F. Bretschneider

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.

Functioning of catfish electroreceptors: fractional-order filtering and non-linearity

Abstract 1. 1. Properties of electroreceptors of the catfish Kryptopterus bicirrhis have been determined by in vivo recording of action potentials from individual receptors. 2. 2. The frequency characteristics were determined using sinusoidal stimuli; the mean spake rate modulation was taken as response variable. 3. 3. The gain characteristics shows an optimum at stimulus frequencies of 5–10 Hz, and has a slope of approximately 3 dB/oct at the low-frequency side of the optimum. 4. 4. The phase characteristic has a plateau at about 45° lead in that region. 5. 5. A mechanism that may be responsible for this functional order characteristic is discussed. 6. 6. Stimulation of electroreceptors with a relatively strong current at frequencies between 0.01 and 0.1 Hz causes a non-linear response, even if the spike rate modulation is less than 100%. 7. 7. We discuss two possible mechanisms for this non-linearity, involving either the synapses or the tight junctions around the receptor cells.

Influence of Direct Current Stimulation On the Ion-Induced Sensitivity Changes of the Electroreceptors (Small Pit Organs) of the Brown Bullhead, Ictalurus Nebulosus LeS

1) The a.c. sensitivity of the electroreceptors of the brown bullhead, Ictalurus nebulosus LeS., could be controlled by applying direct current stimuli with current densities of 2 × 10 -7 to 2 × 10 -5 A/cm 2 . 2) These effects bear a tonic character and may last up to 15 minutes. 3) Increases or decreases in the electroreceptors sensitivity caused by alterations in the ionic contents of the animals environment, could also be compensated by applying direct current stimuli. 4) The implantation of electrodes in intact animals was strongly improved by the use of cocoa butter for electrical insulation and mechanical fixation. 5) Implications of the voltage controlled sensitivity of the electroreceptors are discussed.

Ultrastructure of free nerve endings in respiratory and squamous epithelium on the rat nasal septum

The distribution of nerve fibres in the mucosa of the nasal septum of the rat was investigated by means of transmission electron microscopy on transverse and tangential ultrathin sections. Near the basement membrane of respiratory and squamous epithelium, a rather dense network of unmyelinated nerve fibres occurs. Some fibres in the respiratory epithelium ascend between the epithelial cells to reach up to the tight junctions. These fibres appeared in transverse sections to end as hooks or boutons, sometimes with branches. These shapes resemble the free nerve endings that are considered to act as nociceptors. The small intraepithelial fibres, with diameters of about 0.5–1 μm, contain both dense granules and clear vesicles comparable to synaptic vesicles. Substance P was found in dense granules in basal fibres; vasoactive intestinal peptide was absent throughout the epithelium. Acetylcholinesterase activity was observed closely associated with the basal fibres; the apical fibres showed little if any activity. Membrane specializations pointing to an efferent function as well as structures usually associated with mechanoreceptive functions were lacking in both respiratory and squamous epithelium.

Denervation changes the transmission properties of electroreceptor sensory synapses

1. 1. The effects of denervation on extracellular primary afferent single unit activity in electroreceptor organs or catfish, Ictalurus nebulosus, were studied under alphaxalone anaesthesia. 2. 2. Compared to nerve sectioning, skin patch excision is a useful method for denervation; effects are found on the same time scale as in nerve-sectioned organs. 3. 3. Resting discharge decreases from 6 hr after denervation until, at 30 hr, no activity can be recorded. Sensitivity remains unaffected by denervation. 4. 4. In the absence of resting discharge, stimulation of electroreceptors can still evoke responses. 5. 5. These effects are consistent with morphological evidence, demonstrating that the first changes are found in the unmyelinated primary afferent endings, whereas the receptor cells and the myelinated parts of the primary afferents remain unaffected.

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.

Synaptic noise in spike trains of normal and denervated electroreceptor organs.

The sequence of interspike intervals of the spontaneous activity in denervated electroreceptor organs of the catfish is analysed with several statistical techniques: visual inspection of dot displays, interval histograms, serial correlograms, tests for stationary and trends, and tests for renewal properties, based on the spectrum of intervals. The interspike interval train of primary afferents can usually be treated as a renewal process. Following denervation, a number of non-renewal properties emerge. The interval histogram of the renewal spike trains can be fitted well with a gamma probability density function; non-renewal cases need a more complex approach. We propose that the stochastic fluctuations in interval duration arise from randomly occurring quantal depolarizations (Steins model of stochastic neuronal excitations. Two important properties with regard to synaptic transduction are: afferent firing results from capture of a limited number of depolarizing quanta; and the quantal input rate and the threshold for firing appear to be correlated.