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Outward Currents in Isolated Ventral Cochlear Nucleus Neurons

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Outward Currents in Isolated Ventral Cochlear Nucleus Neurons The Journal of Neuroscience, September 1991, 1 f(9): 2865-2880 Outward Currents in Isolated Ventral Cochlear Nucleus Neurons Paul B. Manis and Steven 0. Marx” Departments of Otolaryngology-Head and Neck Surgery, Neuroscience, and Biomedical Engineering, and The Center for Hearing Sciences, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205 Neurons of the ventral cochlear nucleus (VCN) perform di- neurons are in part attributable to the types of outward (po- verse information processing tasks on incoming activity from tassium) conductances present in these cells. The low- the auditory nerve. We have investigated the cellular basis threshold conductance in the Type II (bushy) cells probably for functional diversity in VCN cells by characterizing the plays a role in the preservation of information about the outward membrane conductances of acutely isolated cells acoustic stimulus phase from the auditory nerve to central using whole-cell, tight-seal, current- and voltage-clamp auditory nuclei involved in low-frequency sound localization. techniques. The electrical responses of isolated cells fall into two broad categories. Type I cells respond to small Neurons of the ventral cochlear nucleus (VCN) receive first- depolarizations with a regular train of action potentials. Un- order input from the auditory nerve (Harrison and Irving, 1966; der voltage clamp, these cells exhibit a noninactivating out- Feldman and Harrison, 1969; Osen, 1970; Brawer and Morest, ward current for voltage steps positive to -35 mV. Analysis 1975; Lorente de No, 198 1; Fekete et al., 1984; Rouiller et al., of tail currents reveals two exponentially decaying compo- 1986). However, VCN neurons can be distinguished by their nents with slightly different voltage dependence. These cur- discharge patterns in responseto acoustic stimuli, suggesting rents reverse at -73 mV, near the potassium equilibrium that different classesof cells perform distinct information pro- potential of -84 mV, and are blocked by tetraethylammon- cessing functions on incoming acoustic information (Pfeiffer, ium (TEA). The major outward current in Type I cells thus 1966a; Bourk, 1976; Young et al., 1988; Blackbum and Sachs, appears to be mediated by potassium channels. In contrast 1989). Some of the different physiological responsetypes are to Type I cells, Type II cells respond to small depolarizations associatedwith cells of specific morphology (Rhode et al., 1983; with only one to three short-latency action potentials and Rouiller and Ryugo, 1984; Smith and Rhode, 1987, 1989). Thus, exhibit strong rectification around -70 mV. Under voltage bushy cells, which receive a strong somatic innervation from clamp, these cells exhibit a noninactivattng outward current large endingsof auditory nerve fibers (Brawer and Mores& 1975; with a threshold near -70 mV. Analysis of tail currents re- Fekete et al., 1984), exhibit responsesquite similar to those of veals two components with different voltage sensitivity and the auditory nerve. In contrast, stellate cells, which receive both kinetics. A low-threshold current with slow kinetics is partly somatic and dendritic innervation by small boutons from au- activated at rest. This current reverses at -77 mV and is ditory nerve fibers (Cant, 1981, 1982) respond to tones with a blocked by 4-aminopyridine (4-AP) but is only partly affected regular dischargepattern. by TEA. The other component is a high-threshold current The responsesof VCN neurons are also shapedby their in- activated by steps positive to -35 mV. This current is blocked trinsic voltage-dependent conductances(Oertel, 1983; Wu and by TEA, but not by 4-AP. A simple model based on the volt- Oertel, 1984). Bushy cells have been shown to have highly rec- age dependence and kinetics of the slow low-threshold out- tifying current-voltage relationships and dischargeonly one or ward current in Type II cells was developed. The model pro- two action potentials in responseto depolarizing current steps. duces current- and voltage-clamp responses that resemble Stellate cells have relatively linear subthresholdcurrent-voltage those recorded experimentally. Our results indicate that the relationships and discharge a regular train of action potentials two major classes of acoustic response properties of VCN in responseto current steps.The specific conductancesthat are responsible for the different discharge characteristics of these two cell classeshave not been identified. Received Nov. 30, 1990; revised Apr. 22, 199 1; accepted Apr. 26, 199 1. In this article, we present the results of voltage-clamp exper- We thank Drs. M. B. Sachs and E. D. Young for their valuable comments on iments on acutely isolated neurons of the VCN. We find, in the manuscript, and Ms. Diane Kitko for editorial assistance. We are especially agreement with Oertel (1983) that two classesof cells can be grateful to Dr. W. E. Brownell for the loan of the voltage-clamp amplifiers used in the initial experiments and for the use of his osmometer. We are also indebted identified basedon their electrophysiologicalproperties. We then to Drs. E. Webster (NIDA) and M. Rogawski (NINDS) for insights into procedures demonstrate that these two classesare distinguished by their for acute cell isolation, and to Dr. D. Bertrand for suggestions on the potassium pharmacology experiments and for his program DATAC. This work was supported different complements of outward currents. The outward cur- primarily by a grant from the Deafness Research Foundation to P.B.M.; additional rents differ in their voltage dependence,kinetics, and pharma- support was provided by NIDCD Grant DC00425. S.O.M. was supported by NIH cological sensitivity to potassium channel blockers. A model Grant T32 NS.07283 to Dr. M. B. Sachs. Correspondence should be addressed to Paul B. Manis, Department of Otolar- incorporating the properties of one of the currents in presump- yngology-Head and Neck Surgery, The Johns Hopkins University School of Med- tive bushy cells was developed to demonstrate its influence on icine, 522 Traylor Research Building, 720 Rutland Avenue, Baltimore, MD 2 1205. subthreshold membrane phenomena. = Present address: Department of Internal Medicine, University of Rochester School of Medicine, Rochester, NY 14642. A preliminary report of these results has been presentedpre- Copyright 0 1991 Society for Neuroscience 0270-6474/91/l 12865-16%03.00/O viously (Manis and Marx, 1989). 2866 Manis and Marx l Voltage Clamp of Isolated VCN Cells Mg-ATP. The pH was brought to 7.2 with KOH, and the final osmolarity Materials and Methods was -270 mOsm. The resistance of these electrodes in the recording Slice preparation and cell isolation. Tight-seal, whole-cell, voltage- and bath was 3-10 MfL Seals were obtained by abutting the electrode against current-clamp recordings were made from neurons isolated from brain the cell membrane and applying gentle suction. The seal resistance be- slices of adult guinea pig ventral cochlear nucleus. Slices were prepared fore rupture of the cell membrane exceeded 1 Gti. Trains of action following established techniques (Oertel, 1985; Manis, 1989). Pig- potentials could be observed in some cells before the patch was ruptured. mented guinea pigs weighing 200-500 gm were deeply anesthetized with Ampl&rs. Three different amplifiers were used for current- and volt- pentobarbital(35 mg/kg) and decapitated with a guillotine. The brain- age-clamp recordings from the isolated cells. In the initial experiments, stem was removed from the skull after transecting the eighth nerves. recordings were obtained with a switching amplifier (custom built by Slices 300-350 pm thick were cut either parasagittally or horizontally Department of Physiology, Centre Medical Universitaire, Geneva; de- through the cochlear nucleus with an oscillating tissue slicer. Small sign of D. Bertrand). The relatively large conductance changes that pieces of the VCN were excised from the slices with Castrovieio scissors occurred during activation of the outward currents caused the time under a dissecting microscope (25-50 x). This ensured that isolated cells constants of the cells to fall below 0.5 msec, close to the electrode time were obtained only from the VCN, and not from adjoining regions of constants (- 100-500 psec). We were thus able to voltage clamp these the brainstem or the dorsal cochlear nucleus. The trimmed slices were neurons properly only over the voltage range where the conductance incubated in a chamber containing approximately 12 ml of oxygenated was low (see Finkel and Redman, 1985). The data from these experi- dissociation media (see below) at -34°C. ments were used only to correlate the threshold voltage for activation The cell isolation procedure was similar to that used for neocortical of the currents with the properties of the cells as studied in current and brainstem structures (Gray and Johnston, 1985; Kay and Wong, clamp and to examine the effects of potassium channel blockers on 1986; Numann et al., 1987; Akaike et al., 1988). The slices were treated small inward and outward currents. with a solution that contained, in addition to the basic components Most of the quantitative voltage-clamp data reported in this article listed below. 0.125-0.33 ma/ml Pronase E (Tvne XXV. Siama Chemical were obtained either with an Axoclamp-2 amplifier (Axon Instruments) Co.) and 0.b4-0.08 mg&? collagenase (CI?? III, Worthington). The operated in the continuous single-electrode voltage-clamp mode, or with slices were treated at 31°C for 1 hr. During the enzymatic treatment, an Axopatch 1 C amplifier. Voltage and current records were filtered at the slices rested on a nylon net and were slightly agitated by bubbling 5-10 kHz and digitized at 10 kHz with a 12-bit A-D converter (Manis the solution with 100% 0,. Enzyme activity was terminated by trans- and Bertrand, 1989). Current records in voltage clamp are averages of ferring the slices to a solution containing 0.25 mg/ml soybean trypsin four traces. The program DATAC (Bertrand and Bader, 1986) was used inhibitor (Sigma) and 0.25 mg/ml BSA (Sigma) for 5 min at room for data acquisition, analysis, curve fitting, and plotting.
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