae, Hypopomidae, and Rhamphichthyidae. The family Apteronotidae is the only one with a neural-derived (neurogenic) electric organ (EO). The pulse-type EOD seems to be a derived trait, with all pulse-type species forming a monophyletic group. This phylogenetic tree includes a sketch of at least one representative member of each family (black horizontal lines within fish silhouettes show the position of the EOs; all three EOs for Electrophorus electricus are labeled) and the characteristic EOD of each species shown (amplitudes are not to scale). Also, the different electrical outputs are shown (s = strong and w = weak) for each family.
(Based on Moller, P., Electric Fishes: History and Behavior, Chapman & Hall, London, 1995; Betancur-R, R., et al., BMC Evol. Biol., 17,162, 2017; Crampton, W.G.R., Neuroscience, 140, 491–504, 2019.)

Gymnotiforms and mormyroids display one of two types of weak electric signal patterns: a wave-type EOD or a pulse-type EOD (see Figures 12.2 and 12.3 for gymnotiform examples). Each EOD pattern is taxon specific and represents a different strategy for characterizing the fish’s electrical environment (Carr, 1990). The majority of mormyroids, the only exception being the family Gymnarchidae, produce wave-type EODs. Gymnotiforms constitute a clade of five families (Figure 12.2): Apteronotidae, Gymnotidae, Hypopomidae, Rhamphichthyidae, and Sternopygidae (Betancur-R et al., 2017). The families Apteronotidae and Sternopygidae produce wave-type EODs, while the families Gymnotidae, Hypopomidae and Rhamphichthyidae produce pulse-type EODs (Figure 12.2).

FIGURE 12.3 Differences between wave-type and pulse-type gymnotiform weakly electric fishes. (a) The wave-type gymnotiform species Apteronotus leptorhynchus produces a regular, quasi-sine wave EOD at high frequencies. (b) The pulse-type gymnotiform species Brachyhypopomus gauderio produces a continuous train of biphasic EOD pulses. Consecutive EOD pulses are separated by a period of silence, known as the interpulse interval (IPI). B. gauderio breeding males display a pronounced EOD circadian rhythm; at night, males increase the EOD repetition rate and the amplitude and duration of the EOD waveform. (c) Under breeding conditions, the EOD biphasic (P1, first [positive] phase and P2, second [negative] phase) waveform and the EOD circadian rhythmicity of B. gauderio are sexually dimorphic.
(Modified from Salazar, V.L. and Stoddard, P.K., J. Exp. Biol., 211, 1012–1020, 2008; Salazar, V.L., et al., J. Exp. Biol., 216, 2459–2468, 2013.)

Wave-type EODs may be an ancestral trait for gymnotiforms and mormyroids, while pulse-type EODs may represent a derived strategy within these clades (Betancur-R et al., 2017; Crampton, 2019) (Figure 12.2). In gymnotiforms, wave-type fishes discharge their EODs in an extremely regular rhythmic pattern (EOD frequency) with a relatively simple sinusoidal waveform when compared to the signals of pulse-type fishes (Moortgat et al., 1998) (Figures 12.2 and 12.3a, b). Pulse-type fishes discharge brief pulse EOD waveforms separated by electrically silent periods known as interpulse intervals (IPIs) (Figures 12.2 and 12.3). This configuration allows pulse-type fishes to generate more plastic and dynamic EODs, whereby EOD repetition rate (=1/IPI) can be altered independently of the duration of the pulse waveform (Hopkins and Bass, 1981) (Figure 12.3b). In addition, pulse-type electric signal complexity is further enhanced in those species that generate EOD waveforms with two or more phases by encoding different pieces of information in each phase. For instance, in the family Hypopomidae, the first phase (P1) of the EOD pulse waveform is believed to be species specific, while the second phase (P2), the sexually dimorphic phase (Figure 12.3b, c), is specific to each individual (Hagedorn and Carr, 1985; Zakon et al., 1991). Therefore, pulse-type EODs appear to encode more information than wave-type EODs (Hopkins, 1974b).

In this chapter, I will briefly describe the repertoire of electrocommunication behaviors and the generalized anatomy and connections of the electro-sensory-motor system of weakly electric gymnotiforms. Then, I will describe in more detail our current knowledge of how connectivity and neuro-endocrine modulation at different levels of the electromotor pathway account for the diversity in electrical behaviors observed in gymnotiforms, with a focus on the best-documented representative genera: Apteronotus, Brachyhypopomus, Eigenmannia, Gymnotus, and Sternopygus.

12.3 Electrocommunication

One of the most fascinating events in the evolutionary history of fishes is that the re-emergence of electroreception in gymnotiforms and mormyroids was accompanied by the additional ability to electrocommunicate among conspecifics by encoding social information (such as sex and dominance status) within the EODs (Lissmann, 1958; Westby, 1988; McGregor and Westby, 1992). In gymnotiforms, sexual dimorphism has been observed in the EOD waveform in the pulse-type family Hypopomidae, while sexually dimorphic EOD frequencies have been documented in the wave-type families Sternopygidae and Apteronotidae (Hagedorn and Heiligenberg, 1985; Stoddard et al., 2007). For instance, during the breeding season, Brachyhypopomus gauderio (formerly Hypopomus or Brachyhypopomus pinnicaudatus) mature males produce an EOD waveform with longer duration and higher amplitude than females; these males further enhance this sexual dimorphism during the nighttime hours of courtship, following a circadian rhythm (Stoddard et al., 2007) (see Figure 12.3b, c). In wave-type species with sexually dimorphic EOD frequencies, it is more common for males to display lower EOD frequencies when compared with females, as seen in Sternopygus macrurus, Eigenmannia virescens, and Apteronotus albifrons (Hopkins, 1974a, 1974b; Zakon and Smith, 2002). Yet, Apteronotus leptorhynchus displays the opposite pattern, with males having higher EOD frequencies than females (Dunlap et al., 1998).

Superimposed on these sexually dimorphic EOD traits are sex differences in EOD frequency changes (EOD modulations) observed during courtship and aggressive interactions. In the context of these social interactions, gymnotiforms exhibit a wide behavioral repertoire of EOD modulations, including gradual EOD frequency increases (accelerations) and decreases (decelerations), rapid and brief EOD frequency increases with a change in the EOD waveform (chirps), and periods of EOD silences (interruptions) (Hagedorn and Heiligenberg, 1985; Hagedorn, 1986). These EOD modulations have been characterized in more detail in A. leptorhynchus and B. gauderio. For instance, during male–female and male–male dyadic interactions, A. leptorhynchus displays two types of chirps (types 1 and 2; although six different types have been categorized), gradual accelerations, and “abrupt frequency rises” or AFRs (Zupanc, 2002; Tallarovic and Zakon, 2005; Hupe and Lewis, 2008). Males chirp more than females, and their dominance status correlates with chirping output (Hagedorn and Heiligenberg, 1985; Zakon and Smith, 2002). In B. gauderio, Perrone and her colleagues (2009) performed an in-depth characterization of EOD modulations across differences in sex and behavioral contexts. During courtship, males produced mostly accelerations and three different types of chirps (A, B, and C), and females generated interruptions (Perrone et al., 2009). In aggressive interactions, males produced a different chirp (type M), and submissive males generated interruptions (Perrone et al., 2009). In addition, during social interactions, gymnotiforms are susceptible to signal jamming from nearby conspecifics emitting EODs at similar frequencies. To avoid this, many gymnotiforms perform the jamming avoidance response (JAR), whereby they shift their EOD frequency away from the jamming source (Heiligenberg et al., 1996). The JAR differs across species; S. macrurus does not have the JAR, E. virescens can shift its frequency up or down during a JAR, while A. leptorhynchus can only shift its frequency up during the JAR (Heiligenberg et al., 1996). Interestingly, during aggressive interactions, A. leptorhynchus males with low EOD frequency will increase it to be within the ‘jamming range’ of a male opponent with a higher EOD frequency (Tallarovic and Zakon, 2005). A similar behavior has been observed in Hypopomus artedi during aggressive interactions, where males display EOD ‘discharge synchrony,’ potentially jamming each other (Westby, 1975).

12.4 Generalized Anatomy of the Electro-Sensory-Motor Pathways in Gymnotiform Weakly Electric Fishes

The evolution of any communication system requires co-adaptation between a sensory pathway that analyzes the environmental cues and a motor pathway that controls different behavioral responses. Gymnotiform weakly electric fishes perceive electric stimuli via their ampullary and tuberous electroreceptors. Their tuberous electroreceptors are tuned to their own electric signal and as such, perceive any distortions to the fish’s own electric signal. Information from the electroreceptors is conveyed to the electrosensory lateral line lobe (ELL) (Krahe and Maler, 2014) (Figure 12.4). The ELL conveys electrosensory information mainly to the torus semicircularis (TS), which then passes it on to the nucleus electrosensorius (nE) (Heiligenberg and Bastian, 1984) (Figure 12.4). The nE is a sensory-motor integration center, a transition place where sensory information is translated into motor commands and conveyed to the EOD motor network (Heiligenberg et al., 1991).

FIGURE 12.4 Sagittal view of the brain of a gymnotiform fish showing the generalized electro-sensory-motor pathway. In brief, electroreceptors detect electrical stimuli and convey this information via their afferents to the electrosensory lateral line lobe (ELL). The ELL sends projections via two main pathways, one to a major processing center, the torus semicircularis (TS), and the other to an electrosensory feedback loop made up of the nucleus praeminentialis (nP) and the eminentia granularis posterior (EGp). The TS sends projections to the optic tectum (TeO) and the nucleus electrosensorius (nE), a sensory-motor interface. The nE sends projections to two premotor areas, the central posterior/prepacemaker nucleus complex (CP/PPn) and the sublemniscal prepacemaker nucleus (SPPn). These two premotor areas control the intrinsic activity of the motor command center, the pacemaker nucleus (Pn). The Pn sends axons to innervate the spinal cord’s electromotoneurons (EMNs). The EMNs form or innervate the peripheral electric organ (EO).
(Based on Heiligenberg, W., Neural Nets in Electric Fish, MIT Press, Cambridge, MA, 1991; Zupanc, G.K. and Maler, L., J. Comp. Physiol. A, 180, 99–111, 1997.)

Gymnotiform weakly electric fishes have an EOD motor network composed of a chain of hierarchically arranged nuclei located at the diencephalic, midbrain, and medullary levels (Heiligenberg et al., 1981; Zupanc and Maler, 1993; Juranek and Metzner, 1997; Zupanc and Maler, 1997) (Figures 12.4 and 12.5). The premotor areas, collectively called the diencephalic central posterior/prepacemaker nucleus (CP/PPn) and the midbrain sublemniscal prepacemaker nucleus (SPPn), send direct input to the medullary pacemaker nucleus (Pn), the EOD control center (Juranek and Metzner, 1998) (Figures 12.4 and 12.5). The Pn directs the activity of the spinal electromotoneurons (EMNs). Subsequently, spinal EMNs innervate, via cholinergic (ACh-R) synapses, the electrocytes that compose the peripheral EO (Bennett, 1971). Electrocytes within the EO fire synchronously to produce the EOD (Bennett et al., 1967). Each action potential of the electrocytes corresponds to an individual EOD event on a one-to-one basis (Mills and Zakon, 1991). In gymnotiforms, the contributions of the central and peripheral motor components to the communication signal can be compartmentalized: EOD frequency or repetition rate is controlled by the medullary Pn, while the EOD waveform’s duration and amplitude are determined by the ionic conductances of the electrocytes (Zakon, 1998).

FIGURE 12.5 Diagram of the synaptic connections between the premotor areas (PPn and SPPn) and the electromotor command center (Pn) for a representative gymnotiform family, Hypopomidae. The different PPn and SPPn projections to the pacemaker neurons (P) and relay neurons (R) are shown, indicating the type of synaptic connection (e.g., AMPA-R, NMDA-R, and GABA-R). R axons project to the spinal cord’s EMNs, which innervate the electrocytes in the electric organ (EO) via cholinergic (ACh-R) synapses.
(Based on Kawasaki, M. and Heiligenberg, W., J. Neurosci., 10, 3896–3904, 1990; Kennedy, G. and Heiligenberg, W., J. Comp. Physiol. A, 174, 267–280, 1994; Quintana, L., et al., J. Comp. Physiol. A, 197, 75–88, 2011.)

12.5 Structural Organization and Premotor Neural Regulation of the Pacemaker Nucleus

In all gymnotiform weakly electric fishes, the EOD is controlled by the Pn, an unpaired midline nucleus in the brainstem (Bennett et al., 1967; Kawasaki and Heiligenberg, 1989, 1990). The Pn is composed of two electrically coupled cell groups, the pacemaker neurons and relay neurons (Bennett et al., 1967; Ellis and Szabo, 1980). The pacemaker neurons fire synchronously and locally excite the relay neurons (Kennedy and Heiligenberg, 1994) (Figure 12.5). The intrinsic bursting activity of pacemaker neurons drives the rhythm of the EOD frequency or repetition rate, while the electrotonic connections between pacemaker and relay neurons contribute to the regularity of the output (Bennett et al., 1967; Moortgat et al., 2000). The relay neurons innervate the spinal EMNs in all gymnotiforms; EMNs innervate a muscle-derived (myogenic) EO or, as observed only in Apteronotidae, have their axons end in specialized processes, which constitute the neural-derived (neurogenic) EO (Bennett et al., 1967; Bennett, 1971; Pappas et al., 1975; Elekes and Szabo, 1981). A third population of Pn neurons, the parvocell interneurons, has been identified in A. leptorhynchus (Smith et al., 2000). Parvocells are connected to pacemaker and relay neurons via chemical and electrical synapses, yet their function remains unclear (Smith et al., 2000).

The association, synapse type, degree of electrotonic coupling, relative size and organization, and ratio between pacemaker and relay neurons vary among gymnotiform genera (Tables 12.1 and 12.2). These differences correlate with the repertoire of electric signal modulations displayed during social interactions. For instance, the pulse-type gymnotiform fish B. gauderio, which arguably produces a more complex repertoire of electric signal modulations, has the pacemaker and relay neurons densely packed in a 1:1 ratio in the Pn and arranged in two distinct populations (Quintana et al., 2011) (Figure 12.5 and Table 12.1). The pacemaker and relay neurons are not only dorso-ventrally segregated but also rostro-caudally segregated, a pattern so far only documented in this genus (Quintana et al., 2011) (Figure 12.5). In addition, the relay neurons can be categorized into three size classes, displaying size class dorso-ventral segregation (larger cells more dorsal and smaller cells more ventral) (Quintana et al., 2011). Quintana and her colleagues (2011) proposed that differential activation of different size classes of relay neurons and uncoupling of pacemaker and relay neurons can account for the diversity of electric social signals (such as chirps) in B. gauderio.

TABLE 12.1
Main Anatomical Characteristics of the Pacemaker Nucleus (Pn) of Five Gymnotiform Genera

Images

TABLE 12.2
Modulation of Premotor Areas to the Pacemaker Nucleus by Differential Synaptic Connectivity

Images

The activity of the Pn is modulated by three distinct diencephalic CP/PPn subpopulations, consisting of the PPnG, the PPnC, and the PPnI, and one midbrain premotor area, the SPPn (Heiligenberg et al., 1981; Kawasaki and Heiligenberg, 1989, 1990; Keller et al., 1991; Kennedy and Heiligenberg, 1994) (Figures 12.4 and 12.5). Different premotor areas send differential neurotransmitter signals to the Pn, which modify the electrical properties of the pacemaker and relay neurons and produce a diversity of electrical behaviors (Heiligenberg, 1994; Kennedy and Heiligenberg, 1994; Juranek and Metzner, 1998) (Figure 12.5 and Tables 12.2 and 12.3). For instance, experimental stimulation by current injection to different CP/PPn subpopulations and SPPn yields temporal patterns in the EOD rhythm similar to the fish’s natural behaviors (Kawasaki and Heiligenberg, 1989).

TABLE 12.3
EOD Frequency or Repetition Rate Modulations Observed as a Result of Direct Input of the Different Premotor Areas to the Pn

Images

In all gymnotiforms studied to date, the PPnG sends axons to the pacemaker neurons, but not the relay neurons, and excites them via glutamatergic synapses involving NMDA receptors (NMDA-R), AMPA receptors (AMPA-R), or both (Dye and Heiligenberg, 1987; Dye et al., 1989; Kennedy and Heiligenberg, 1994) (Figure 12.5 and Table 12.2). The PPnG has the common function of generating gradual accelerations (i.e. EOD frequency or repetition rate increases) (Dye and Heiligenberg, 1987; Kawasaki et al., 1988). In the wave-type genus Eigenmannia, gradual accelerations via PPnG activation of pacemaker neurons are complemented by gradual decelerations resulting from disruption of the SPPn tonic input to relay neurons via NMDA-Rs (Heiligenberg et al., 1996). The combined effect of these connections allows Eigenmannia to have a more dynamic control of its EOD frequency. Brachyhypopomus implements a different strategy to generate gradual accelerations and decelerations. In common with all other gymnotiforms, PPnG controls the gradual accelerations, but a CP/PPn subpopulation only documented in this species, PPnI, controls the gradual decelerations (Kawasaki and Heiligenberg, 1989) (Figure 12.5 and Tables 12.2 and 12.3). The PPnI sends axons to the pacemaker neurons and inhibits them via activation of GABA receptors (GABA-R) (Kawasaki and Heiligenberg, 1990) (Figure 12.5). It remains unclear why the PPnI is not present in other gymnotiform species. These gradual accelerations and decelerations are used in courtship and aggressive interactions and to execute the JAR (Juranek and Metzner, 1997; Zakon et al., 2002; Perrone et al., 2009). Interestingly, the SPPn–relay connection plays a different role in other gymnotiform genera. In the wave-type genus Apteronotus, which displays co-expression of NMDA-R and AMPA-R receptors at this synaptic connection, SPPn is not tonically active, and its excitatory input on the relay neurons generates gradual accelerations (Heiligenberg et al., 1996; Juranek and Metzner, 1997). As such, Apteronotus can only shift up when performing a JAR (Heiligenberg et al., 1996). In the wave-type genera Eigenmannia and Sternopygus and the pulse-type genus Brachyhypopomus, SPPn input to relay neurons via NMDA-R causes interruptions, temporarily silencing the EOD (Keller et al., 1991; Heiligenberg, 1994).

The PPnC seems to be the “chirp” control in all the genera displaying this behavior. It innervates dendrites of the relay neurons and excites them via AMPA-R, producing chirps (rapid, short accelerations with a decrease in EOD waveform) (Dye and Heiligenberg, 1987; Kawasaki et al., 1988; Dye et al., 1989; Heiligenberg, 1994) (Figure 12.5 and Tables 12.2 and 12.3). Connectivity of the Pn and modulation of the Pn by the PPnC seem to play a role in explaining the diversity of chirps (e.g. courtship chirps versus agonistic chirps) observed in gymnotiforms (Zupanc and Maler, 1993). PPnC input to relay neurons can desynchronize the Pn network as well as briefly increase the firing rate of relay cells (Kawasaki and Heiligenberg, 1989). As such, in species where the Pn is more compact, and the pacemaker and relay connections are heterogeneous, this PPnC-driven desynchronization can increase the diversity of chirps produced across species (Lucas et al., 2019). In B. gauderio, a different model has been proposed, whereby differential PPnC stimulation (i.e. brief, low strength versus long, high strength) recruits different size class populations of relay neurons, resulting in the production of different chirp types (Quintana et al., 2011). Another premotor input to the Pn, the medullary Mauthner cells (M-cells), has been identified in the pulse-type genus Gymnotus (Trujillo-Cenoz and Bertolotto, 1990). M-cells send connections to the pacemaker neurons, but not to the relay neurons, and their input is excitatory via NMDA-R and metabotropic glutamatergic synapses (Curti et al., 2006). M-cell activation generates a “Mauthner-initiated abrupt increase rate” or M-AIR (Falconi et al., 1995). Unlike the pattern observed in chirps, the M-AIR consists of a rapid, longer-lasting, and smaller increase in the EOD rate without a change in the EOD waveform, and as such, it is believed to improve sampling of electrical information in moving fishes (Falconi et al., 1995). This connection has not been found in any other gymnotiform genera.

12.6 Endocrine Regulation and Neuromodulation of the Premotor and Motor Brain Centers

As discussed in the previous section, the effects of the premotor inputs on the pacemaker and relay neurons vary among species (Table 12.3). Connections between the CP/PPn and brain areas associated with mating behavior and neuroendocrinological control (e.g. ventral telencephalon, hypothalamus, and preoptic nucleus) have been documented (Zupanc, 2002). In addition, the rhythmic output of the Pn can also be altered due to neuromodulation targeting any of the PPn subpopulations or the Pn. In Apteronotus and Eigenmannia, studies using immunohistochemical labeling and brain site-specific injection techniques have shown the presence of many neuromodulators in the CP/PPn, including serotonin, noradrenaline, dopamine, somatostatin, galanin, substance P, met-enkephalin, and corticotropin-releasing hormone (Zupanc, 2002). Interestingly, in A. leptorhynchus, substance P-labeling in fibers innervating the PPnC is sexually dimorphic (females’ fibers have no label), and androgen treatment in females not only masculinized chirping pattern but also masculinized substance P-labeling associated with the PPn (Weld and Maler, 1992; Dulka et al., 1995). In addition, in B. gauderio and G. omarorum, arginine vasotocin (AVT)–positive cells in the preoptic area (POA) send projections nearby to the Pn, and treatment of Pn-containing brain slices with AVT increased the Pn’s firing rate (Perrone et al., 2014; Pouso et al., 2017). In B. gauderio, the number of AVT-positive cells in the anterior POA positively correlated with the number of chirps recorded in social males (Pouso et al., 2019). In A. leptorhynchus, AVT injections in intact fish increased male chirping but had no effect in females, while electrical stimulation of the POA in paralyzed fish produced chirp-like responses (Wong, 2000; Bastian et al., 2001).

Sex-specific and seasonal changes in behavior (e.g. courtship) are typically associated with physiological changes due to hormones and peptides. For instance, in Sternopygus, androgens such as dihydrotestosterone (DHT) decrease the firing frequency of the Pn, masculinizing the EOD frequency, yet androgen receptor (AR) expression was found in the PPn and SPPn but not in the Pn (Zakon, 1996, 1998). In contrast, in B. gauderio, breeding males have a higher expression of ARs in both pacemaker and relay neurons when compared with nonbreeding males (Pouso et al., 2010). When nonbreeding males were treated with testosterone implants, AR expression was upregulated in the Pn (Pouso et al., 2010). AR upregulation could lead to increased expression of glutamate receptors such as NMDA-R and AMPA-R.

12.7 Endocrine Regulation of the Peripheral Electric Organ

EMNs’ organization and sensitivity to steroid effects can contribute to EOD waveform plasticity. For instance, in Gymnotus carapo, two EMN populations have been described: small EMNs, which innervate the rostral portion of the EO and tend to fire first, and large EMNs, which innervate the highest number of electrocytes (caudal region of the EO) and fire last, with a mixture of the two populations prevailing at the intermediate segment of the EO (Caputi and Trujillo-Cenoz, 1994). In addition, steroid hormones can also modulate the electromotor network directly at the level of the EMNs. In spinally transected A. leptorhynchus treated with either the androgen 11-ketotestosterone (11-KT) or estrogen, EMNs display an increase or a decrease (respectively) in their firing rate (Zakon, 1996).

Since, with the exception of Apteronotus, all gymnotiforms have a myogenic EO (Bennett, 1971), this section will focus on the anatomy and physiology of myogenic EOs. Electrocyte architecture constitutes one of the most diversified structures in gymnotiforms (Mills et al., 1992). The anatomical distribution, pattern of innervation, and ionic conductances of the electrocytes determine the shape, the complexity, and the generation of the EOD waveform (Bennett, 1971). For instance, the wave-type monophasic Sternopygus and Eigenmannia have only one excitable membrane (single innervation) in the electrocytes (Bennett, 1971). The pulse-type biphasic Brachyhypopomus has two excitable membranes (single innervation of only one of these membranes) (Bennett, 1971). And in the pulse-type multiphasic G. carapo, its two EMN populations differentially innervate electrocytes depending on their location in the EO; rostral and mid-body electrocytes are innervated on both rostral and caudal sides, while caudal electrocytes are only innervated caudally (Caputi, 1999). The differential distribution of the EMNs (as described earlier) plus their differential innervation of the electrocytes generates a highly complex EOD waveform while maintaining synchronicity of the EOD.

The duration of the EOD waveform is controlled by the kinetics of the electrocytes’ ionic currents (Zakon, 1996). The excitable membranes of the electrocytes are composed of ion channels, which control the inward and outward flow of Na+, K+, Cl−, and other ions (Ferrari and Zakon, 1993; Zakon, 1996). Steroid hormones can target the EO directly to modify the EOD waveform (Heiligenberg and Bastian, 1984). The EO can be described as an androgen-target tissue. This can be readily observed in the hormone-dependent sex differences in the EOD (Mills and Zakon, 1991). In Sternopygus, the effects of androgens in the Pn are independent of the effects of androgens in the electrocytes (Few and Zakon, 2001). Mills and Zakon (1991) showed that androgens affect the EO directly by changing the ionic currents responsible for the action potential generation. DHT broadens the EO’s action potential, which is mainly controlled by the Na+ current (Zakon, 1998).

Sex steroid regulatory effects on electrocytes’ action potential duration could be better assessed by understanding the processes of expression, diversity, and kinetics of the Na+ and K+ channels (Ferrari and Zakon, 1993). In S. macrurus, recordings from electrocytes after treatment with DHT showed a decrease in the Na+ channels’ closed state, and this effect correlated with an increase in the duration of the electrocytes’ action potential (Ferrari et al., 1995). Ferrari and colleagues (1995) offered a few possible ways by which DHT could exert the variation observed: differential expression of Na+ channel α subunit genes or transcripts that generate kinetically distinct Na+ channels, and/or differential expression of Na+ channels’ accessory β subunits. Subsequent studies have provided evidence in support of both these mechanisms. In S. macrurus, two different Na+ channel α subunits have been identified in electrocytes, Nav1.4a and Nav1.4b, as well as an accessory β1 subunit (Zakon et al., 2006; Liu et al., 2007, 2008). In addition, Nav1.4b occurs as two splice variants, short and long transcripts. Androgen treatment decreases the expression of the Nav1.4b long transcript and the β1 subunit, and the expression of these Na+ channel subunits negatively correlates with the duration of the electrocyte’s action potential (i.e. EOD duration) (Liu et al., 2007, 2008).

Finally, beyond these sex differences, hormones can also regulate the electrocyte Na+ current in a shorter timeline to account for the day–night EOD waveform changes that have been observed in some gymnotiforms. For instance, in a series of elegant studies, Markham and his colleagues (2009) showed that Na+ channels can be trafficked in and out of the electrocyte membrane in response to treatment with the melanocortin hormones, α-melanocyte hormone (α-MSH) and adrenocorticotropic hormone (ACTH) (Markham et al., 2009b). Injections of these hormones in intact fish mimicked the timescale and magnitude of the observed day-to-night increase in the EOD waveform (Markham et al., 2009a). Based on electrophysiological recordings and pharmacological manipulations of electrocytes in vitro, the effect of α-MSH and ACTH seems to be mediated by binding to the melanocortin receptor 5, a G-protein coupled receptor, and activation of a cyclic AMP second messenger pathway, resulting in the insertion of Na+ channels in the membrane from a cytoplasmic vesicular pool and an increase in the Na+ current (Markham and Stoddard, 2005; Markham et al., 2009b).

12.8 Conclusion

All the electric behaviors observed in gymnotiform weakly electric fishes (JAR, agonistic and courtship chirps, gradual accelerations and decelerations, interruptions, and daily and seasonal EOD changes) have an unifying underlying neural circuitry, which, depending on the behavioral context, can be modified by the action of a wide range of neural synaptic connections, neuromodulators, and hormones (Zakon, 1996). Neural modulation is observed at the premotor and motor areas of the CNS, and it tends to mediate rapid and brief responses.

The premotor areas (i.e. CP/PPn and SPPn) are the principal neural modulators of the Pn. They briefly and rapidly change the basic firing properties of the same group of neurons (pacemaker and relay neurons) by sending connections with different neurotransmitters. This process increases the repertoire of signals expressed, allowing a fish to produce a complex set of behaviors. The premotor areas and the Pn are sensitive to steroid hormones. Steroid hormones have been shown to exert slower, long-term changes to the electrical properties of the neurons in the premotor areas and the Pn (Zupanc and Heiligenberg, 1989). In the periphery, the electrocytes are major targets of hormonal modulation. Different studies have shown that treatment with steroid hormones affects the kinetics of the ionic channels of the excitable membranes of the electrocytes (Zakon, 1996). These ionic changes in the electrocytes seem to be responsible for sex differences in the EODs (Zakon, 1998). Fast EOD waveform circadian changes are mediated by melanocortins via the activation of second messenger systems and circadian cycling of Na+ channels. Although the basic architecture of the electromotor pathway is fairly well conserved across gymnotiforms, a diversity of electrical behaviors and electric signal plasticity has emerged across the clade as a result of a rich repertoire of neural and endocrine modulatory inputs.

Acknowledgements

Supported by the Natural Sciences and Engineering Research Council of Canada, the Canada Foundation for Innovation, and the Nova Scotia Research and Innovation Trust.

References

  1. Bastian J, Schniederjan S, Nguyenkim J. 2001. Arginine vasotocin modulates a sexually dimorphic communication behavior in the weakly electric fish Apteronotus leptorhynchus. J Exp Biol 204:1909–1923.
  2. Bennett MVL. 1971. Electric organs. In: Hoar WS, Randall DJ, editors. Fish Physiology. London: Academic Press.
  3. Bennett MVL, Pappas GD, Gimenez M, Nakajima Y. 1967. Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish. J Neurophysiol 30:236–300.
  4. Betancur-R R, Wiley EO, Arratia G, Acero A, Bailly N, Miya M, Lecointre G, Orti G. 2017. Phylogenetic classification of bony fishes. BMC Evol Biol 17:162.
  5. Bullock TH. 1982. Electroreception. Ann Rev Neurosci 5:121–170.
  6. Caputi A, Trujillo-Cenoz O. 1994. The spinal cord of Gymnotus carapo: the electromotoneurons and their projection patterns. Brain Behav Evol 44:166–174.
  7. Caputi AA. 1999. The electric organ discharge of pulse gymnotiforms: the transformation of a simple impulse into a complex spatio-temporal electromotor pattern. J Exp Biol 202:1229–1241.
  8. Carr CE. 1990. Neuroethology of electric fish. Bioscience 40:259–267.
  9. Crampton WGR. 2019. Electroreception, electrogenesis and electric signal evolution. J Fish Biol 95:92–134.
  10. Curti S, Comas V, Rivero C, Borde M. 2006. Analysis of behavior-related excitatory inputs to a central pacemaker nucleus in a weakly electric fish. Neuroscience 140:491–504.
  11. de Santana CD, Crampton WGR, Dillman CB, Frederico RG, Sabaj MH, Covain R, Ready J, Zuanon J, de Oliveira RR, Mendes-Júnior RN, Bastos DA, Teixeira TF, Mol J, Ohara W, Castro NCe, Peixoto LA, Nagamachi C, Sousa L, Montag LFA, Ribeiro F Waddell JC Piorsky NM, Vari RP, Wosiacki WB. 2019. Unexpected species diversity in electric eels with a description of the strongest living bioelectricity generator. Nature Comm 10:4000.
  12. Dulka JG, Maler L, Ellis W. 1995. Androgen-induced changes in electrocommunicatory behavior are correlated with changes in substance P-like immunoreactivity in the brain of the electric fish Apteronotus leptorhynchus. J Neurosci 15:1879–1890.
  13. Dunlap KD, Thomas P, Zakon HH. 1998. Diversity of sexual dimorphism in electrocommunication signals and its androgen regulation in a genus of electric fish, Apteronotus. J Comp Physiol A 183:77–86.
  14. Dye J, Heiligenberg W. 1987. Intracellular recording in the medullary pacemaker nucleus of the weakly electric fish, Apteronotus, during modulatory behaviors. J Comp Physiol A 161:187–200.
  15. Dye J, Heiligenberg W, Keller CH, Kawasaki M. 1989. Different classes of glutamate receptors mediate distinct behaviors in a single brainstem nucleus. Proc Natl Acad Sci U S A 86:8993–8997.
  16. Elekes K, Szabo T. 1981. Comparative synaptology of the pacemaker nucleus in the brain of weakly electric fish (Gymnotidae). In: Szabo T, Czeh G, editors. Sensory Physiology of Aquatic Lower Vertebrates. Budapest: Akademiai Kiado. p 107–127.
  17. Ellis DB, Szabo T. 1980. Identification of different cells types in the command (pacemaker) nucleus of several gynotiform species by retrograde transport of horseradish peroxidase. Neuroscience 5:1917–1929.
  18. Falconi A, Borde M, Henandez-Cruz A, Morales FR. 1995. Mauthner cell-initiated abrupt increase of the electric organ discharge in the weakly electric fish Gymnotus carapo. J Comp Physiol A 176:679–689.
  19. Ferrari MB, McAnelly ML, Zakon HH. 1995. Individual variation in and androgen-modulation of the sodium current in electric organ. J Neurosci 15:4023–4032.
  20. Ferrari MB, Zakon HH. 1993. Conductances contributing to the action potential of Sternopygus electrocytes. J Comp Physiol A 173:281–292.
  21. Few WP, Zakon HH. 2001. Androgens alter electric organ discharge pulse duration despite stability in electric organ discharge frequency. Horm Behav 40:434–442.
  22. Hagedorn M. 1986. The ecology, courtship and mating of gymnotiform electric fish. In: Bullock TH, Heiligenberg W, editors. Electroreception. New York: Wiley. p 497–525.
  23. Hagedorn M, Carr C. 1985. Single electrocytes produce a sexually dimorphic signal in South American electric fish, Hypopomus occidentalis (Gymnotiformes, Hypopomidae). J Comp Physiol A 156:511–523.
  24. Hagedorn M, Heiligenberg W. 1985. Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Behav 33:254–265.
  25. Heiligenberg W. 1991. Neural Nets in Electric Fish. Cambridge, MA: MIT Press.
  26. Heiligenberg W. 1994. The detection and generation of electric communication signals in gymnotiform fish. In: Schildberger K, Elsner N, editors. Neural Basis of Behavioural Adaptations. Stuttgart: Gustav Fischer Verlag. p 13–24.
  27. Heiligenberg W, Bastian J. 1984. The electric sense of weakly electric fish. Annu Rev Physiol 46:561–583.
  28. Heiligenberg W, Finger T, Matsubara J, Carr C. 1981. Input to the medullary pacemaker nucleus in the weakly electric fish, Eigenmannia (Sternopygidae, Gymnotiformes). Brain Res 211:418–423.
  29. Heiligenberg W, Keller CH, Metzner W, Kawasaki M. 1991. Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fish Eigenmannia: detection and processing of electric signals in social communication. J Comp Physiol A 169:151–164.
  30. Heiligenberg W, Metzner W, Wong CJH, Keller CH. 1996. Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates. J Comp Physiol A 179:653–674.
  31. Hopkins CD. 1974a. Electric communication in the reproductive behavior of Sternopygus macrurus (Gymnotoidei). Z Tierpsychol 35:518–535.
  32. Hopkins CD. 1974b. Electric communication: functions in the social behavior of Eigenmannia virescens. Behaviour 50:270–305.
  33. Hopkins CD, Bass AH. 1981. Temporal coding of species recognition signals in an electric fish. Science 212:85–87.
  34. Hupe GJ, Lewis JE. 2008. Electrocommunication signals in free swimming brown ghost knifefish, Apteronotus leptorhynchus. J Exp Biol 211:1657–1667.
  35. Juranek J, Metzner W. 1997. Cellular characterization of synaptic modulations of a neuronal oscillator in electric fish. J Comp Physiol A 181:393–414.
  36. Juranek J, Metzner W. 1998. Segregation of behavior-specific synaptic inputs to a vertebrate neuronal oscillator. J Neurosci 18:9010–9019.
  37. Kawasaki M, Heiligenberg W. 1989. Distinct mechanisms of modulation in a neuronal oscillator generate different social signals in the electric fish Hypopomus. J Comp Physiol A 165:731–741.
  38. Kawasaki M, Heiligenberg W. 1990. Different classes of glutamate receptors and GABA mediate distinct modulations of a neuronal oscillator, the medullary pacemaker of a gymnotiform electric fish. J Neurosci 10:3896–3904.
  39. Kawasaki M, Maler L, Rose GJ, Heiligenberg W. 1988. Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus. J Comp Neurol 276:113–131.
  40. Keller CH, Kawasaki M, Heiligenberg W. 1991. The control of pacemaker modulations for social communication in the weakly electric fish Sternopygus. J Comp Physiol A 169:441–450.
  41. Kennedy G, Heiligenberg W. 1994. Ultrastructural evidence of GABA-ergic inhibition and glutamatergic excitation in the pacemaker nucleus of the gymnotiform electric fish, Hypopomus. J Comp Physiol A 174:267–280.
  42. Krahe R, Maler L. 2014. Neural maps in the electrosensory system of weakly electric fish. Curr Opin Neurobiol 24:13–21.
  43. Lissmann HW. 1951. Continuous electrical signals from the tail of a fish. Gymnarchus niloticus Cuv. Nature 167:201–202.
  44. Lissmann HW. 1958. On the function and evolution of electric organs in fish. J Exp Biol 35:156–191.
  45. Lissmann HW, Machin KE. 1958. The mechanisms of object location in Gymnarchus niloticus and similar fish. J Exp Biol 35:451–486.
  46. Liu H, Wu MM, Zakon HH. 2007. Individual variation and hormonal modulation of a sodium channel beta subunit in the electric organ correlate with variation in a social signal. Dev Neurobiol 67:1289–1304.
  47. Liu H, Wu MM, Zakon HH. 2008. A novel Na+ channel splice form contributes to the regulation of an androgen-dependent social signal. J Neurosci 28:9173–9182.
  48. Lucas KM, Warrington J, Lewis TJ, Lewis JE. 2019. Neuronal dynamics underlying communication signals in a weakly electric fish: implications for connectivity in a pacemaker network. Neuroscience 401:21–34.
  49. Markham MR, Allee SJ, Goldina A, Stoddard PK. 2009a. Melanocortins regulate the electric waveforms of gymnotiform electric fish. Horm Behav 55:306–313.
  50. Markham MR, McAnelly ML, Stoddard PK, Zakon HH. 2009b. Circadian and social cues regulate ion channel trafficking. PLoS Biol 7:e1000203.
  51. Markham MR, Stoddard PK. 2005. Adrenocorticotropic hormone enhances the masculinity of an electric communication signal by modulating the waveform and timing of action potentials within individual cells. J Neurosci 25:8746–8754.
  52. McGregor PK, Westby GWM. 1992. Discrimination of individually characteristic electric organ discharges by a weakly electric fish. Anim Behav 43:977–986.
  53. Mills A, Zakon HH. 1991. Chronic androgen treatment increases action potential duration in the electric organ of Sternopygus. J Neurosci 11:2349–2361.
  54. Mills A, Zakon HH, Marchaterre MA, Bass AH. 1992. Electric organ morphology of Sternopygus macrurus, a wave-type, weakly electric fish with a sexually dimorphic EOD. J Neurobiol 23:920–932.
  55. Moller P. 1995. Electric FIshes: History and Behavior. London: Chapman & Hall.
  56. Moortgat KT, Bullock TH, Sejnowski TJ. 2000. Precision of the pacemaker nucleus in a weakly electric fish: network versus cellular influences. J Neurophysiol 83:971–983.
  57. Moortgat KT, Keller CH, Bullock TH, Sejnowski TJ. 1998. Submicrosecond pacemaker precision is behaviorally modulated: the gymnotiform electromotor pathway. Proc Natl Acad Sci U S A 95:4684–4689.
  58. Pappas GD, Waxman SG, Bennett MV. 1975. Morphology of spinal electromotor neurons and presynaptic coupling in the gymnotid Sternarchus albifrons. J Neurocytol 4:469–478.
  59. Perrone R, Macadar O, Silva A. 2009. Social electric signals in freely moving dyads of Brachyhypopomus pinnicaudatus. J Comp Physiol A 195:501–514.
  60. Perrone R, Migliaro A, Comas V, Quintana L, Borde M, Silva A. 2014. Local vasotocin modulation of the pacemaker nucleus resembles distinct electric behaviors in two species of weakly electric fish. J Physiol Paris 108:203–212.
  61. Pouso P, Cabana A, Goodson JL, Silva A. 2019. Preoptic area activation and vasotocin involvement in the reproductive behavior of a weakly pulse-type electric fish, Brachyhypopomus gauderio. Front Integr Neurosci 13:37.
  62. Pouso P, Quintana L, Bolatto C, Silva AC. 2010. Brain androgen receptor expression correlates with seasonal changes in the behavior of a weakly electric fish, Brachyhypopomus gauderio. Horm Behav 58:729–736.
  63. Pouso P, Radmilovich M, Silva A. 2017. An immunohistochemical study on the distribution of vasotocin neurons in the brain of two weakly electric fish, Gymnotus omarorum and Brachyhypopomus gauderio. Tissue Cell 49:257–269.
  64. Quintana L, Pouso P, Fabbiani G, Macadar O. 2011. A central pacemaker that underlies the production of seasonal and sexually dimorphic social signals: anatomical and electrophysiological aspects. J Comp Physiol A 197:75–88.
  65. Salazar VL, Krahe R, Lewis JE. 2013. The energetics of electric organ discharge generation in gymnotiform weakly electric fish. J Exp Biol 216:2459–2468.
  66. Salazar VL, Stoddard PK. 2008. Sex differences in energetic costs explain sexual dimorphism in the circadian rhythm modulation of the electrocommunication signal of the gymnotiform fish Brachyhypopomus pinnicaudatus. J Exp Biol 211:1012–1020.
  67. Smith GT, Lu Y, Zakon HH. 2000. Parvocells: a novel interneuron type in the pacemaker nucleus of a weakly electric fish. J Comp Neurol 423:427–439.
  68. Stoddard PK, Markham MR, Salazar VL, Allee S. 2007. Circadian rhythms in electric waveform structure and rate in the electric fish Brachyhypopomus pinnicaudatus. Physiol Behav 90:11–20.
  69. Tallarovic S, Zakon HH. 2005. Electric organ discharge frequency jamming during social interactions in brown ghost knifefish, Apteronotus leptorhynchus. Anim Behav 70:1355–1365.
  70. Trujillo-Cenoz O, Bertolotto C. 1990. Mauthner cells in the medulla of the weakly electric fish Gymnotus carapo. Experentia 46:441–443.
  71. Weld MM, Maler L. 1992. Substance P-like immunoreactivity in the brain of the gymnotiform fish Apteronotus leptorhynchus: presence of sex differences. J Chem Neuroanat 5:107–129.
  72. Westby GWM. 1975. Comparative studies of the aggressive behaviour of two gymnotoid electric fish (Gymnotus carapo and Hypopomus artedi). Anim Behav 23:192–213.
  73. Westby GWM. 1988. The ecology, discharge diversity and predatory behaviour of gymnotiform electric fish in the coastal streams of French Guiana. Behav Ecol Sociobiol 22:341–354.
  74. Wong CJ. 2000. Electrical stimulation of the preoptic area in Eigenmannia: evoked interruptions in the electric organ discharge. J Comp Physiol A 186:81–93.
  75. Zakon H, Oestreich J, Tallarovic S, Triefenbach F. 2002. EOD modulations of brown ghost electric fish: JARs, chirps, rises and dips. J Physiol (Paris) 96:451–458.
  76. Zakon H, Smith GT. 2002. Weakly electric fish: behavior, neurobiology and neuroendocrinology. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbath SE, Rubin RT, editors. Hormones, Brain and Behavior. Amsterdam: Elsevier. p 611–638.
  77. Zakon HH. 1996. Hormonal modulation of communication signals in electric fish. Dev Neurosci 18:115–123.
  78. Zakon HH. 1998. The effects of steroid hormones on electrical activity of excitable cells. Trends Neurosci 21:202–207.
  79. Zakon HH, Lu Y, Zwickl DJ, Hillis DM. 2006. Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc Natl Acad Sci U S A 103:3675–3680.
  80. Zakon HH, Thomas P, Yan HY. 1991. Electric organ discharge frequency and plasma sex steroid levels during gonadal recrudescence in a natural population of the weakly electric fish Sternopygus macrurus. J Comp Physiol [A] 169:493–499.
  81. Zupanc GK, Heiligenberg W. 1989. Sexual maturity-dependent changes in neuronal morphology in the prepacemaker nucleus of adult weakly electric knifefish, Eigenmannia. J Neurosci 9:3816–3827.
  82. Zupanc GK, Maler L. 1993. Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis. Can J Zool 71:2301–2310.
  83. Zupanc GK, Maler L. 1997. Neuronal control of behavioral plasticity: the prepacemaker nucleus of weakly electric gymnotiform fish. J Comp Physiol A 180:99–111.
  84. Zupanc GKH. 2002. From oscillator to modulators: behavioral and neural control of modulations of the electric organ discharge in the gymnotiform fish, Apteronotus leptorhynchus. J Physiol (Paris) 96:459–472.