Morphology of the ampullae of Lorenzini in juvenile freshwater Carcharhinus leucas

Ampullae of Lorenzini were examined from juvenile Carcharhinus leucas (831–1,045 mm total length) captured from freshwater regions of the Brisbane River. The ampullary organ structure differs from all other previously described ampullae in the canal wall structure, the general shape of the ampullary canal, and the apically nucleated supportive cells. Ampullary pores of 140–205 µm in diameter are distributed over the surface of the head region with 2,681 and 2,913 pores present in two sharks that were studied in detail. The primary variation of the ampullary organs appears in the canal epithelial cells which occur as either flattened squamous epithelial cells or a second form of pseudostratified contour‐ridged epithelial cells; both cell types appear to release material into the ampullary lumen. Secondarily, this ampullary canal varies due to involuted walls that form a clover‐like canal wall structure. At the proximal end of the canal, contour‐ridged cells abut a narrow region of cuboidal epithelial cells that verge on the constant, six alveolar sacs of the ampulla. The alveolar sacs contain numerous receptor and supportive cells bound by tight junctions and desmosomes. Pear‐shaped receptor cells that possess a single apical kinocilium are connected basally by unmyelinated neural boutons. Opposed to previously described ampullae of Lorenzini, the supportive cells have an apical nucleus, possess a low number of microvilli, and form a unique, jagged alveolar wall. A centrally positioned centrum cap of cuboidal epithelial cells overlies a primary afferent lateral line nerve. J. Morphol. 276:481–493, 2015. © 2014 Wiley Periodicals, Inc.     

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.     

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.     

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.     

Morphological comparison of the ampullae of Lorenzini of three sympatric benthic rays

This study investigated and compared the morphology of the electrosensory system of three species of benthic rays. Neotrygon trigonoides, Hemitrygon fluviorum and Maculabatis toshi inhabit similar habitats within Moreton Bay, Queensland, Australia. Like all elasmobranchs, they possess the ability to detect weak electrical fields using their ampullae of Lorenzini. Macroscopically, the ampullary organs of all three species are aggregated in three bilaterally paired clusters: the mandibular, hyoid and superficial ophthalmic clusters. The hyoid and superficial ophthalmic clusters of ampullae arise from both dorsal and ventral ampullary pores. The dorsal pores are typically larger than the ventral pores in all three species, except for the posterior ventral pores of the hyoid grouping. Ampullary canals arising from the hyoid cluster possessed a quasi‐sinusoidal shape, but otherwise appeared similar to the canals described for other elasmobranchs. Ultrastructure of the ampullae of Lorenzini of the three species was studied using a combination of light, confocal and electron microscopy. All possess ampullae of the alveolar type. In N. trigonoides and M. toshi, each ampullary canal terminates in three to five sensory chambers, each comprising several alveoli lined with receptor and supportive cells and eight to 11 sensory chambers in H. fluviorum. Receptor cells of all three species possess a similar organization to those of other elasmobranchs and were enveloped by large, apically nucleated supportive cells protruding well into the alveolar sacs. The luminally extended chassis of supportive cells protruding dramatically into the ampullary lumen had not previously been documented for any elasmobranch species.     

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.     

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.     

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.     

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.     

Changes in transepithelial potential and spike responses of ampullae of Lorenzini of the skate to temperature stimulation

Response of the sensory epithelium of single ampullae of Lorenzini and spike responses of nerve fibers connected to them to temperature stimulation of the region of the sensory epithelium were studied in experiments on Black Sea skatesRaja clavata. Electrically isolated ampullae with input resistance R=500–800 k, to which an external load (a controllable resistance R_ext) could be connected through a feedback circuit, were investigated. Heating the ampulla was accompanied by the appearance of a negative potential in the canal, and other conditions being the same, its magnitude was an almost linear function of the resultant inward resistance of the preparation [R_in=(R_a·R_ext)/(R_a+R_ext)]. The character and intensity of the spike response of the nerve fiber also was determined by the magnitude of R_in. With a resistance of more than 400–500 k, quickening of spike activity occurred in response to heating, and the degree of quickening increased with an increase in R_in. With a smaller value of R_in, the discharge was inhibited, and the inhibition strengthened as the resistance decreased. The presence of two sources of potential, evoked by a change of temperature and giving rise to opposite spike responses, is 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. 14, No. 1, pp. 11–18, January–February, 1982.     

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.     

A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces,Rajoidei)

A comparison of the ampullae of Lorenzini among 40 species of skates (Rajoidei) demonstrates a close relationship between inferred electroreceptive capabilities and feeding mechanisms. Three general lines of morphological modifications are noted. (1) Whereas the majority of ampullary pores are located on the ventral surface of the dorsoventrally flattened body, the relative proportion of ventral pores is significantly lower on species inhabiting aphotic waters. (2) The ventral pores on more piscivorous species are distributed over a larger portion of body surface than they are on those species that feed primarily on invertebrates. Ventral pores in this latter group are more noticeably concentrated around the mouth and their densities on the adult are inversely related to the overall mobility of preferred prey species. (3) The size of each ampulla and the number of alveoli associated with it are directly related to the habitat depth occupied by each species. Shallow-water species have smaller ampullae with fewer alveoli than deeper-dwelling (> 1,000 m) species. The general distribution of ampullary pores on deep dwelling rajoids appears to compensate for reduced visual input, whereas their relative densities are a measure of the system's resolution and reflect major differences in feeding strategies. The increased ampullary size and complexity observed in deep-sea rajoids provides mechanisms to increase both the sensitivity and signal-to-noise ratios.     

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.     

Effects of excitatory amino acid antagonists on synaptic transmission in the ampullae of Lorenzini of the skate Raja clavata

Summary The spectral sensitivity of the ocellus in the cucumber looper moth, Anadevidia peponis, was investigated by recording electroretinograms (ERGs). The peak sensitivities were observed at 340 nm in the ultraviolet and at 520–540 nm in the green. Selective spectral adaptation revealed the existence of at least two receptor types in the ocellar retina. The ratio of green to ultraviolet sensitivities for an ocellus whose ocellar nerve was cut was higher than that for an intact ocellus. It is suggested that efferent signals which control the spectral sensitivity of the ocellus are present in the ocellar nerve.Abbreviations ERG electroretinogram - GR/UV green to ultraviolet sensitivities - ON ocellar nerve     

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

1. Effects of kainic acid (KA) on resting and evoked activities of the ampullary electroreceptor were studied in marine skates (Raja clavata). 2. Perfusion of the basal membrane with 10(-6)-10(-9) M KA produced significant and reversible changes in impulse activity depending on initial firing rate. 3. When synaptic transmission was blocked by perfusion with elevated Mg2+, the resting and evoked activities were restored if KA was added. 4. The results are consistent with the view that KA is a potent excitant of the ampullae receptors and its effects appear to be presynaptic.