R.C. Peters

Low-Dimensional Dynamics in Sensory Biology 1: Thermally Sensitive Electroreceptors of the Catfish

We report the results of a search for evidence of periodic unstableorbits in the electroreceptors of the catfish. The function of thesereceptor organs is to sense weak external electric fields. Inaddition, they respond to the ambient temperature and to the ioniccomposition of the water. These quantities are encoded by receptorsthat make use of an internal oscillator operating at the level of themembrane potential. If such oscillators have three or more degreesof freedom, and at least one of which also exhibits a nonlinearity,they are potentially capable of chaotic dynamics. By detecting theexistence of stable and unstable periodic orbits, we demonstratebifurcations between noisy stable and chaotic behavior using theambient temperature as a parameter. We suggest that the techniquedeveloped herein be regarded as an additional tool for the analysisof data in sensory biology and thus can be potentially useful instudies of functional responses to external stimuli. We speculatethat the appearance of unstable orbits may be indicative of a stateof heightened sensory awareness by the animal.

On the electrodetection threshold of aquatic vertebrates with ampullary or mucous gland electroreceptor organs

Reinterpretation of research on the electric sense in aquatic organisms with ampullary organs results in the following conclusions.

Periodic firing pattern in afferent discharges from electroreceptor organs of catfish

Spontaneous afferent activity was recorded from 26 single ampullary electroreceptive organs of freshwater catfish (Ictalurus nebulosus LeS) at various temperatures. Regular grouping of action potentials was apparent in this secondary sensory system at 35°C and occasionally at 30°C. Impulse groups consisted of up to seven impulses. The precise timing of impulse generation and the temporal sequence of impulses indicated that oscillating processes are involved. Expectation density functions were calculated for records of afferent activity obtained at various temperatures below 35°C. In the majority of records the function was periodic. Impulse grouping and expectation density functions became more distinct in units exhibiting extremely high thresholds (i.e. being insensitive) to electrical stimuli. The results suggest that the oscillations originate from the postsynaptic membrane. The temporal pattern of impulse generation within impulse groups of ampullary electroreceptor organs and of specific warm and cold receptors was compared and found to be similar. Application of cadmium and menthol, which both reduce calcium entry, suppressed spontaneous activity in normal and insensitive electroreceptor systems, attenuated the sensitivity of normal receptors and modified the periodic pattern. This indicates that calcium is implicated in sensory transduction and in postsynaptic mechanisms. The data suggest that an oscillating process is one component of signal transmission in ampullary electroreceptor organs of teleost fish.

Ampullary electroreceptors in catfish (Teleostei): temperature dependence of stimulus transduction

The response properties of ampullary electroreceptors have been studied in the catfish Ictalurus nebulosus at skin temperatures between 5 and 35 °C. A unimodal relationship between spontaneous activity and temperature was obtained. Mean (±SEM) peak discharge rate was 57.3 ±1.8 impulses s−1 at 25 ° C; the receptors were active at 5 °C (15.0 impulses s−1) and at 35 °C (31.5 impulses s−1). There were no dynamic responses to temperature changes in either the warming or cooling direction. The shape of the frequency characteristic depended on temperature: the peak of the gain curve shifted to low frequencies at low temperatures. There was a concomitant change of the phase characteristic: the intersection at zero degree phase angle shifted to higher frequencies with an increase of temperature, thus increasing the lead at lower frequencies and decreasing the lag at higher frequencies. Latency after combined excitatory and inhibitory impulse stimulation was temperature dependent, ranging from 16.4 ms (5 °C) to 5.6 ms (35 °C). Application of the specific calcium channel blocker menthol (0.2 mM) suppressed spontaneous activity, the effect becoming more prominent at higher temperatures. Sensitivity to sinusoidal electrical stimulation was also impaired, but to a lesser degree and mainly at lower temperatures. We conclude that the filter properties of the receptor organ can be modelled by a band-pass filter in series with a latency, both of which are temperature dependent. These filter properties might be partially based on the activation kinetics of the tranduction channels.

Converging electroreceptor cells improve sensitivity and tuning.

We studied the effect of convergent clustering of ampullary electroreceptor organs on stimulus transduction and transmission in the catfish Icalurus melas by electrophysiologically recording primary afferent activity of single ampullae (singlets) and pairs (doublets) innervated by the same afferent. Doublets were twice as sensitive as singlets, and showed sharper tuning around the best frequency. The slope of the phase curve in the doublets was slightly steeper than in the singlets. The spontaneous activity and scatter in interspike interval were not correlated with clustering. The implications of these findings for signal averaging in sensory neurons and their relevance for behaviour are discussed.

Transduction at electroreceptor cells manipulated by exposure of apical membranes to ionic channel blockers

Abstract 1. Stimulus transduction in catfish electroreceptors was investigated electrophysiologically during local exposure to low-Ca 2+ water and the ionic channel blockers verapamil, bepridil, Cd 2+ TTX and TEA. 2. Current through receptor cells is not carried by Ca-ions passing through voltage sensitive Ca-channels in the apical membranes. Ca-channel Mockers act on compartments inside the receptor cells. 3. Resting discharge rate and modulation of resting discharge can be manipulated independently. This is inconsistent with the concept that both parameters are controlled by neurotransmitter release only; more receptor cell functions must be involved.

The electroreceptor organ of the catfish, Ictalurus melas, as a model for cisplatin-induced ototoxicity.

The ototoxic side-effects of the anti-cancer drug cisplatin (cis-diaminedichloroplatinum) have been widely investigated. However, the exact site of action remains unclear. In this study, the electroreceptor organ of the freshwater catfish Ictalurus melas is used as a model for examining the acute effects of cisplatin. The sensory cells in the electroreceptor organ are homologous to the inner hair cells in the cochlea of mammals. The effects of cisplatin administration can be investigated by in vivo recording of the spike trains from the electroreceptor organ primary afferents. Exposure of electroreceptor organs to 330 microM cisplatin for 1 h causes the spontaneous activity to drop, the overall sensitivity to diminish and the shape of the frequency characteristics to change. These effects persist in the week after administration. Control levels have returned at day 22. These results demonstrate an acute and, with considerable hysteresis, reversible cisplatin effect on the electroreceptor organs, which is to a large extent consistent with the cisplatin-induced effects in isolated hair cells in mammals. The time-course of the effect supports the hypotheses that ion channels are blocked immediately by cisplatin administration, and that cisplatin metabolites disturb enzymatic cellular processes.

In vitro electroreceptor organs for pharmacological studies.

Electroreception is a well-established sensory faculty in aquatic vertebrates. The general physiology of the receptor organs is comprehensively documented. The transduction mechanism of the receptor cells and the synaptic transmission mechanism are less well understood. Research has been hampered by the inaccessibility of the synaptic site. This paper describes how to prepare an in vitro preparation of ampullary electroreceptor organs which allows exposure of both the mucosal and the serosal sides of the receptor cells to superfusion of test solutions. The preparation is quite robust and has been shown to function reliably for more than 8 h. Furthermore, the use of in vitro electroreceptors organs as a model for pharmacological studies is evaluated.

The actions of L-glutamate and its agonists on the ampullary electroreceptor organs of the catfish Ictalurus nebulosus

Abstract 1. Ampullary electroreceptors of the freshwater catfish, Ictalurus nebulosus, were examined for the effects of bath-applied l -glutamate ( l -GLU) and its agonists quisqualate (Q), kainate (KA) and n -methyl- d -aspartate (NMDA). Resting discharge rate and stimulus-evoked activity in single afferent fibers were recorded in an in vitro preparation. 2. l -GLU (0.1–1 mM), Q (0.8–40 μM) and KA (10–250 μM) strongly increased both resting activity and stimulus-evoked activity in the afferent fibres. NMDA had no effect, even at a concentration of 5.0 mM. 3. The potencies of l -GLU and its agonists, arbitrary defined as the concentrations which gave 50% of maximal frequency increase, were of the order of 7 μM (Q), 25 μM (KA) and 0.6 mM ( l -GLU). 4. The excitatory effects of l -GLU persisted in receptors suppressed by high Mg2+, indicating that l -GLU was acting at the postsynaptic site. 5. The data presented are consistent with our current concept that the action of l -GLU in Ictalurus electroreceptors is mediated via Q/AMPA- and KA-types, but not the NMDA-type, of membrane receptors.

Simultaneous measurements of calcium mobilization and afferent nerve activity in electroreceptor organs of anesthetized Kryptopterus bicirrhis

The transduction pathway of ampullary electroreceptor organs involves ionic currents. It has been shown that calcium, as well as sodium and potassium play important parts in this process. In this study we examine the stimulus-evoked changes in the Fura-2 ratio in electroreceptor cells. Furthermore, we recorded stimulus-evoked Fura-2 ratio changes while Na+ and K+ channels were blocked by amiloride and TEA. Simultaneously, extracellular recordings of the afferent spike activity were made. The results show the presence of stimulus evoked fluctuations in the Fura-2 ratio. These fluctuations can be abolished by the application of Cd2+, TEA, and amiloride. The stimulus-evoked activity of the afferent nerve was decreased due to application of these drugs. We conclude that the transduction current is carried by Na+, K+, and probably Ca2+. This fits the existing model on transduction in electroreceptors.