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First published online October 10, 2003

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Electrical activity of caudal neurosecretory neurons in seawater- and freshwater-adapted flounder: responses to cholinergic agonists

M. J. Brierley, A. J. Ashworth, T. P. Craven, M. Woodburn, J. R. Banks, W. Lu, D. Riccardi, R. J. Balment and C. R. McCrohan^*

School of Biological Sciences, University of Manchester, Manchester M13 9PT, UK

View larger version (14K): [in a new window]   Fig. 1. Responses to depolarising and hyperpolarising current pulses in type 1 and type 2 Dahlgren cells recorded intracellularly from SWA and FWA preparations. (Ai,ii) Both SWA (i) and FWA (ii) cells fire in response to a depolarising current pulse (+0.9 nA, 300 ms) and on the rebound following a hyperpolarising (-0.9 nA, 300 ms) pulse. (B) Voltage-dependent sag potentials (dotted lines) and depolarizing afterpotentials (DAP, arrow) recorded from a type 1 FWA cell in response to hyperpolarising square-wave current injection (-1.2 nA, 300 ms). The membrane potential was held at three levels [-50, -60 (RMP) and -70 mV] by constant current injection. At the more depolarised potential, the DAP triggered an action potential. RMP, resting membrane potential.

View larger version (26K): [in a new window]   Fig. 2. (A) Extracellular recordings of action potentials from CNSS. Dahlgren cell shows a triphasic, long-duration (ca. 8 ms) action potential waveform. An unidentified cell type, neuron, generates a short duration (<1 ms) action potential. (B) Multiunit extracellular recording (i) of spontaneously firing Dahlgren cells in SWA CNSS, analysed off-line using Spike2 to distinguish activity (action potentials displayed by the software as event marks) in four separate units (ii-v). Three different firing patterns are seen: tonic (ii), phasic (iii) and bursting activity (iv,v). (C) Intracellular recordings from three type 1 Dahlgren cells, illustrating spontaneous tonic (i), phasic (ii) and bursting activity patterns (iii).

View larger version (11K): [in a new window]   Fig. 3. Spontaneous transitions between different activity patterns in single units identified from multiunit recordings from CNSS. (A) SWA recording (i) in which two tonically active Dahlgren cells become silent (ii,iv) and a quiescent cell becomes tonically active (iii). (B) FWA recording (i) in which one cell switches spontaneously from phasic to tonic activity (ii), one from tonic to phasic activity (iii) and a third, quiescent, cell becomes bursting (iv).

View larger version (25K): [in a new window]   Fig. 4. Responses of Dahlgren cells to superfusion with acetylcholine (100 µmol l-1, 600 s; solid horizontal bar, onset shown by dotted line) in a SWA CNSS preparation. The activity of four units (ii-v) is separated from the original multiunit recording (i) and shows a range of responses, including a change from bursting to phasic activity (ii), short-term inhibition (iii), and increased firing frequency in a phasically active cell (v).

View larger version (19K): [in a new window]   Fig. 5. Superfusion of SWA CNSS with oxotremorine (100 µmol l-1, 600 s; solid horizontal bars) increased activity of neurons but inhibited Dahlgren cell activity, recorded extracellularly. Upward deflections in rectified integrated (RIT) traces reflect an increase in total activity in the CNSS. (A) No spontaneous Dahlgren cell or neuron activity is recorded; oxotremorine activated neurons, as shown in both RIT and voltage (CNSS) traces. (B,C) Several spontaneously active Dahlgren cells are inhibited by oxotremorine. However, an upward deflection in the RIT trace reflects an increase in overall activity due to neuron spikes.

View larger version (20K): [in a new window]   Fig. 6. Effects of oxotremorine (100 µmol l-1, 600 s; horizontal bars) on FWA and SWA Dahlgren cells. (A,B) Activity of individual Dahlgren cells (ii-v) extracted from multiunit recordings (i) from FWA (A) and SWA (B; same recording as Fig. 5C) CNSS. In both recordings, bursting and phasically active Dahlgren cells ceased firing, at least for the duration of the superfusion period. (C) Intracellular recording of FWA type 1 Dahlgren cell, showing hyperpolarisation of membrane potential (ca. 20 mV) in response to oxotremorine. Repolarisation (broken line) occurred in the continuing presence of the agonist. (D) Instantaneous firing frequency (top), and voltage recording (bottom) from a single, tonically active, SWA Dahlgren cell, showing a slow onset increase in firing frequency (from 1 to 3 Hz) in response to oxotremorine, accompanied by a reduction in spike amplitude (between horizontal dotted lines).

View larger version (23K): [in a new window]   Fig. 7. (A,B) Superfusion with nicotine (100 µmol l-1, 600 s; horizontal bars) promotes bursting activity in SWA Dahlgren cells. (A) Nicotine induces a transition from tonic to bursting activity in a Dahlgren cell recorded intracellularly. (B) Extracellular recording shows no change in ongoing bursting activity in at least three Dahlgren cells in response to nicotine. (C) Superfusion with nicotine (100 µmol l-1, 600 s; horizontal bar) inhibits Dahlgren cells in FWA CNSS. Three bursting units extracted from an extracellular recording become silent following application of nicotine; only one resumes firing after 15 min washout.