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Deactivation and Desensitization of Non-NMDA Receptors in Patches and the Time Course of Epscs in Rat Cerebellar Granule Cells

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Deactivation and Desensitization of Non-NMDA Receptors in Patches and the Time Course of Epscs in Rat Cerebellar Granule Cells 5404 Journal of Physiology (1996), 493.1, pp.167-173 167 Deactivation and desensitization of non-NMDA receptors in patches and the time course of EPSCs in rat cerebellar granule cells R. Angus Silver, David Colquhoun, Stuart G. Cull-Candy and Brian Edmonds Department of Pharmacology, University College London, Gower Street, London WC1E 6BT, UK 1. Spontaneous and evoked non-NMDA receptor-mediated EPSCs were recorded from cerebellar granule cells in slices at -24 and -34 'C. The EPSC decay was fitted with the sum of two exponential functions. 2. The time courses of non-NMDA receptor deactivation and desensitization were determined with fast concentration jumps of glutamate onto patches from cultured granule cells. Deactivation (decay time constant r = 0 6 ms at 24 °C) was substantially faster than desensitization ('r = 4 ms). Both processes were fitted by single exponential functions. 3. The decay of the fast component of the spontaneous EPSC (TEPSCfast = 09 ms at 23 °C) was marginally slower than deactivation but too fast to be determined by desensitization. Our results suggest that the decay of this component is set by both the rate of decline of transmitter concentration and channel deactivation. 4. A simple diffusion model predicts that the time course of transmitter in the cleft declines slowly during the later stages of its action. The slow phase of transmitter removal could account for the time course of the slow component of the spontaneous EPSC (rEPscslow = 8 ms at 23°C). The time course of excitatory postsynaptic currents (EPSCs) the mossy fibre to granule cell EPSC (Silver, Traynelis & is determined by the time course of the concentration of Cull-Candy, 1992). We have investigated the mechanisms transmitter in the synaptic cleft and the kinetic properties that shape non-NMDA component EPSCs in granule cells by of the postsynaptic receptors. If the concentration of comparing the time- and temperature-dependent properties transmitter in the cleft declines slowly, relative to the EPSC, of EPSCs with those of deactivation and desensitization in both the time course of transmitter decay and the rate of isolated patches from the soma of cultured granule cells. A receptor desensitization would be expected to shape the preliminary report has been published in this journal EPSC (Trussell, Zhang & Raman, 1993; Barbour, Keller, (Silver, Colquhoun, Cull-Candy & Edmonds, 1994). Llano & Marty, 1994). In contrast, if the decay of transmitter is relatively fast, the EPSC decay would be determined predominantly by the rate of deactivation (defined here as METHODS the rate at which current declines after a jump to zero Recordings agonist concentration) (Magleby & Stevens, 1972; Katz & As previously described, 10- to 14-day-old Sprague-Dawley rats Miledi, 1973; Colquhoun, Jonas & Sakmann, 1992). Recent were decapitated and their brains rapidly removed and placed in studies on glutamatergic synapses suggest that mechanisms ice-cold saline containing (mM): 125 NaCl, 2-5 KCl, 1 CaCl2, the of the 5 MgCl2, 125 NaH2PO4, 26 NaHCO3 and 15 glucose (pH 7-3 when underlying decay non-N-methyl-D-aspartate bubbled with 95 % 02-5 % CO2) (see Traynelis, Silver & Cull-Candy, (non-NMDA) component may vary at different synapses. 1993). Synaptic recordings were made from granule cells in 150 #sm Deactivation alone may account for the time course of EPSCs thick cerebellar slices. The effect of asynchrony of transmitter at some central synapses (Colquhoun et al. 1992; Hestrin, release on EPSC shape was minimized by examining spontaneous 1992), while at others, receptor desensitization may be currents and by selecting evoked currents that had a monotonic important in shaping the synaptic current (Trussell et al. rising phase (Traynelis et al. 1993). EPSCs were evoked at 1993). 0-5-1P0 Hz by stimulating (5-20 V; duration, 200 ,us) mossy fibre inputs with a patch electrode in the surrounding tissue. Spontaneous Cerebellar granule cells are electrically compact, allowing EPSCs were collected in the interstimulus period. Recordings were high resolution recordings of the non-NMDA component of made with an external solution containing (mM): 125 NaCl, This manuscript was accepted as a Short Paper for rapid publication. 16f8 R. A. Silver and others J. Phy8iol.493.1 25 KCl, 2 CaCl2, 1P25 NaH2PO4, 26 NaHCO3 and 15 glucose Non-NMDA currents from patches were filtered at 3 kHz, and (pH 7-3 when bubbled with 95% 02-5% CO2). MgCl2 (1 mM) was sampled on-line at 100 kHz or recorded onto tape. added in some experiments. D-Amino-5-phosphonopentanoic acid Fitting and (20 uM), 20/uM 7-chlorokynurenic acid and 15 uM bicuculline analysis methiodide were added to the perfusate to block NMDA and Non-NMDA EPSCs recorded in granule cells were averaged by y-aminobutyric acid type A receptors. Patch pipettes (5-15 M.Q) aligning the onset of the current and the decay was fitted with the were made from thick-walled borosilicate glass (Clark sum of two exponentials. Electrical models of granule cells (Silver et Electromedical) and coated with Sylgard (Dow Corning). The al. 1992), and the fact that single NMDA channel openings can be pipette solution consisted of (mM): 110 CsF, 30 CsCl, 4 NaCl, 0 5 resolved in the synaptic current, indicate that the voltage at CaC12, 10 Hepes and 5 EGTA (pH 7 3). EPSCs were recorded using synapses located on the dendrites is well clamped. The capacitance, an L/M-EPC-7 (List) or an Axopatch 200A (Axon Instruments) input resistance and series resistance were determined for each cell amplifier and recorded on tape. Recordings were filtered at 4-8 kHz from the capacitative current response to a -10 mV voltage step. (-3 dB) and digitized from tape at 50-100 kHz. The mean values were: 3-2 + 0'3 pF, 6 + 2 GQl and 23 + 3 MQl (n = 12), respectively, at 24 °C; and 3'0 + 0 3 pF, 6 + 2 GQ and Non-NMDA receptors were not detectable in patches taken from 21 + 3 M.Q (n = 11), respectively, at 34 'C. Least-squares fits were the soma of granule cells in slices. Outside-out patches were made by fixing the asymptote of the exponential function to the therefore made from cultured granule cells prepared from 7-day-old pre-event baseline. Since the relative amplitude of fitted rats and used 3-5 days after plating (Cull-Candy, Howe & Ogden, exponentials depends on where t = 0 is taken to be, and in the case 1988). Application of glutamate (0 3-5 0 mM) was achieved by of EPSCs this is somewhat arbitrary, we have defined t = 0 as the rapid movement (using a piezotranslator, model P-244.40; Physik peak of the EPSC. Instrumente, Waldbronn, Germany) of the interface of solutions flowing from either side of a theta glass partition. Junction Temperature coefficient (Q1o) values were calculated from current responses to the shortest (200 ,us) jumps were usually (TT/1T2)lO/AT, where TTl and 1T2 are the mean time constants of within 90% of the steady-state value. The inflowing bath perfusate decay at lower and higher temperatures, respectively, and ATis the (1-2 ml min-') was heated with a Peltier device and the temperature difference. Errors for the numerator (e.g. TTlO0/AT) and temperature was monitored in the bath. Immersion of about 2 cm denominator were calculated using a Taylor series approximation. of the thin theta glass application tool, and the relatively low flow An approximate standard deviation for the Qlo was then obtained rates used (0-1-0-2 ml min-'), ensured that the perfusate in the using Fieller's theorem. P values were calculated with Student's t rapid application tool and bath were close to thermal equilibrium. and randomization tests. A C Spontaneous EPSCs at 260C Evoked EPSCs at 25 00 rEPSCsIow -47 ms TEPSCsiow -103 ms 10 pA 50 TEPSCfast = 07 ms TEPSCfast 1-4 ms pA 5 ms 5 ms B D Evoked EPSCs at 350°C 7EPSCsIow = 4O0 ms 7EPSCslow - 7 9 ms 5 pA 100 pA 0 7 ms EPSCfast =5 5 ms EPSCfast = 5 ms Figure 1. The non-NMDA component of EPSCs in cerebellar granule cells decays biphasically A, the average of 102 spontaneous EPSCs recorded from a granule cell at room temperature. The superimposed curve shows a least-squares fit of the sum of two exponentials to the EPSC decay (I(t) = -23'2exp(-t/0 69) - 3-5exp(-t/4 7), where I is current and t is time). B, the average of 233 EPSCs recorded at 34 °C. The superimposed curve is the least-squares fit to the EPSC (I(t) =-12-2exp(-t/0 49)-1-91 exp(-t/4 0)). C, the average of 63 evoked EPSCs at 25 °C with superimposed fit (I(t) = -46-5exp(-t/1-4) - 671exp(-t/10-3)). D, the average of 76 evoked EPSCs at 35 °C with superimposed fit (I(t) = -162-9exp(-t/0 67) - 14-2exp(-t/7 9)). All EPSCs were recorded at -70 mV. Part of the stimulus artifact in C and D was omitted for clarity. J Physiol.493.1 Time course of EPSCs and non-NMDA receptor currents 169 Diffusion calculations change. The values of the resistive and capacitative elements of the There is insufficient knowledge of the properties of release, cleft circuit were taken from granule cell recordings at 35 'C. The time- geometry, receptor density and binding kinetics to allow realistic dependent conductance change was determined by approximating calculation of the expected time course of transmitter the mean waveform of the evoked synaptic current with the sum of concentration. However, a rough estimate can be obtained if the three exponential functions.
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