Plasticity of electroreceptor tuning in the weakly electric fish,Sternopygus dariensis

Zakon, Harold H.; Jh, Meyer

doi:10.1007/bf00612602

Cited by 49 publications

(57 citation statements)

References 28 publications

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“…As noted previously (Sisneros and Bass, 2003), a similar mechanism for steroid-dependent frequency sensitivity has been proposed for electroreceptors in weakly electric fish (Zakon and Meyer, 1983). One of the primary determinants of electrical resonant frequencies of vertebrate auditory hair cells is the expression of large conductance, calcium-activated potassium (BK) channels (Fettiplace and Fuchs, 1999).…”

Section: Mechanisms For Saccular Hair Cell Plasticitymentioning

confidence: 58%

Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish

Rohmann

Bass

2011

Journal of Experimental Biology

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SUMMARYVertebrates displaying seasonal shifts in reproductive behavior provide the opportunity to investigate bidirectional plasticity in sensory function. The midshipman teleost fish exhibits steroid-dependent plasticity in frequency encoding by eighth nerve auditory afferents. In this study, evoked potentials were recorded in vivo from the saccule, the main auditory division of the inner ear of most teleosts, to test the hypothesis that males and females exhibit seasonal changes in hair cell physiology in relation to seasonal changes in plasma levels of steroids. Thresholds across the predominant frequency range of natural vocalizations were significantly less in both sexes in reproductive compared with non-reproductive conditions, with differences greatest at frequencies corresponding to call upper harmonics. A subset of non-reproductive males exhibiting an intermediate saccular phenotype had elevated testosterone levels, supporting the hypothesis that rising steroid levels induce non-reproductive to reproductive transitions in saccular physiology. We propose that elevated levels of steroids act via long-term (days to weeks) signaling pathways to upregulate ion channel expression generating higher resonant frequencies characteristic of nonmammalian auditory hair cells, thereby lowering acoustic thresholds.

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Section: Mechanisms For Saccular Hair Cell Plasticitymentioning

confidence: 58%

Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish

Rohmann

Bass

2011

Journal of Experimental Biology

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“…The kinetics of these ion currents are key elements responsible for the tuning of hair cell receptors to a specific frequency [Art and Fettiplace, 1987]. In weakly electric teleost fishes, the resonant frequency of tuberous electroreceptor potentials closely matches the BF of electrosensory primary afferents and is thought to be responsible for the frequency tuning of the afferent neurons [Zakon and Meyer, 1983]. Furthermore, in Sternopygus, as the fish increases in size the BF of the electroreceptive units increases [Sanchez and Zakon, 1990].…”

Section: Discussionmentioning

confidence: 99%

“…Alternatively, age-related changes in the ionic membrane properties of the ampullary epithelium could affect the frequency selectivity of electroreceptors. Frequency selectivity of hair cell receptors is related to the electrical resonance of receptor potentials in vertebrates [Crawford and Fettiplace, 1981;Art et al, 1986;Hudspeth, 1989] including the electroreceptors of elasmobranch and teleost fishes [Clusin and Bennett, 1979;Viancour, 1979;Zakon and Meyer, 1983]. The oscillation of receptor potentials and the resultant electrical resonance along the receptor epithelium is due to the interaction between inward calcium and outward calcium-dependent potassium currents [Lewis and Hudspeth, 1983;Fettiplace, 1987].…”

Section: Discussionmentioning

confidence: 99%

Ontogenetic Changes in the Response Properties of the Peripheral Electrosensory System in the Atlantic Stingray <i>(Dasyatis sabina)</i>

Sisneros

Tricas

2002

Brain Behav Evol

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Adult stingrays use their ampullary electroreceptors to detect prey and locate mates, but the response properties and function of their electrosensory system in the pre-adult stages are unknown. We examined the response properties of Atlantic stingray (Dasyatis sabina) electrosensory primary afferent neurons through ontogeny to determine whether encoding of electrosensory information changes with age, and how it relates to the ontogenetic encoding of biologically relevant electric stimuli. We show that during development electrosensory primary afferents increase resting discharge regularity, show an upward shift in best frequency (BF), an increase in neural sensitivity, and a decrease in bandpass. These ontogenetic changes in the response properties of the stingray electrosense are consistent with sensory adaptations to enhance the avoidance of large predators as young, and increase the location of prey and mates as adults.

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“…Four Hertz has been determined to be in the optimal range of frequency differences for eliciting JARS (Bullock et al, 1972;Partridge et al, 198 1). The Sl frequency was set close to the fish's electric organ discharge frequency so as to stimulate its electroreceptors optimally (Hopkins, 1976;Zakon and Meyer, 1983). Physiology Our experimental procedures were similar to those used in earlier intracellular studies (Heiligenberg and Dye, 1982;Heiligenberg and Rose, 1985).…”

Section: Behaviormentioning

confidence: 99%

A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology

Carr¹,

Heiligenberg²,

Rose³

1986

J. Neurosci.

141

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Behavioral experiments show that the weakly electric fish, Eigenmannia, detects differences in timing as small as 400 nsec between electric signals from different parts of its body surface. The neural basis of this remarkable temporal resolution was investigated by recording from elements of the phase-coding system, a chain of electrotonically connected neurons devoted to the processing of temporal information. Each element of this system fires a single action potential for every cycle of the electric signal (either the fish's own electric organ discharge or a sinusoidal signal of similar frequency). For phase-coding primary afferents and midbrain neurons, the temporal resolution was determined by measuring each unit's capacity to lock its spike to a particular phase of the stimulus cycle. The jitter of a neuron's response (measured as the standard deviation of the timing of the spikes with respect to the stimulus) decreases from the level of the primary afferent (mean = 30 ctsec) to the midbrain torus (mean = 11 rsec); these results can be correlated with morphological measures of convergence. The temporal resolution of single neurons is still inferior to that displayed at the behavioral level.The detection of small temporal disparities between two signals is a process of general interest in sensory physiology, mediating localization of sound in the auditory system and providing an illusion of depth perception in vision (Pulfrich phenomenon). We employ a behavioral assay, the Jamming Avoidance Response (JAR), to demonstrate that the weakly electric fish, Eigenmannia, is able to detect temporal disparities of electrical signals as small as 400 nsec. In order to understand the origins of this sensitivity, we used intracellular recording techniques to identify the individual elements of the underlying neuronal circuit with respect to their response properties and morphology. In a subsequent study (Carr et al., in press), ultrastructural techniques have been used to reconstruct the midbrain circuit that performs these time comparisons.Eigenmannia is a South American gymnotiform fish which produces a high-frequency wave-type electric organ discharge. It uses this discharge both for electrolocation and for social communication. These fish possess a simple behavior, the JAR, whereby they shift the frequency of their electric organ discharge so as to avoid being jammed by a neighboring conspecific with a similar frequency (usually within +/-20 Hz; Bullock et al.,

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Plasticity of electroreceptor tuning in the weakly electric fish,Sternopygus dariensis

Cited by 49 publications

References 28 publications

Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish

Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish

Ontogenetic Changes in the Response Properties of the Peripheral Electrosensory System in the Atlantic Stingray <i>(Dasyatis sabina)</i>

A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology

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