Electrophysiological investigation of the properties of the electroreceptors (ampullae of Lorenzini) in Black Sea rays

Responses of electroreceptors (ampullae of Lorenzini) in Black Sea rays to electrical stimuli were recorded in vivo as spike activity of single nerve fibers. Depending on their functional properties the fibers could be divided into silent, those with regular activity (10–15 spikes/sec) and those with grouped activity. Electrical stimuli evoked a tonic response with a varied degree of adaptation in the nerve fibers. The threshold currents were between 10^?10 and 10^?11 A/mm². The minimal latent period of the on-responses to pulses of current of maximal intensity was 15–40 msec, whereas that of the off-responses was 15–200 msec. The effect of intensity, duration, and polarity of the stimuli on the responses of the receptors and the adaptation of the electroreceptors during application of a steady current were investigated. The properties of the ampullae of Lorenzini were compared with those of other types of electroreceptors.     

Functional properties of lamprey electroreceptors

Spike discharges in nerve fibers, evoked by stimulation of electroreceptors by an electric field directed along the body axis (square pulses of current and a sinusoidal current) were recorded in the lampreyLamperta fluviatilis (L.). Excitation of electroreceptors was shown to arise through the action of the cathode. Minimal values of electric field at which appreciable changes took place in spike activity were 10–60 µV/cm for different nerve fibers. The optimal frequency range of sinusoidal electrical stimulation was 0.05–0.5 Hz. It is suggested that electroreceptors of the Agnatha (caudata) and of gnathostomatous cartilaginous fish share a common origin.Murmansk Marine Biological Institute, Kola Branch, Academy of Sciences of the USSR, Dal'nie Zelentsy, Murmansk Region. Translated from Neirofizioloigya, Vol. 16, No. 1, pp. 105–110, January–February, 1984.     

Functional features of electroreceptors (small pit organs) in the catfish

Characteristics of responses of the small pit organs of the catfishIctalurus nebulosus to the action of electrical stimuli of varied polarity, intensity, and duration were studied. Single fibers of the lateral nerve innervating these organs possessed regular spontaneous activity with a frequency of 35–45/sec or grouped activity, coinciding with the rhythm of the animal's swimming movements. Threshold current densities varied from 10⁻¹¹ to 10⁻¹⁰ A/mm². Electrical stimuli evoked a phasic-tonic response of the receptor. The latent period was 10–50 msec for on-responses and 10–200 msec for off-responses. In the presence of strong electric fields the receptor responded to a cathodal stimulus by excitation, whereas under ordinary experimental conditions an anodal stimulus is excitatory. The properties of small pit organs are compared with the characteristics of other electroreceptors.     

Functional characteristics of electroreceptors of the Turkestan catfish

Acute experiments to record spike activity from single fibers of the lateral line nerve of the Turkestan catfish revealed electroreceptor formations which, in their functional characteristics, were similar to the ampullated electroreceptors of other freshwater fish (the so-called small pit organs). The threshold intensity of the uniform electric field was 1 µV/cm. A voltage drop on the skin of the fish was shown to be an effective stimulus for the electroreceptors. A spike response to a change in the magnetic field was found for the first time in electroreceptors of freshwater fish. The threshold level of magnetic induction for a velocity of rotation of the permanent magnet of 1 m/sec was 2.9 · 10^–4 T. Temperature and mechanical sensitivity of the electroreceptors was determined. The biological significance of electroreceptors of the Turkestan catfish is discussed.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. M. I. Kalinin Andizhan Medical Institute, Ministry of Health of the Uzbek SSR. S. M. Kirov Murmansk Marine Biological Institute, Kola Branch, Academy of Sciences of the USSR, Dal'nie Zelentsy. Translated from Neirofiziologiya, Vol. 12, No. 5, pp. 508–516, September–October, 1980.     

Cutaneous mechanism of electroreceptor temperature sensitivity of the ampullae of Lorenzini

The potential difference on the receptor epithelium of the ampullae of Lorenzini and on the skin and also spike discharges of single electroreceptor nerve fibers in response to temperature stimulation of the region of the pores of the ampullae were studied in the Black Sea skateRaja clavata. Heating the skin in the region of the pore led to the appearance of a positive potential on the skin and on the epithelium of the ampulla, and to inhibition of spike activity. The time course of the change in potential reflected the course of change of temperature; the temperature coefficient was 100–150 µV/°C. Cooling the skin was accompanied by a negative deviation of potential on the skin and in the ampullary canal and by excitation of spike activity. During cooling the temperature coefficient was 30–50 µV/°C. It is concluded that spike activity of electroreceptors reflects changes in potential on the skin due to changes in temperature. The mechanism and biological significance of the phenomena discovered are discussed.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 13, No. 3, pp. 307–314, May–June, 1981.     

Electrical activity and structural correlates of giant nerve fibers in Kuruma shrimp (Penaeus japonicus)

Morphology and recordings of electrical activity of Kuruma shrimp (Penaeus japonicus) giant medullated nerve fibers were carried out. A pair of giant fibers with external diameter of about 120 μ and 10 μ in myelin thickness were found in the ventral nerve cord. The diameter of the axon is about 10 μ. Thus there is a wide gap between the axon and the external myelin sheath. Each axon is doubly coated directly by Schwann cells and indirectly by the myelin sheath layer which is produced by those Schwann cells. Impulse conduction velocities of these giant fibers showed a range between 90–210 m/sec at about 22°C. Large action potentials (up to 113 mV, rise time of 0.16–0.3 msec, maximum rate of rise of 650–1250 V/sec, half decay time of 0.2–0.3 msec, maximum rate of fall of 250–450 V/sec and total duration of less than 1.5 msec) could be obtained by inserting microelectrodes or by longitudinal insertion of 25 μ diameter capillary electrodes into the gap but no DC-potential difference was observed across the myelin sheath. Transmyelin electrical parameters were very favorable for fast impulse conduction: myelin resistance of 3 × 10⁴ Ω cm²; time constant of 0.38 msec; myelin capacitance of 1.35 × 10^?8 F/cm²; gap fluid resistivity of 23 Ω cm. The existence of nodes of Ranvier could not be demonstrated morphologically, but electrophysiological evidence suggests that a type of saltatory conduction occurs in these giant fibers.     

Investigation of the mechanism of temperature sensitivity of the electroreceptors of ampullae of lorenzini

In experiments on Black Sea skates (Raja clavata), the potential of the receptor epithelium of the ampullae of Lorenzini and spike activity of single nerve fibers connected to them were investigated during electrical and temperature stimulation. Usually the potential within the canal was between 0 and –2 mV, and the input resistance of the ampulla 250–400 k. Heating of the region of the receptor epithelium was accompanied by a negative wave of potential, an increase in input resistance, and inhibition of spike activity. With worsening of the animal's condition the transepithelial potential became positive (up to +10 mV) but the input resistance of the ampulla during stimulation with a positive current was nonlinear in some cases: a regenerative spike of positive polarity appeared in the channel. During heating, the spike response was sometimes reversed in sign. It is suggested that fluctuations of the transepithelial potential and spike responses to temperature stimulation reflect changes in the potential difference on the basal membrane of the receptor cells, which is described by a relationship of the Nernst's or Goldman's equation type.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. I. M. Sechenov, Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Pacific Institute of Oceanology, Far Eastern Scientific Center, Academy of Sciences of the USSR, Vladivostok. Translated from Neirofiziologiya, Vol. 12, No. 1, pp. 67–74, January–February, 1980.     

Effects of kainic acid on synaptic transmission in skate electroreceptors (ampullae of Lorenzini)

The effects of kainic acid on synaptic transmission in electroreceptors were investigated in the skate using techniques of uninterrupted superfusion of the synaptic area with a solution containing this substance and then recording the spike activity of single nerve fibers of the ampullae of Lorenzini. Kainic acid at threshold concentrations of the order of 10^–9 M effectively changed spontaneous and evoked activity of the receptors. Level of background activity served as an indication of the effects taking place. During blockage of synaptic transmission produced by magnesium ions the addition of kainic acid to the magnesium-saturated solution restored both spontaneous and evoked activity. It was deduced that the action of kainic acid on skate electroreceptors is of a primarily presynaptic nature.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 18, No. 2, pp. 147–153, March–April, 1986.     

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

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.     

Effects of aspartic acid on skate electroreceptors

The effects of L-aspartic acid (L-ASP) on spontaneous and evoked activity in afferent nerve fibers were investigated by perfusing the basal membrane of sea skate electroreceptors (the ampullae of Lorenzini) with this substance. It was found that perfusion with physiological saline containing L-ASP exerted a primarily excitatory effect on afferent activity (threshold concentration: 10^–7 M). When synaptic transmission was blocked by magnesium ions, activity was restored in the afferent fibers if L-ASP was added to the solution and spike activity persisted for longer; this would imply the presence of desensitizing processes in the postsynaptic receptors of the ampullae. Finding would lead to the conclusion that L-ASP and L-glutamate fulfill a set of criteria for likely neurotransmitters in the ampullae of Lorenzini.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 19, No. 1, pp. 61–67, January–February, 1987.     

Reception of millimeter-band electromagnetic radiation by the ampullae of Lorenzini of skates

During recording of impulse activity from single nerve fibers of electroreceptors of the ampullae of Lorenzini of skates, we studied the responses to electromagnetic radiation (EMR) at a frequency of 37–55 GHz and an intensity of 1–100 mW/cm².Exposure of the ampullar canal pore to EMR at an intensity of 1–5 mW/cm² and a distance of 1–10 mm evoked a transient increase in the frequency of low-threshold receptor activity (current threshold was 0.04–0.2 µA). An increase in EMR intensity by more than 8–10 mW/cm² produced, together with elevation of receptor activity, an inhibition due to a rise in temperature of 1–3°C in the region exposed. The phase of increase in frequency of activity was absent in high current-threshold receptors (0.3–2.0 µA) when exposed to EMR. The receptors responded to irradiation of the ampullar canal pore at a distance of 15–20 mm by an increase in discharge frequency for 20 min. Direct irradiation of the ampullae of Lorenzini induced only inhibitory responses in receptor cells regardless of their excitability.The results obtained indicate that the sensory receptors of vertebrates are sensitive to EMR. It is concluded that the excitatory effects are due to direct reception of EMR by electroreceptors, and the inhibitory effects are related to local heating of the Lorenzini ampullar pore.Neirofiziologiya/Neurophysiology, Vol. 25, No. 5, pp. 325–329, September–October, 1993.     

Transduction and transmission in ampullary electroreceptors of catfish

• 1.1. Transduction and transmission in catfish ampullary electroreceptors is mediated by sensory cells bearing microvilli, chemically mediating synapses, nerve terminals and one axon. Although some aspects still remain to be clarified, a number of properties have been found.
• 2.2. Spike generation per seand the modulation of spike frequency by electrical stimuli behave differently with respect to a number of experimental factors.
• 3.3. Stimulus current enters presumably through non-voltage-sensitive or non-specific ion channels.
• 4.4. Fluctuations of the spike frequency may be used as a measure for proper functioning of this sense organ.

     

Radular mechanosensory neuron in the buccal ganglia of the terrestrial slug,Incilaria fruhstorferi

A radular mechanosensory neuron, RM, was identified in the buccal ganglia of Incilaria fruhstorferi. Fine neurites ramified bilaterally in the buccal ganglia, and main neurites entered the subradular epithelium via buccal nerve 3 (n3). When the radula was distorted by bending, RM produced an afferent spike which was preceded by an axonic spike recorded at n3. The response of RM to radular distortion was observed even in the absence of Ca²⁺, which drastically suppressed chemical synaptic interactions. Therefore, RM was concluded to be a primary radular mechanoreceptor.During rhythmic buccal motor activity induced by food or electrical stimulation of the cerebrobuccal connective, RM received excitatory input during the radular retraction phase. In the isolated buccal ganglia connected to the radula via n3s, the afferent spike, which had been evoked by electrical stimulation of the subradular epithelium, was broadened with the phasic excitatory input. Since the afferent spike was also broadened by current injection into the soma, depolarization due to the phasic input may have produced the spike broadening.Spike broadening was also observed during repetitive firing evoked by current injection. The amplitude of the excitatory postsynaptic potential in a follower neuron increased depending on the spike broadening of RM.Abbreviations CBC cerebrobuccal connective - EPSP excitatory postsynaptic potential - n1,n3 buccal nerves 1 and 3 - RBMA rhythmic buccal motor activity - RM radular mechanosensory neuron - SMT supramedian radular tensor neuron     

Electrical current and cAMP induce lateral branching in the stolon of hydroids

Pulses of cAMP injected ionophoretically or mechanically into the epidermis of the stolon of the hydroid Hydractinia induce lateral branching at the site of stimulation. Up to 72% of the punctured loci developed a bud 6–24 hr after stimulation. Only pulsatile injection in periods of, e.g., 5 min is effective in inducing lateral buds. Controls provided evidence that in the ionophoretic mode the inducing effect derives not only from the cAMP signal but also, in part, from the positive electric current passed through the micropipet during the retention interval: DC (e.g., 8 nA × 1 hr or 20 nA × 2 hr) entering the tissue also evokes a positive response. Additional pulses of cAMP, but not of AMP, enhance the current effect. The threshold dose for a significant amplification has been determined to be 3.6 × 10^?13M (18 pulses à 2 × 10^?14M).     

Changes in the duration of the electric response of single nerve fibers following repetitive stimulation

Single nerve fibers were isolated from the nerve innervating the sartorius or semitendinosus muscle of the toad (Bufo marinus). Single nerve fiber responses were recorded with three arrangements of the "bridge insulator" method. During stimulation at 50 to 150 pulses per second for 20 to 140 minutes the spike duration was progressively increased. After tetanization the spike duration usually continued to increase at a more rapid rate. Within 5 to 60 minutes further prolongation stopped and within 1 to 10 hours the spike duration was normal. The duration of the response of tetanized fibers was from 2.5 to more than 10 times the spike duration of untetanized fibers. Prolongation was observed in nerve fibers isolated from nerves tetanized in vivo.     

Electrical model of the electroreceptor of the ampulla of Lorenzini

On the basis of experimental data [2] a model of electrical processes taking place on the receptor epithelium of the ampulla of Lorenzini was developed. The basic assumption made in the model is that the apical membrane of the receptor cell has a stationary current-voltage characteristic curve with a region of negative resistance. The model explains logically the unusual sign of the spike response of the ampullae (excitation on application of a cathode to the apical surface of the epithelium) and experimental data obtained by various workers [2,7–10], including some concerned with the most complex forms of electrical and spike responses.     

Temperature effects on the tympanal membrane and auditory receptor neurons in the locust

Poikilothermic animals are affected by variations in environmental temperature, as the basic properties of nerve cells and muscles are altered. Nevertheless, insect sensory systems, such as the auditory system, need to function effectively over a wide range of temperatures, as sudden changes of up to 10 °C or more are common. We investigated the performance of auditory receptor neurons and properties of the tympanal membrane of Locusta migratoria in response to temperature changes. Intracellular recordings of receptors at two temperatures (21 and 28 °C) revealed a moderate increase in spike rate with a mean Q10 of 1.4. With rising temperature, the spike rate–intensity–functions exhibited small decreases in thresholds and expansions of the dynamic range, while spike durations decreased. Tympanal membrane displacement, investigated using microscanning laser vibrometry, exhibited a small temperature effect, with a Q10 of 1.2. These findings suggest that locusts are affected by shifts in temperature at the periphery of the auditory pathway, but the effects on spike rate, sensitivity, and tympanal membrane displacement are small. Robust encoding of acoustic signals by only slightly temperature-dependent receptor neurons and almost temperature-independent tympanal membrane properties might enable locusts and grasshoppers to reliably identify sounds in spite of changes of their body temperature.     

Analysis of the modulating effect of catecholamines on electrogenesis in an isolated mechanoreceptor

Perfusion of isolated Pacinian corpuslces in the cat mesentery with solutions of dibutyryl-cAMP or theophylline caused an increase in spike activity against the background of a reduction in amplitude of receptor potentials and lowering of the threshold for spike generation. The opposite effect on mechanoreceptor electrical responses was found when catecholamines were used. It was postulated on the basis of these findings that the action of catecholamines on Pacinian corpuscles is accompanied by a fall in the cAMP level in the sensory nerve terminal. Noradrenalin caused a decrease in adenylate cyclase activity in receptor homogenates. The activating effect of noradrenalin on Na⁺, K⁺-ATPase, abolished by phentolamine but unchanged by propranolol, was demonstrated. The possible role of -adrenoreceptors in the modulating effect of catecholamines on electrical activity of Pacinian corpuscles is discussed.S. V. Kurashov Medical Institute, Ministry of Health of the RSFSR, Kazan'. Translated from Neirofiziologiya, Vol. 14, No. 2, pp. 158–163, March–April, 1982.     

Investigation of mechanisms of synaptic transmission in ampullae of Lorenzini in the skate

The effect of magnesium ions, L-glutamate (L-GLU), and the diethyl ester of glutamic acid (DEE-GLU) on temperature and electrical sensitivity of the ampullae of Lorenzini in skates was studied by the method of perfusion of the basal membrane of electroreceptor cells and recording spike activity from single nerve fibers. Addition of 10^–4–10^–5 M L-GLU to the solution was shown to cause an increase in the spontaneous discharge frequency of receptors with low initial level of activity (8–20 spikes/sec) and a decrease in receptors with spontaneous activity of 22–42 spikes/sec. In solution with an increased magnesium ion concentration (15–50 mM) both spontaneous and evoked receptor activity was blocked, Under these conditions the addition of L-GLU to the solution caused partial recovery of spontaneous receptor activity. Reversible blocking of spontaneous and evoked receptor activity was observed in a solution containing 10^–4–10^–3 M DEE-GLU. It is suggested that L-GLU is the synaptic transmitter in the ampullae of Lorenzini of the skate.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 13, No. 3, pp. 292–298, May–June, 1981.