The emergence of electroreceptor organs in regenerating fish skin and concurrent changes in their transduction properties.

The process of regeneration of skin patch denervated empullary electroreceptor organs of the African catfish Clarias gariepinus has been investigated at an ambient temperature of 28 degrees C with both electrophysiological and histological methods. At day 1 after denervation none of the receptor organs on the skin patch showed afferent activity. At this stage none of the ampullary organs previously recorded showed a normal appearance. Degenerative changes consisted of a decreased number of receptor cells and an often invisible lumen. At day 7 regeneration seems to start with a high density of primordial ampullary organs, more than a seven-fold increase compared to controls. In these units, the level of spontaneous activity is very low: compared to controls, more than a two-fold increase in mean interspike interval. At this stage, the sensitivity to electrical stimuli is already at the level of untreated control organs. At day 15 there is a lower, i.e. approximately normal, density of ampullary organs with a normal morphology. In these units both spontaneous firing and sensitivity returned to normal. It can be concluded that the functional dichotomy between spontaneous firing and sensitivity that was found in degenerating ampullary electroreceptor organs is also found during the process of their regeneration, although the underlying cellular changes may be totally different. The speed of recovery suggests that only regeneration of the distal part of the sectioned nerve fibers takes place.     

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.     

Spontaneous nerve activity and sensitivity in catfish ampullary electroreceptor organs after tetanus toxin application

The functioning of electroreceptor organs of Ictalurus sp. was investigated by inhibiting synaptic transmission by the administration of tetanus toxin in vitro. A piece of Ictalurus skin of about 20 mm diameter was mounted in an Ussing-type chamber. After establishing the normal functioning of the organ, tetanus toxin (TeTx) was applied basolaterally for 150 min in 66.7 pM and 400 pM concentrations, while the single unit nerve activity was recorded extracellularly. Spontaneous spike activity and the sensitivity of the electroreceptor organs were measured. The results show that TeTx reduces sensitivity to less then 20% of its original value, whereas the spontaneous activity is unaffected by the treatment. This indicates that the afferent nerve is capable of generating impulses independent of receptor cell neurotransmitter release. In the discussion we suggest two alternative mechanisms for the emergence of the spontaneous spike activity.     

Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. II. Intra-axonal recordings show initial stages of central processing

1. Physiologically and morphologically identified primary afferent fibers from mormyromast electroreceptor organs were recorded intracellularly. The fiber recordings were made from the nerve root of the posterior lateral line nerve, where the fibers enter the brain, and from the electrosensory lateral line lobe (ELL), near the central terminals of the fibers. 2. The intracellular recordings reveal a variety of potentials, synaptic and nonsynaptic, in addition to the large orthodromic action potentials from the periphery. The goal of the present study was to describe and interpret these various potentials in mormyromast afferent fibers as a first step in understanding the processing of electrosensory information in ELL. 3. Three types of synaptic potentials were recorded inside mormyromast afferent fibers: 1) electric organ corollary discharge (EOCD) excitatory postsynaptic potentials (EPSPs), driven by the motor command that elicits the electric organ discharge (EOD); 2) EPSPs evoked by electrosensory stimulation of electroreceptors in the skin near the electroreceptor from which the recorded fiber originates or by direct stimulation of an electrosensory nerve; and 3) inhibitory postsynaptic potentials (IPSPs) evoked by electrosensory stimulation of more distant electroreceptors. These synaptic potentials can be attributed to synaptic input to postsynaptic cells in ELL that is observed inside the afferent fibers because of electrical synapses between the fibers and the postsynaptic cells. 4. The peripherally evoked EPSPs could frequently be shown to be unitary. The unitary EPSPs were identical to the orthodromic spikes in originating from a single electroreceptor, in threshold, and in latency shift with increasing stimulus intensity. These similarities suggest that the unitary EPSPs are electrotonic EPSPs caused by impulses in other mormyromast afferent fibers that terminate on some of the same postsynaptic cells as the recorded fiber. The peripherally evoked IPSPs had a longer latency than the EPSPs or orthodromic spikes, requiring the presence of an inhibitory interneuron. 5. The peripherally evoked EPSPs, both unitary and nonunitary, show absolute refractory periods of 3-8 ms, followed by relative refractory periods of approximately 8 ms, when tested with two identical stimuli to a nerve. These refractory periods are interpreted as because of refractoriness in the fine preterminal branches of the axonal arbor. 6. A depolarizing afterpotential is commonly associated with the orthodromic spike and probably results from the successful propagation of the spike into the entire terminal arbor. The depolarizing afterpotential has a refractory period that is similar to that of the peripherally evoked EPSPs and that is also interpreted as refractoriness in the fine preterminal branches.(ABSTRACT TRUNCATED AT 400 WORDS)     

The Effect of Extracellular Calcium on Thermal Excitability of the Sensory Units in the Tooth of the Cat

Intradental sensory nerve impulse activity was measured from dentinal cavities in canine teeth of anesthetized cats. No spontaneous activity was usually recorded in cavities filled with isotonic saline. Heat stimulation of 15–20^oC failed to give any impulse activity, while other stimuli, such as air blasts produced bursts of impulses. Lowering extracellular calcium ion concentration. by local application of sodium citrate, sodium oxalate or EDTA, induced impulse activity. Under these conditions, heat produced a rapid increase in discharge activity. which lasted as long as the stimulus was applied. Increased extracellular calcium concentration abolished this response to heat. The present findings show that a change in the extracellular calcium ion concentration modulates the excitability of intradental sensory units, and may thus also modulate the resulting experience of pain.     

The fine structure of ampullary and tuberous electroreceptors in the South American blind catfish Pseudocetopsis spec

Summary Two types of electroreceptors, the ampullary and the tuberous electroreceptor (silurid knollenorgan) in the epidermis of the catfish, Pseudocetopsis spec., were investigated with semithin and ultrathin serial sections. The ampullary organ contains one or two sensory cells which are embedded in supporting cells at the base of open epithelial canals. They bear some slender microvilli on their apical surface and form several synaptic bars. The afferent myelinated nerve fiber arborizes in the connective tissue papilla and looses its myelin sheath about 30 m below the supporting cell layer. A second thin myelinated axon occur up to the supporting cell layer. The tuberous electroreceptor organ contains one large receptor cell. Most of the cell body is exposed to the lumen of a specialized proximal canal segment and is closely covered with microvilli. A single myelinated axon looses its myelin sheath within the supporting cell layer about 1 m before terminating as a flat calyx at the base of the sensory cell. A functional significance of the two types of receptors will be discussed.     

Cold-sensitive mechanoreceptors with afferent C-fibres in the sheep duodenum

The effect of changes of temperature on the impulse activity of duodenal mechanoreceptors with afferent C-fibres was studied in acute electrophysiological experiments in chloralose-anaesthetised sheep. The impulse activity of 4 tension receptor units increased when the duodenal mucosa was cooled over the range 0–39° C. The impulse activity of 10 tension receptors was reduced when the mucosa was cooled. Temperature changes between 39° C and 52° C did not alter the discharge pattern of either type of tension receptor response. An additional unit, which may have been associated with pyloric circular muscle, was excited by cooling over the temperature range 0–39° C. This unit was insensitive to compression and was excited by close-intra-arterial injections of pentagastrin, nor-adrenaline, prostaglandin F₂ and prostaglandin E₂. The cold-sensitivity of mechanoreceptors in the duodenal muscularis externa may play a role in the reflexes regulating gastric emptying in experimental situations when duodenal chyme is cold.     

Afferent G Units Responding to Mechanical,Thermal and Chemical Stimuli in Human Non-Glabrous Skin

C unit activity was recorded with microelectrodes from intact sensory fascicles in the human peroneal nerve. The analysis includes 46 afferent units with receptive fields predominantly on the dorsum of the foot and ankle. 16 units were tested quantitatively. Another 30 units were tested qualitatively by a combination of electrical and natural stimuli in the skin. This method was valuable for a reliable identification of activity in individual afferent C elements, when several C units with similar potential amplitudes responded to testing in the skin. The units were not spontaneously active at normal skin temperatures but one unit showed a low frequency discharge at a skin temperature of 22^o C. Cooling by ether evaporation was an inefficient stimulus except for 2 units. Gentle mechanical stimuli did not activate any of the units, whereas afferent C unit impulses were induced by moderately intense mechanical stimuli, noxious heat and various chemical irritants. The sensations produced by stimuli inducing intense afferent C unit activity were reported as “burning or delayed pain”, whereas stimuli eliciting low frequency activity often were reported as “itch”. It is concluded that polymodal C receptors, similar with “polymodal nociceptors” in the cat and monkey, are numerous in skin areas sparsely covered with hairs on the dorsum of the foot and ankle in man, whereas no low threshold C mechanoreceptors were identified. The experiments do not exclude the possibility that both delayed pain and burning itch sensations may be mediated by different impulse patterns from polymodal C receptors.     

Analysis of cold and warm receptor activity in vampire bats and mice

The response characteristics of facial thermoreceptors of the common vampire bat and of the mouse have been quantitatively studied. Cold receptors were identified in bat and mouse; warm receptors were only established in the bat. Cold and warm receptor populations of the two species share most of their properties with facial thermoreceptor populations of various mammalian species investigated so far. The temporal pattern of activity of cold receptors of the mouse corresponded to that observed in cats, dogs and monkeys: impulse groups at lower, and beating activity at higher temperatures. At maintained temperature, no impulse groups were initiated in cold receptors of the bat. However, cooling steps from various initial temperatures induced a transient grouped discharge in both cold receptor populations. A discharge in regular groups of impulses was occasionally generated in warm receptors of the bat at maintained temperatures and following warming steps. The data indicate that the temperature dependence of periodic activity in warm receptors is not as uniform as it is in cold receptors. It is concluded that cyclic processes are involved in sensory transduction of both warm and cold receptors, and that this cyclic behavior seems to be a general property of thermoreceptors of presumably all vertebrate species.     

Static and dynamic discharge patterns of bursting cold fibers related to hypothetical receptor mechanisms

Static and dynamic discharge patterns of bursting cold fibers in the lingual nerve of the cat were analysed at temperatures between 10 and 40°C. The period of the static burst discharge depends only on temperature and is not affected by the number of spikes per burst. The termination of an intraburst sequence of impulses can be predicted by the duration of the intraburst intervals. Irregular impulse patterns at low static temperatures show a unimodal interval distribution, whereas the interval histograms from irregular spike sequences at high temperatures have multiple peaks with nearly equal distances.The dynamic responses to cooling steps of 5°C show a transient reduction of the burst period and a transient increase of the number of spikes per burst or the burst duration, respectively. In addition, the maximmum intraburst frequencies transiently increase while the frequency decay within the burst is continuously reduced. At low temperatures, the burst discharge is sometimes interrupted by a continuous impulse sequence of high frequency.A model of temperature transduction is discussed on the basis of membrane processes which are particularly described for molluscan neurons. The results support the hypothesis that the bursts are triggered by an endogenously oscillating receptor potential. It is assumed that at high temperatures the oscillation continues but certain cycles fail to trigger impulses. The results during dynamic cooling are interpreted as a flattening of the oscillation which is transiently superposed by a depolarizing shift of the potential waves.     

Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. III. Physiological differences between two morphological types of fibers

1. Mormyromast electroreceptor organs in electric fish of the family Mormyridae have two types of separately innervated sensory cells, the A and B sensory cells of Szabo and Wersall. The first paper in this series showed anatomically that afferent fibers from the two types of sensory cell terminate centrally in separate zones of the electrosensory lateral line lobe (ELL), fibers from A cells terminating in the medial zone and fibers from B cells terminating in the dorsolateral zone. The goal of the present study was to determine the physiological differences between the two morphologically distinct types of mormyromast afferent fibers. 2. The present study has two parts. In the first part, mormyromast fibers were recorded near their central terminals in the two mormyromast zones of ELL. In the second part, mormyromast fibers were recorded from a peripheral electrosensory nerve. In both parts, various electrosensory stimuli were delivered and voltage thresholds were measured at the electroreceptor. 3. In the first part of the study, mormyromast fibers terminating in the two central zones were found to be different in their thresholds and in the maximum number of spikes evoked by a single stimulus. Afferent fibers terminating in the medial zone, which arise from A sensory cells, had higher thresholds and smaller maximum spike numbers than fibers terminating in the dorsolateral zone, which arise from B sensory cells. 4. In the second part of the study, the same two groups of fibers--one group with a high threshold and a small maximum spike number, and a second group with a low threshold and a large maximum spike number--were identified in extracellular recordings from a peripheral electrosensory nerve. The thresholds of the two groups were quite distinct, allowing the fibers to be divided into high- and low-threshold groups, which most likely represent the fibers from the A and B sensory cells, respectively. 5. The high- and low-threshold groups of fibers recorded from peripheral nerve were found to be different in a number of additional properties besides threshold and maximum spike number. Additional differences were found in the following properties: strength-duration curve, correlation with a receptor potential recorded at the electroreceptor, tuning curve, and short latency facilitation by a conditioning stimulus. Thus there appear to be several physiological differences between mormyromast afferent fibers from A and B sensory cells, in addition to the differences in threshold and spike number.(ABSTRACT TRUNCATED AT 400 WORDS)     

Effects of local nerve cooling on conduction in vagal fibres shed light upon respiratory reflexes in the rabbit

In ten vagus nerves the effect of local cooling on the compound action potential was studied in the temperature range of 34 to 0 °C in spontaneously breathing, anaesthetized rabbits. The mean temperature at which the myelinated (A) fibres were completely blocked, was 10.2±2.4 °C (mean ± S.D.). In nine nerves, local vagus cooling to 0 °C failed to block all non-myelinated (C) fibres. In one nerve, total blocking occurred at 2.0 °C. We conclude that in the rabbit, the earlier found increase in tonic activity of the diaphragm following lung inflation or deflation during bilateral local vagus cooling to a temperature between 8 and 0 °C is due to afferent impulses in vagal C fibres.     

Activity of foot skin mechanoreceptors and afferent nerve fibres in the adult rat sciatic nerve are altered after central axotomy of sensory neurons

The functional properties of skin mechanoreceptors were examined in the hind foot of normal rats in comparison with animals subjected to dorsal rhizotomy. Evoked nerve impulses were recorded from afferent nerve fibres of the tibial nerve. The decentralized mechanoreceptors displayed evidence of autonomous functioning, but with several abnormalities as compared to normal animals. There was a decreased sensitivity to mechanical stimulation and a lower adaptive capacity as a consequence of rhizotomy. The underlying mechanism is suggested to be a loss of central trophic support because of the interrupted link between the central nervous system and the sensory ganglion cell periphery.The findings indicate that mechanical receptors continue functioning under conditions when sensory impulses flow cannot reach postsynaptic target neurons in the central nervous system, but stop at the level of the primary sensory neuron.     

Variability in impulse discharges in rat chorda tympani fibers in response to repeated gustatory stimulations

Impulse discharges in eight chorda tympani fibers of rats to repeated lingual stimulations by five kinds of chemicals were recorded, and variability in the magnitude and temporal pattern of impulse discharges evoked by the same stimulus was examined. Number of impulses elicited during a certain period after stimulation by a particular test solution varied widely from one trial to another, but after repeated stimulations impulse trains tended to appear at a higher dischage rate. Temporal patterns of impulse discharges produced by a particular stimulus were nearly identical from one trial to another on repeated trials, though they differed to some extent from one unit to another even when the same stimulus was employed. Rhythmic bursts were consistently observed in impulse discharges elicited by sucrose and saccharin in a unit highly sensitive to sucrose. The degree of rhythmicity depended on the sensitivity of a unit to sucrose as well as the frequency and duration of impulse discharges.     

Cutane Wärmereceptoren bei primaten

Summary In preparations from the saphenous nerve and the superficial branch of the radial nerve in Rhesus monkeys (Macaca mulatta), afferent impulses could be recorded during moderate warming of the skin. Single warm fibres serving the back of the hand and the foot had spot-like peripheral fields which were not excited by mechanical stimulation. Multi-fibre preparations excited by mild warming were also obtained, indicating a relatively dense distribution of warm receptors. At constant temperatures from 32° C on, single warm fibres showed a static discharge with a maximum frequency up to 20 impulses/sec in the range between 40 and 44° C. At higher temperatures the frequency decreased again, the discharge often changing from a regular sequence of impulses to an irregular type or a series of periodic bursts. Rapid warming caused an overshoot, rapid cooling a transient inhibition of the warm receptor discharge.

Die Untersuchungen wurden während eines Forschungsaufenthalts am Department of Psychology, Florida State University, Tallahassee, Florida, USA, ausgeführt.     

Selective effects of (−)-baclofen on spinal synaptic transmission in the cat

Summary When ejected microelectrophoretically near spinal interneurones of cats anaesthetised with pentobarbitone and under conditions where postsynaptic excitability was maintained artificially at a constant level, (–), but not (+), -baclofen selectively reduced monosynaptic excitation by impulses in low threshold muscle (Ia and Ib) and cutaneous (A) afferents. Polysynaptic excitation of interneurones and Renshaw cells by impulses in higher threshold afferents was less affected, and baclofen had little or no effect on the cholinergic monosynaptic excitation of Renshaw cells. Glycinergic and gabergic inhibitions of spinal neurones were relatively insensitive to baclofen. These stereospecific actions of baclofen, produced by either a reduction in the release of excitatory transmitter or postsynaptic antagonism, suggest that Ia, Ib, and A afferents may release the same excitatory transmitter which differs from that of spinal excitatory interneurones.Microelectrophoretic (–), but not (+), -baclofen also reduced primary afferent depolarization of ventral horn Ia extensor afferent terminations produced by impulses in low threshold flexor afferents, without altering either the electrical excitability of the terminations or their depolarization by electrophoretic GABA or L-glutamate. This stereospecific action of baclofen is interpreted as a reduction in the release of GABA at depolarizing axo-axonic synapses on Ia terminals.     

Limitations on impulse conduction at the branch point of afferent axons in frog dorsal root ganglion

Summary Impulse conduction at the branch point of afferent axons in dorsal root ganglion (DRG) has been studied using intracellular recording from frog DRG neurons in vitro. The least conduction interval (LCI, the minimum inter-response interval) was determined for pairs of impulses to successfully propagate through the branch point into the dorsal root. At 21°–23°C, average branch point LCI was significantly longer than for afferent fibers in the peripheral nerve. This result suggested that the branch point would limit the maximum frequency of action potentials that could conduct into the dorsal root. This was found to be the case. The maximum frequency of impulses in short trains ( 40 ms) which could conduct into the dorsal root without failure (363 Hz) was accurately predicted by branch point LCI and was far less than the maximum frequency predicted from the LCI of axons in the peripheral nerve (610 Hz). Branch point LCI was correlated (r = -0.78) with the natural log of peripheral axon conduction velocity (CV). However, the relationship of LCI and CV was different for different types of neurons and the shape of the somatic action potential was found to be a reliable predictor of branch point LCI. Neurons with long-duration somatic action potentials with a shoulder on the falling phase tended to have low CV and invariably had long LCI's. Neurons with brief, smooth action potentials had short LCI's regardless of CV. These cells, which appear to be the most differentiated type, have found a way to minimize branch point LCI which is virtually independent of their axonal CV. For the latter neurons, branch point LCI was correlated (r = 0.42) with the reciprocal of the hyperpolarization level, at the cell body, required to block conduction through the branch point, suggesting that the proximity of the cell body to the branch point might play a role in determining the LCI of some neurons. Over a range of 12 °C to around 35°C, branch point LCI was inversely related and maximum firing frequency directly related to temperature. At high temperatures (30°–40°C) conduction failure occurred at sites having particularly long LCI's. It is concluded that a) these axon branch points act as lowpass filters and set the maximum frequency of conducted impulses that can access the central nervous system; b) certain varieties of DRG neurons exhibit more branch point filtering action than others; and c) warming, within limits, reduces branch point filtering action.     

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.     

Effect of temporal and spatial temperature gradients on the ampullae of Lorenzini

Summary Afferent single fiber impulses were recorded from isolated ampullae of Lorenzini of dogfishes (Scyliorhinus canicula). The ampullae were placed between two thermodes, each of which could be circulated separately with water at 12°, 18° and 24° C, thus allowing cooling and warming with various combinations of spatial temperature gradients. At constant temperature, there was a static discharge in the ampullary fibers. Cooling elicited a dynamic overshoot in frequency, followed by adaptation to a new steady state, whereas warming led to a transient inhibition. Within the limits of error the direction and slope of the spatial temperature gradient had no influence whatsoever on the static and dynamic responses of the ampullae, the only effective parameters being the temperature at the site of the receptor and the rate of temperature change with time.About 13% of the single fibers responded with bursts of impulses, interrupted by silent intervals, and 10% showed an inversed dynamic response, i.e. dynamic overshoot on warming and transient inhibition on cooling. It is possible that these patterns of activity are anomalous responses.This work was supported by the Deutsche Forschungsgemeinschaft.     

Conduction of trains of impulses in uniform myelinated fibers: Computed dependence on stimulus frequency

The conduction of trains of action potentials in myelinated fibers was studied using computer simulations based on a modification of the Hodgkin-Huxley equations. Stimulation at short but regular interstimulus intervals caused some stimuli to fail to elicit propagated action potentials.Propagated impulse trains observed close to the stimulation site, elicited by high frequency stimulus trains, took the form of ‘clusters’ of impulses, e.g. doublets or triplets. When these impulse trains were observed at distances farther from the stimulation site, interspike intervals were more uniform. For interstimulus intervals of less than 10 ms, distant intervals between impulses were relatively insensitive to the temporal patterning of impulses at the initiation zone and tended toward regular intervals corresponding to the average interstimulus intervals for propagated stimuli. This tendency toward uniform intervals between impulses was also observed for lower average frequency stimulus trains with irregular interstimulus intervals. Moreover, for the first two stimuli in a train, there was a very strong tendency toward impulse entrainment.These results indicate that intervals between impulses along unbranched myelinated axons are not fixed, but vary according to the site along the conduction pathway where they are observed. The tendency toward entrainment, and regularization of intervals, may represent a factor limiting the frequency with which interval-coded impulses are initiated.