Electroreceptor mechanisms of the ampullae of lorenzini in skates

Responses of the receptor epithelium of single electrically isolated ampullae of Lorenzini and spike responses of nerve fibers connected to them to electrical stimulation under voltage clamping conditions were studied in experiments on the Black Sea skateRaja clavata. The preparations had an input resistance of 200–800 KΩ, a transepithelial resting potential of between 0 and ?2 mV, and the usual spontaneous spike activity in their afferent fibers. Thresholds of the electroreceptors were 2–10 µV (current about 10^?11 A). Within the working range of the electroreceptors (up to ±500 µV, current up to 1 nA) the current-voltage characteristic curve of the epithelium was linear without any evidence of spike or wave activity of the receptor cells. With negative currents of over 1–10 nA a regenerative spike appeared on the epithelium and was accompanied by an uncharacteristic pattern of spike discharge of the nerve fiber. It is concluded that, contrary to Bennett's hypothesis, spike or oscillatory activity bears no relationship to normal working of electroreceptors. It is postulated that "secondarily sensitive" receptor cells share a common functional organization, which is based on a chemical synapse with high electrical sensitivity.     

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.     

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.     

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.     

Effect of dalargin,a synthetic leu-enkephalin analogue on synaptic transmission in the Lorenzini ampullae of rays

Effects of dalargin, a synthetic leu-enkephalin analogue and its antagonist naloxone on synaptic transmission in afferent synapses of ray electroreceptors were investigated using an isolated preparation of Lorenzini ampullae from Black sea rays. It was shown that dalargin (10^–6–10^–10 mole liter) both decreased background activity and evoked activity of an afferent fiber in a dose-dependent manner. Naloxone (10^–5 mole/liter) also inhibited afferent impulsation and completely blocked responses of the Lorenzini ampullae to dalargin application. L-glutamate-induced excitatory responses were reduced in the presence of dalargin. It is suggested that the modulatory action of dalargin on glutamatergic synaptic transmission in the Lorenzini ampullae is exerted via specific opiate receptors.Translated from Neirofiziologiya, Vol. 25, No. 1, pp. 18–21, January–February, 1993.     

Mode of Operation of Ampullae of Lorenzini of the Skate, Raja

Ampullae of Lorenzini are sensitive electroreceptors. Applied potentials affect receptor cells which transmit synaptically to afferent fibers. Cathodal stimuli in the ampullary lumen sometimes evoke all-or-none "receptor spikes," which are negative-going recorded in the lumen, but more frequently they evoke graded damped oscillations. Cathodal stimuli evoke nerve discharge, usually at stimulus strengths subthreshold for obvious receptor oscillations or spikes. Anodal stimuli decrease any ongoing spontaneous nerve activity. Cathodal stimuli evoke long-lasting depolarizations (generator or postsynaptic potentials) in afferent fibers. Superimposed antidromic spikes are reduced in amplitude, suggesting that the postsynaptic potentials are generated similarly to other excitatory postsynaptic potentials. Anodal stimuli evoke hyperpolarizations of nerves in preparations with tonic activity and in occasional silent preparations; presumably tonic release of excitatory transmitter is decreased. These data are explicable as follows: lumenal faces of receptor cells are tonically (but asynchronously) active generating depolarizing responses. Cathodal stimuli increase this activity, thereby leading to increased depolarization of and increased release of transmitter from serosal faces, which are inexcitable. Anodal stimuli act oppositely. Receptor spikes result from synchronized receptor cell activity. Since cathodal stimuli act directly to hyperpolarize serosal faces, strong cathodal stimuli overcome depolarizing effects of lumenal face activity and are inhibitory. Conversely, strong anodal stimuli depolarize serosal faces, thereby causing release of transmitter, and are excitatory. These properties explain several anomalous features of responses of ampullae of Lorenzini.     

Effects of quisqualate,N-methyl-D-aspartate,and some amino acid antagonists on synaptic transmission in ampullae of Lorenzini

The effects of quisqualic acid (QA), N-methyl-D-aspartate (NMDA), and a number of NMDA and non-NMDA receptor antagonists on background and induced activity in afferent nerve fibers were investigated in skates by means of bath application to the basal membrane of electroreceptors (ampullae of Lorenzini). Perfusion with physiological saline containing QA or NMDA (minimum concentrations required: 10^–8 and 10^–5 M respectively) was found to exert an excitatory effect on afferent activity. Aminoadipate and aminophosphonobutyrate had no effect on synaptic transmission, which was blocked by aminophosphonovalerate, however. Raising magnesium ion concentration (of 30 mM) led to blockade of NMDA-induced response without changing that produced by QA. Aminophosphonovalerate blocked NMDA response and partially reduced the effects of L-aspartic acid. Glutamyl glycine produced blockade of synaptic transmission. The findings obtained would point to synaptic sensitivity to the action of amino acid agonists (QA and NMDA) in the ampullae of Lorenzini.Neurocybernetics Research Institute, Rostov-on-Don. Translated from Neirofiziologiya, Vol. 21, No. 2, pp. 160–167, March–April, 1989.     

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.     

Mechanism of perception of changes in the magnetic field by ampullae of lorenzini of elasmobranchs

The mechanisms of reception of changes in the magnetic field by electroreceptor formations were investigated in experiments on Black Sea rays in which spike activity was recorded from single nerve fibers connected with the ampullae of Lorenzini. The responses of the ampullae of Lorenzini to magnetic stimulation were shown to be due to induced electric currents creating potential gradients in the body tissues of the fish and the sea water. On the basis of differences in responses of different ampullae to magnetic stimulation, it is possible to distinguish between magnetic stimuli and other stimuli acting on the electroreceptor system. Potentiation of the receptor response to magnetic stimulation was found as the fish came closer to the "shore." The mechanisms and biological importance of reception of changes in the magnetic field by the ampullae of Lorenzini are discussed.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 10, No. 1, 75–83, January–February, 1978.     

Influence of L-serine-O-phosphate on synaptic transmission in afferent synapses of the ampullae of Lorenzini of skates

The method of superfusion of the basal membranes of the ampullae of Lorenzini of skates was used to investigate the influence of L-serine-O-phosphate (SOP) on the background and evoked activity of afferent nerve fibers, as well as on the effects of application of agonists: exciting amino acids — L-glutamate (L-GLU), kainate (KA), quisqualte (Q), and N-methyl-D-aspartate (NMDA). It was found that SOP (threshold concentration 10^–7 M) had an inhibiting effect on the background and evoked activity of the nerve fibers; depending on the concentration it decreased the stimulatory effects of L-GLU and NMDA and did not change the responses due to application of KA and Q. The data obtained suggest that the effects of SOP observed in the ampullae of Lorenzini are associated with its interaction with NMDA-type amino acid receptors.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 23, No. 4, pp. 387–391, July–August, 1991.     

Effects of glutamic acid diethylester on synaptic transmission in the skate ampullae of Lorenzini

The effects on synaptic transmission of glutamic acid diethylester (GDEE), a glutamate receptor blocker, were investigated by recording spike activity from single nerve fibers in the electroreceptor cells of the skate (Raja clavata) ampullae of Lorenzini. It was found that adding GDEE to the bathing medium led to a concentration-dependent reduction in or complete blockade of background and evoked receptor activity; 10^–6 M GDEE was the minimum effective concentration. It was also shown that GDEE reversibly blocked postsynaptic response produced by excitatory amino acids: L-glutamate (L-GLU) and L-asparate (L-ASP). Findings suggest the involvement of L-GLU or a related substance in synaptic transmission in the ampullae of Lorenzini.I. P. Pavlov Institute of Physiology of the Academy of Science of the USSR, Leningrad, USSR. Translated from Neirofiziologiya, Vol. 19, No. 3, pp. 323–327, May–June, 1987.     

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.     

Effects of some agonists of excitatory amino acids on synaptic transmission in the skate electroreceptors (ampullae of Lorenzini)

The effects on synaptic transmission of blockers of amino acids at postsynaptic receptors were investigated by means of external perfusion of the basal membrane of electroreceptor cells in ampullae of Lorenzini and by recording of spike activity from individual nerve fibers in the skateRaja clavata: glutamic acid diethyl ester (DEE-GLU), glutamic acid dimethyl ester (DME-GLU), D--aminoadipic acid (DAA), kynurenic acid (KYN), and cis-2,3-piperidine dicarboxylic acid (PDA). The most effective blocker was found to be DEE-GLU, producing reversible blockade of postsynaptic amino acid response. It was found that DAA did not change synaptic transmission in the electroreceptors, while PDA largely affected response produced by applying L-aspartic acid (L-ASP); KYN affected response produced by L-glutamic acid (L-GLU). It is deduced that L-GLU and L-ASP are the most effective agonists at the afferent synapse of ampullae of Lorenzini and that their excitatory effect is produced by activating quisqualate receptors.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 20, No. 4, July–August, 1988, pp. 457–463.     

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.     

Effect of potassium ions on firing pattern of ampullae of Lorenzini in rays

The effect of a change in potassium ion concentration in the region of the basal membranes of the ampullae of Lorenzini of the thornback ray on spontaneous and evoked discharges of the receptors was investigated. A decrease in potassium ion concentration in the solution of perfusion with potassium-free solution led to a decrease in firing rate. Conversely, an increase in the potassium ion concentration caused an increase in discharge frequency followed by a decrease; thresholds of the receptors to the action of electrical stimuli were unchanged. When synaptic transmission was blocked by magnesium ions, an increase in the potassium ion concentration did not cause the appearance of activity in nerve fibers. If, however, activity of the nerve fibers in solution with a high magnesium ion concentration was restored with L-glutamic acid (10^–4 M), an increase in the potassium ion concentration caused an increase in firing rate. The role of potassium ions in the activity of receptors of the lateral-line system is discussed.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 16, No. 4, pp. 493–497, July–August, 1984.     

Electrophysiological investigation of central neurons of the electroreceptor system of the skate

Bioelectrical responses of acoustico-lateral neurons to electrical stimulation of the ampullae of Lorenzini were investigated in acute experiments on the anesthetized Black Sea skateTrigon pastinaca. Three types of responses were found: a primary composite response, prolonged activity, and single unit activity. Excitation of the neurons corresponded to a more marked negative phase, and inhibition to a more marked positive phase of the primary response. The thresholds of the unit responses to adequate electrical stimulation were 10^–9–10^–10 A/mm² and the minimal latent period 20 msec. The spontaneous activity of some neurons clearly depended on the animal's respiration. The character of the response depended on stimulus polarity, as reflected in the appearance of on- and off-responses. A tonic type of response with features of adaptation was predominant. The dependence of some response parameters (latent period of on- and off-responses, firing rate, duration of the contrast interval, response thresholds) on those of the stimulus is analyzed. The mechanisms of these bioelectrical responses are discussed.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol.6, No.1, pp.59–67, January–February, 1974.     

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.     

Effects of divalent ions and drugs on synaptic transmission in phasic electroreceptors in a mormyrid fish

We recorded impulses in afferent nerve fibers innervating two kinds of phasic electroreceptors in a mormyrid fish. We used an isolated preparation of skin, receptors, and sensory nerves to estimate synaptic delays, and to change solution in contact with the receptor-nerve synapse. The minimum delays between stimuli and sensory nerve responses, which must be slightly larger than synaptic delays, are about 0.7 msec in medium receptors and about 0.25 msec in large receptors. This result supports previous suggestions that transmission is chemically mediated in medium receptors and electrically mediated in large receptors. Furthermore, Mg⁺² depresses synaptic transmission in medium receptors, and has little effect on transmission in large receptors. A complex dependence of response on both Mg⁺² and Ca⁺² masks divalent ion dependence of transmission, but a large excess of Mg⁺² cannot completely block transmission in medium electroreceptors. L-glutamate, and not cholinergic drugs, produces a sequence of excitation and depression of medium receptor response which indicates that a similar chemical is the transmitter in the afferent synapse.     

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.     

Responses of the ampullae of Lorenzini in a uniform electric field

A linear relationship was established by analysis of discharges from electroreceptors of the ampullae of Lorenzini in a uniform electric field between the potential difference on a single ampulla and the relative change in the spike response of a single fiber. This relationship can serve as the basis for a model of activity of ampullary groups considered as functional units of the electroreceptor system.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 11, No. 2, pp. 158–166, March–April, 1979.