Avoidance conditioning of the rate of electric organ discharge in mormyrid fish

doi:10.1016/0003-3472(68)90039-0

Animal Behaviour

Volume 16, Issue 4, November 1968, Pages 448-455

https://doi.org/10.1016/0003-3472(68)90039-0 Get rights and content

Abstract

In Mormyrid fish the electric organ appears to discharge as a single unit, and the frequency of discharge is a simply quantifiable behavioural variable. Following a study showing that acceleration in discharge rate can be conditioned classically, demonstration of operant conditioning was undertaken using a yoked control procedure. For each pair of fish six to twelve series of trials were run, and in successive series the avoidance and control contingencies were reversed. The procedure permitted comparison of the contingencies successively in the same fish and simultaneously between fish. The results from eight Gnathonemus indicated that avoidance conditioning can control electric organ activity. In naive subjects avoidance conditioning produced significantly more responding than yoked classical conditioning (P > 0·02). The occurrence of avoidance conditioning was confirmed by the effects of subsequent reversals of avoidance and control schedules.

References (10)

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Cited by (13)

Electric organs
2023, Fish Physiology
Neural mechanisms and behaviors for acoustic communication in teleost fish
2003, Progress in Neurobiology
Sound communication is not unique to humans but rather is a trait shared with most non-mammalian vertebrates. A practical way to address questions of vocal signal encoding has been to identify mechanisms in non-mammalian model systems that use acoustic communication signals in their social behavior. Teleost fishes, the largest group of living vertebrates, include both vocal and non-vocal species that exploit a wide range of acoustic niches. Here, we focus on those vocal species where combined behavioral and neurobiological studies have recently begun to elucidate a suite of adaptations for both the production and the perception of acoustic signals essential to their reproductive success and survival. Studies of these model systems show that teleost fish have the vocal–acoustic behaviors and neural systems both necessary and sufficient to solve acoustic problems common to all vertebrates. In particular, behavioral studies demonstrate that temporal features within a call, including pulse duration, rate and number, can all be important to a call’s communicative value. Neurobiological studies have begun to show how these features are produced by a vocal motor system extending from forebrain to hindbrain levels and are encoded by peripheral and central auditory neurons. The abundance and variety of vocal fish present unique opportunities for parallel investigations of neural encoding, perception, and communication across a diversity of natural, acoustic habitats. As such, investigations in teleosts contribute to our delineating the evolution of the vocal and auditory systems of both non-mammalian and mammalian species, including humans.
Further analysis of the individual discharge characteristics predicting social dominance in the electric fish, Gymnotus carapo
1975, Animal Behaviour
The electric organ discharge (EOD) behaviour of Gymnotus carapo was analysed in isolated fish with no previous experimental experience. All animals were then allowed social interaction (4 hr total), and were finally retested in isolation. Each of the two individual testing sessions consisted of four trials per fish, during which frequency histograms of the EOD intervals were accumulated. The results showed that the histograms were invariably multi-modal, and the reasons for this were examined. They were then subjected to a computer-aided statistical analysis, and various features were shown to be related to the dominance status of the fish determined in the second part of the study. A subsequent experiment performed 6 months later demonstrated sequential frequency ‘shifts’ in resting isolated Gymnotus. These shifts are discussed in terms of the interval histogram results, and it is suggested that they represent a type of social advertisement. Finally, a hypothetical physiological mechanism is proposed to account for the observed EOD distributions.
Electroreception
1971, Fish Physiology
Many groups of fish have receptors that are specialized for the detection of electric fields. The existence of these electroreceptors was first clearly indicated in weakly electric fish, which continually set up low voltage electric fields around themselves by means of their electric organs. If the water over a receptor opening is replaced by air, a local electrode need pass much less current to produce a given voltage change outside the receptor; the shunting by the water is reduced. Although the degree of residual shunting by the skin and remaining water has not been satisfactorily evaluated, the current voltage relation measured under these conditions is likely to have considerable contribution from the receptor cells because the input resistances become large, as high as several megohms. Receptor cells of phasic receptors contribute importantly to the external potentials under these conditions. Another important characteristic of the input–output relationship of the receptor synapses is sensitivity. The input–output relationship of synaptic membrane of phasic receptor cells differs from that of tonic receptor cells in that there is little resting release of transmitter. It is difficult to be confident of the shape of the potential-secretion relationship because of active processes in the receptor cells. It is likely but uncertain that the secretory membrane of phasic receptors does have an input–output relationship that has a much greater slope than that at known interneuronal and neuromuscular synapses.
Electric Organs
1971, Fish Physiology
Electric organs are specialized for the production of an electric field outside the body. The study of electric organs and electrocytes has illuminated many aspects of membrane physiology. They are found only in fish but apparently have evolved independently in some six different groups. Their primary usefulness is a result of evolution that has exaggerated different membrane functions in different electrocytes. For example, the concept of independent sites that pass different ions or groups of ions becomes more reasonable given that specific kinds of permeability can occur in isolation in different regions of a single cell or in different cells. Examples are the isolated occurrence of membrane generating postsynaptic potentials (in Astroscopus and torpedinids), of membrane exhibiting delayed rectification, and of the electrically excitable sodium system without delayed rectification (in the electric eel). This macroscopic separation suggests microscopic separation, which in many single membranes can only be inferred from functional arguments or pharmacological data. These specializations of different kinds of membrane cannot really be said to have been responsible for major advances in electrophysiological knowledge. As new morphological, biochemical, and biophysical techniques become available, electrocytes may provide the best tissues for their evaluation.
'Communication' in weakly electric fish, Gnathonemus niger (Mormyridae) I. Variation of electric organ discharge (EOD) frequency elicited by controlled electric stimuli
1970, Animal Behaviour
The weakly electric fish, Gathonemus niger, discharged with a frequency of 4 to 8 Hz during the day and 10 to 16 Hz during the night. The frequency of superimposed burst discharges (32 to 56 Hz) was independent of diurnal factors. The variation of the electric organ discharge frequency during the day was investigated in response to controlled electric stimulus patterns: (a) A free running stimulus frequency of 4 Hz, simulating the resting frequency of another fish, and different stimulus intensities, simulating different distances between two fish. (b) Free running frequencies of 4, 8, 16, …, 128 Hz and two particular stimulus intensities. (c) Discharge coupled stimuli (each discharge triggered an electric stimulus with a fixed delay) and different stimulus intensities.
All three kinds of stimuli elicited defined and predictable response discharge patterns supporting the assumption that an electric fish would respond to a particular discharge pattern of another fish also in a similar and predictable manner. Low stimulus intensities (0·04 to 0·2 mV per cm) caused cessation of the discharge activity, a ‘hiding’ or ‘listening’ response. The discharge rate increased linearly with the logarithm of the stimulus intensity. The fish was particularly sensitive to stimulus frequencies which simulated its burst activity (32 to 56 Hz). Discharge coupled stimuli showed that the fish responded to about eight times lower stimulus intensities if the stimulus occurred between two discharges (15 to 30 m-s after the fish's discharge) than if the stimulus occurred within or immediately after the discharge. All suprathreshold stimuli elicited a typical discharge pattern: The irregular resting discharge activity became significantly regular. The degree of regularity was even improved during maintained stimulation. The regularisation of the discharge activity is thought to be involved in the fish's electrolocating system whereas frequency variations are considered as being involved in both the locating system and as communication signals among weakly electric fish.

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^☆: This report is based on experiments carried out while the authors were at the College of Physicians and Surgeons, Columbia University, New York. Supported in part by grants from the United States Public Health Service (Research Grants MH 07152, MH13644, training grant 5TINB5328 and Career Program Award K3GM-5828) and from the United States Air Force Office of Scientific Research (AF-AFOSR-550).

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Avoidance conditioning of the rate of electric organ discharge in mormyrid fish☆

Abstract

Electroreceptors in Mormyrids

Mechanisms of eletroreception

Physiology and ultrastructure of efectrotonic junctions. II. Spinal and medullary electromotor nuclei in Mormyrid fish

J. Neurophysiol

Habitation and conditioning

J. comp. physiol. Psychol

Systematic effect of random error in the yoked control design

Psychol. Bull