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First published online August 22, 2008
Journal of Experimental Biology 211, 2876-2888 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018515

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Hydrozoan nematocytes send and receive synaptic signals induced by mechano-chemical stimuli

Dominik Oliver^*, Martin Brinkmann, Thiemo Sieger and Ulrich Thurm

Institute for Neurobiology and Behavioral Biology, University of Münster, Badestr. 9, D-48149 Münster, Germany

View larger version (6K): [in this window] [in a new window]   Fig. 1. Schematic diagram of an isolated capitate tentacle arranged for stimulation of a nematocyte or sensory hair cell and synchronous intracellular recording from a distant nematocyte. The tentacular sphere is held by a suction capillary. , angle between stimulated and recorded cells; CA, cnidocil apparatus; CC, cnidocyst; CP, cytoplasm of nematocyte.

View larger version (19K): [in this window] [in a new window]   Fig. 2. L-potentials in nematocytes. Upper trace of each record: membrane voltage; lower trace: stimulatory excursion of the probe. (A,B) L-potentials induced by deflections of the hair bundle of a sensory hair cell at two different time scales (a,b). (A) in Stauridiosarsia hair deflection was 28°; a pre-impulse was used to guarantee synchronous starts of the probe and the hair at the second step. The first response in Aa is superimposed by a T-potential (arrow; see Fig. 4). (B) L-potentials in Coryne induced by hair deflection of +10° (Ba, 1) and –9° (opposite direction, Ba, 2). (C,D) L-potentials induced by deflections of the cnidocil apparatus of a distant nematocyte in Stauridiosarsia; responses from the same pair of cells in C and D; (C) without, (D) with discharge of the cnidocyst of the stimulated cell. The responses in Ca and Da are shown on an enlarged time scale in Cb and Db. Note shortening of latency of L-potential from 15 ms (C) to 2.6 ms (D). T-potentials are superimposed in D (arrows). (E,F) Responses of nematocytes of Stauridiosarsia to transepithelial electrical stimulation at the site of a distant nematocyte. The duration of the voltage step stimuli is indicated by a bar beneath the responses and is reflected in the recorded voltage by distorted rectangles. (E) Four superimposed responses to impulses (Stimulus) of equal duration with positive sign at the cell surface (depolarizing the basolateral membrane); two impulses were of 100 mV, 2 of 120 mV amplitude. One stimulus of each amplitude induced an L-potential; the highest was induced by a 100 mV impulse (latencies 20 and 48 ms). (F) Two superimposed responses to impulses with negative sign at the distant cell surface (depolarizing the apical membrane): the smaller impulse (–40 mV) did not induce a response; the larger (–60 mV) elicited the discharge of the stimulated nematocyte and induced a corresponding large L-potential (latency 10 ms) of long duration, superimposed by two T-potentials. (The small peak-amplitude of the L-potential corresponds to the small membrane voltage of the recorded cell. At the peak the membrane became depolarized to the usual range, about –25 mV, as found in D.)

View larger version (31K): [in this window] [in a new window]   Fig. 3. (A) Series of L-potentials induced in the same nematocyte by chemo-mechanically stimulating the cnidocil apparatus of a distant nematocyte (saturating amplitude). Time intervals between records as indicated. The stimuli 1–4 and 6 (left to right) stimulated the same cell (cell I) but stimulus 5 deflected the cnidocil apparatus of another nematocyte (stimulated cell II) and induced the discharge of its cyst. Thin arrows indicate T-potentials. The initial phases of the responses and stimuli in Aa are shown on an enlarged time scale in Ab. Note the trend in the amplitudes of the L-potentials and the correlated changes in their latencies. (B) Amplitudes of L-potentials plotted against the latencies of the same responses; both axes with logarithmic scales. Values of L-potentials that occurred associated with discharge of the cyst of the stimulated cell are marked by open symbols (N=136), those that occurred without cyst-discharge (N=164) are marked by filled symbols. Open and filled triangles represent potentials induced by purely mechanical stimuli; open and filled squares represent those induced by combined chemo-mechanical stimuli. Values are from 222 stimulated cells. (C) Peak voltages of L-potentials of three recorded cells (series as in A), plotted against the latency of the same responses. Each recorded cell is represented by one symbol (square, triangle or diamond), each pair of a stimulated and a recorded cell by a roman number. Data points of series I–II are from records shown in A. Filled symbols represent responses accompanied by the discharge of the cyst of the stimulated cell; open symbols represent responses not accompanied by discharge. Resting voltages of the recorded cells as indicated. Values of r are correlation coefficients; lines indicate linear regression. Differences between absolute peak voltages of discharge associated L-potentials are smaller than the amplitudes. (D) L-potentials induced in the same nematocyte (Stauridiosarsia) by chemo-mechanical stimulation of other nematocytes that diverged from the recorded cell by the angles , given above the records. Each of these responses was associated with cyst discharge of the stimulated cell. The rising phase of each response and stimulus shown in Da is shown at higher time resolution in Db.

View larger version (27K): [in this window] [in a new window]   Fig. 4. T-potentials in nematocytes of Stauridiosarsia (A–C,F–H), Coryne (D) and Dipurena (E). Membrane voltage (upper traces) and probe excursion (lower traces) as in Fig. 2. (A) T-potentials induced by contacts of the probe with an area of the tentacle distant from nematocytes; the first response of Aa is enlarged in Ab. (B) A hyper-/re-polarizing component was observable at depolarizing membrane voltage. (C–E) Representative waveforms of T-potentials recorded from nematocytes of Stauridiosarsia (C), Coryne (D), and Dipurena (E). E 2 shows the superposition of L- and T-potentials, typically occurring in Dipurena upon mechanical stimulation of nematocytes or, here, pulling at the stinging thread of a discharged nematocyst. (F 1,2) Series of T-potentials following an L-potential that was induced by a discharge-triggering stimulation of a distant nematocyte; F 2 is a section of the same `tail' of T-potentials, recorded 1 min after F 1. (G) Time course of amplitude and instantaneous frequency of the series of T-potentials illustrated in F. (H) Mean (± s.d.) of the hyperpolarizing component of T-potentials as a function of the instantaneous frequency of preceding T-potentials (intervals averaging 20 s; N=number of trials).

View larger version (18K): [in this window] [in a new window]   Fig. 5. Membrane currents of L- and T-responses of nematocytes. (Aa, Ba) Two L-responses of the same nematocyte (voltage-clamped near the resting potential) induced by deflections of the same cnidocil apparatus of a distant nematocyte with a time interval of 0.6 s. The L-response in B was associated with cyst discharge of the stimulated cell. T-events occurred superimposed on the L-responses. Lower traces: probe excursions (the small second excursions did not reach the cnidocil). (Ab, Bb) Higher time resolution of the initial phases of the responses. Note the earlier and steeper start of the L-response in B. (C) Membrane currents of T-events recorded when the membrane voltage was clamped at –70 mV. (D) T-currents at various clamped membrane voltages; voltages indicated next to the traces. Arrowheads indicate steps of outward current at reversed membrane voltages. Note sign reversal of the current at clamped –10 mV. (E) Amplitudes of T-currents as a function of clamped membrane voltage. Filled circles indicate the second outward current component of two-phase events. The straight line indicates a linear fit to the data. All records from Stauridiosarsia.

View larger version (24K): [in this window] [in a new window]   Fig. 6. Voltage sensitivity of nematocytes in the absence of chemical sensitization. (A) Voltage responses of a nematocyte from Stauridiosarsia to depolarizing current steps, increased in increments of 0.25 nA, starting from –100 mV. At depolarizations above –10 mV a regenerative action potential is elicited. (B) Typical action potential at a threshold of –8 mV, induced by current injection. (C) Voltage responses of a nematocyte from Dipurena to depolarizing current steps, increased in increments of 0.5 nA, starting from resting voltage. At about –40 mV a regenerative, persistent depolarization is triggered, while an action potential occurs at a threshold close to 0 mV. (D) Membrane currents from a Stauridiosarsia nematocyte recorded in discontinuous voltage-clamp mode in response to voltage steps in increments of 10 mV, starting from –70 mV (data are shown with linear leak currents subtracted). (E) Membrane currents from D as a function of membrane potential: steady-state currents (open symbols) are compared to transient values (filled symbols). Transient inward currents activate at about –10 mV, matching the action potentials threshold.

View larger version (15K): [in this window] [in a new window]   Fig. 7. Ionic dependence of T- and L-potentials. (A) T-potentials during substitution of sodium in ASW by choline and after restitution of ASW. Data below the traces indicate time after exchange of solution. (B) T-potentials during superfusion with `0 Ca2+-ASW' (i.e. no Ca2+ added) and subsequent exchange with regular ASW. Data below records as in A. (C) L- and superimposed T-potentials during superfusion with ASW containing 1 mmol l–1 Ca2+ and double the Mg2+ concentration (96 mmol l–1 Mg2+); highest response amplitude recorded immediately before switching to the test medium; progressively reduced amplitudes recorded at 3, 4 and 5 min of superfusion by the test medium. Records from Dipurena. Lower trace: excursion of the stimulus probe pulling at a stinging thread of a discharged nematocyst. (D) Effect of reduced Mg2+ concentration on T-potentials: upper trace before, lower trace 1 min after reduction of [Mg2+] to 10% (5 mmol l–1) in ASW. All records except those in C from Stauridiosarsia.

View larger version (19K): [in this window] [in a new window]   Fig. 8. Effects of transmitter agonists and antagonists on L- and T-potentials. All recordings from Dipurena. (Aa) Effect of glutamate (50 mmol l–1 sodium glutamate) on resting potential (continuous line) and amplitude of superimposed LT-potentials (circles and dotted line). Superfusion with glutamate-ASW as indicated. (Ab) Records of superimposed LT-potentials: (1) before, (2) during, (3) after the application of glutamate. (Ba) Effect of NS102 (5 µmol l–1, with 0.025% DMSO), a blocker of kainate glutamate receptors, on the amplitude of superimposed LT-potentials of two nematocytes (filled circles and triangles). A third cell (control; open triangles) exposed to 0.025% DMSO only in ASW. Re-impaling the second cell (filled triangles) after wash-out of the blocker tested the reversibility of its action. (Bb) LT-potentials of the first cell recorded 20–32 min (data given below the records) after start of superfusion with NS102; recorded at the times indicated in Ba. The resting potential remained constant at –62 mV. (C) T-potentials recorded before (1), 5 min after the start (2), and 5 min after the end (3) of superfusion with mecamylamine (10 µmol l–1). (D) T-potential recorded during superfusion with physostigmine (100 µmol l–1). Prior to application of physostigmine, the amplitude of the hyperpolarizing component was 5 mV, analogue to C 1.

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