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Development of Glycinergic and Glutamatergic Synaptic Transmission in the Auditory Brainstem of Perinatal Rats

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Development of Glycinergic and Glutamatergic Synaptic Transmission in the Auditory Brainstem of Perinatal Rats The Journal of Neuroscience, October 1995, 15(10): 6890-6904 Development of Glycinergic and Glutamatergic Synaptic Transmission in the Auditory Brainstem of Perinatal Rats Karl Kandler and Eckhard Friauf” Department of Animal Physiology, University of Ttibingen, D-72076 Ttibingen, Germany In contrast to our knowledge about the anatomical devel- In contrast to our detailed knowledge of the development of opment of the mammalian central auditory system, the de- excitatory connectionsin the CNS (review, Goodman and Shatz, velopment of its physiological properties is still poorly un- 1993), relatively little is known about the developmentof inhib- derstood. In order to better understand the physiological itory connections.This is due to the fact that inhibitory circuits properties of the developing mammalian auditory brain- are usually intrinsic to nuclei and formed by interneurons,and stem, we made intracellular recordings in brainstem slices are therefore relatively inaccessiblefor analysis. The auditory from perinatal rats to examine synaptic transmission in the brainstemof mammals,however, has proven to be a useful mod- superior olivary complex, the first binaural station in the el for addressingthe development of inhibitory connections(Sa- ascending auditory pathway. We concentrated on neurons nes and Siverls, 1991; Saneset al., 1992; Sanes, 1993; Sanes in the lateral superior olive (LSO), which in adults, are ex- and Takacs, 1993), becauseinhibitory connectionsbetween au- cited from the ipsilateral side and inhibited from the con- ditory brainstem nuclei are highly topographically ordered and tralateral side. Already at embryonic day (E) 18, when axon their adult anatomy and physiology are well documented (re- collaterals begin to invade the LSO anlage, synaptic poten- views, Irvine, 1992; Schwartz, 1992). The lateral superior olive tials could be evoked from ipsilateral, as well as from con- (LSO), a nucleus in the superior olivary complex (SOC) that is tralateral inputs. lpsilaterally elicited PSPs were always de- involved in sound localization by processingbinaural intensity polarizing, regardless of age. They had a positive reversal differences, receives inhibitory, glycinergic input from the con- potential and could be completely blocked by the non- tralateral ear via the medial nucleus of the trapezoid body NMDA glutamate receptor antagonist CNQX. In contrast, (MNTB), and excitatory, glutamatergic input from the ipsilateral contralaterally elicited PSPs were depolarizing from El& ear via the ventral cochlear nucleus (see Fig. 1). Both inputs are P4, yet they turned into “adult-like,” hyperpolarizing PSPs tonotopically organized and perfectly aligned with each other after P8. Their reversal potential shifted dramatically from (Caird and Klinke, 1983). During development, the contralateral -21.6 + 17.7 mV (El&PO) to -73.0 + 7.1 mV (PlO). Re- glycinergic pathway is refined in part by pruning of the afferent gardless of their polarity, contralaterally elicited PSPs were glycinergic axon terminals of MNTB neurons within the LSO reversibly blocked by the glycine receptor antagonist (Sanes and Siverls, 1991; Sanes and Takacs, 1993) as well as strychnine. Bath application of glycine and its agonist p-al- the postsynaptic dendritic trees of LSO neurons (Sanes and anine further confirmed the transitory depolarizing action Chokshi, 1992; Sanes et al., 1992; Rietzel and Friauf, 1995). of glycine in the auditory brainstem. Since the transient The morphological remodeling of the inhibitory pathway ap- excitatory behavior of glycine occurs during a period dur- pearsto be activity dependent,because remodeling is prevented ing which glycinergic synaptic connections in the LSO are by chronically blocking postsynaptic glycine receptors (Sanes refined by activity-dependent mechanisms, glycinergic ex- and Chokshi, 1992) or by reducing neural activity in the MNTB citation might be a mechanism by which synaptic rear- (Moore, 1992; Sanesand Takacs, 1993). However, the cellular rangement in the contralateral inhibitory pathway is ac- mechanismsunderlying the activity-dependent remodelingof in- complished. hibitory synapsesare completely unknown. [Key words: auditory, development, glutamate, glycine, Innervation of the SOC begins at embryonic day (E) 18 (Kan- inhibitory glycine receptor, lateral superior olive, rat, su- dler and Friauf, 1993a),but physiological hearing doesnot begin perior olivary complex, strychnine] until the end of the secondpostnatal week (P12-14, e.g., Uziel et al., 1981). In the present study we used an in vitro brainstem slice preparation to examine the physiology and pharmacology Received Mar. 31, 1995; revised June 12, 1995; accepted June 19, 1995. of early synaptic transmissionin the embryonic and postnatal We thank Dr. Donata Oertel for technical advice, Drs. Richard Mooney and SOC of rats during the period from El8 to the onset of hearing. Ellen Covey for helpful comments on an earlier version of the manuscript, and We found that ipsilateral and contralateral synaptic transmission Dinnie-Ma Goldring for correcting our English. This work was supported by grants from the Deutsche Forschungsgemeinschaft to E.E (Fr 772/l-2 and are both presentas early as El 8 and that the maturation of post- Fr772/1-3) and by fellowships from the Graduiertenkolleg Neurobiologie Tii- synaptic potentials (PSPs) in SOC neurons is marked by a de- bingen and the DAAD/NATO to K.K. Correspondence should be addressed to Karl Kandler, Ph.D., Department of creasein their latency and duration. Most interestingly, however, Neurobiology, Box 3209, Duke University Medical Center, Durham, NC we found that contralaterally elicited PSPs in LSO neuronsre- 27710. verse their polarity during development: in embryonic and early *Present address: Zentrum der Physiologic, University of Frankfurt, D-60590 Frankfurt, Germany. postnatal animals, the glycinergic strychnine-sensitive input is Copyright 0 1995 Society for Neuroscience 0270-6474/95/156890-15$05.00/O depolarizing, but in animals older than P8 it is hyperpolarizing. The Journal of Neuroscience, October 1995, 75(10) 6891 and Oertel (1984). Penetration of neurons was achieved by applying short current or voltage pulses through the electrodes using the built-in circuits of the intracellular amplifier (Neurodata, Model 286). In a few cases, a weak negative current (holding current, -0.1 to -0.3 nA) was applied for the first few minutes following the penetration in order to help stabilize the recording. Holding currents were always turned off before data gathering. Synaptic responses were elicited by applying short current pulses (60-80 ps, 0.1-10 mA, 0.03-0.1 Hz) to the ipsilateral or contralateral afferent fibers. Bipolar stainless steel electrodes (Rhodes NEX 200) were placed in the ventral acoustic stria (VAS), lateral to the SOC to activate the ipsilateral input and at the midline decussation, to activate the contralateral input (Fig. 1). To minimize current spread outside of the VAS, the two poles of each stimulation electrode were arranged perpendicular to the VAS, with the auditory fibers running between the w two poles. contra Pharmacological solutions. Concentrated stock solutions of the fol- ret lowing drugs were prepared in distilled water, aliquoted, and stored at stim -20°C: glycine, @-alanine, strychnine, kynurenic acid, 6-cyano-7-nitro- Figure 1. Schematic drawing of the auditory brainstem slice prepa- quinoxaline-2.3.dione (CNOX), amino-5-ohosnhonovaleric acid (APV). ration illustrating the experimental design. Ipsilateral fibers from the i+)-5-methyl-lo,1 l-dihydco-!5H-dibenzi[a,djcyclohepten-5,1d-imine cochlear nucleus (Chr) to the SOC were electrically stimulated lateral (MK801), and y-aminobutyric acid (GABA). During the experiment, to the lateral superior olive (LSO) (ipsi stim) and contralateral fibers small amounts of stock solutions were added to the ACSF, resulting in were stimulated at the midline (contra stim). Most intracellular record- the final drug concentration in the recording chamber. Kynurenic acid ings (ret) were obtained from LSO neurons, which receive excitatory, was purchased from Fluka, CNQX, APV, and MK-801 were purchased glutamatergic input (solid line) from the ipsilateral CN and inhibitory, from Research Biochemicals International, and the remaining chemicals glycinergic input (dashed line) from the contralateral CN via the medial from Sigma. nucleus of the trapezoid body (MNTB). Other nuclei of the SOC from Data analysis. On-line analysis of intracellular signals was performed which we obtained intracellular recordings are the medial superior olive by digitizing (20-20,000 Hz, AD-board from Batelle Europe) the output (MS@, the ventral nucleus of the trapezoid body (VNTB), and the su- of the intracellular amplifier and by further processing with software perior paraolivary nucleus (SPM. (TIDA, Batelle Europe). Unprocessed signals were also stored on digital audiotape (DAT-recorder, Biologic, sampling rate 24 kHz) for later off- line analysis. PSPs were characterized by their latency, amplitude, half-width du- This is further supported by our finding that during the same ration, and reversal potential. PSP latency was measured from the be- period at whic,h the contralateral input is depolarizing, bath-ap- ginning of the stimulus artifact to the first noticeable deflection of the plied glycine has depolarizing effects in the SOC. We suggest voltage trace from the baseline membrane potential. Spike latency was that the depolarizing action of glycine plays
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