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Synaptic Transmission Between Dorsal Root Ganglion and Dorsal 0270.6474/85/0508~2281$02.00/0 The Journal of Neuroscrence Copyright 0 Society for Neuroscrence Vol. 5, No 8, pp. 2281-2289 Printed rn U S.A. August 1985 Synaptic Transmission between Dorsal Root Ganglion and Dorsal Horn Neurons in Culture: Antagonism of Monosynaptic Excitatory Postsynaptic Potentials and Glutamate Excitation by Kynurenate’ C. E. JAHR AND T. M. JESSELL* Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115 Abstract Randic, 1984). Several lines of evidence suggest that the fast EPSPs in spinal cord neurons evoked by primary afferent stimulation are intracellular recording techniques have been used to pro- mediated by L-glutamate or by compounds with similar postsynaptic vide information on the identity of excitatory sensory trans- actions. lontophoretic and pressure applications of L-glutamate de- mitters released at synapses formed between dorsal root polarize the majority of mammalian spinal neurons in vivo and in ganglion (DRG) and dorsal horn neurons maintained in cell vitro (Ransom et al., 1977b; Watkins and Evans, 1981; Salt and Hill, culture. Explants of embryonic rat DRG were added to dis- 1983) with a reversal potential (Mayer and Westbrook, 1984) similar sociated cultures of embryonic dorsal horn neurons and to that of the EPSP evoked by dorsal root ganglion (DRG) neuron synaptic potentials were recorded intracellularly from dorsal stimulation (Engberg and Marshall, 1979; Finkel and Redman, 1983; horn neurons after DRG explant stimulation. More than 80% MacDonald et al., 1983). Biochemical analysis has demonstrated a of dorsal horn neurons within 1 mm of DRG explants received higher concentration of L-glutamate in dorsal than in ventral roots at least one fast, DRG-evoked, monosynaptic input. In the (Roberts et al., 1973) and has provided evidence for release of presence of high divalent cation concentrations, the acidic endogenous L-glutamate from regions of the CNS containing primary amino acid receptor agonists, L-glutamate, kainate, and quis- afferent terminals (Roberts, 1974; Takeuchi et al., 1983). Moreover, qualate excited all dorsal horn neurons which received a L-glutamate-binding sites are found in high density in the superficial monosynaptic DRG neuron input, whereas aspartate and N- dorsal horn of rat spinal cord (Greenamyre et al., 1984) suggesting methyl-D-aspartate (NMDA) had little or no action. Several that amino acids may function as sensory transmitters released from compounds reported to antagonize the actions of acidic cutaneous afferents. amino acids were tested for their ability to block DRG-evoked Direct confirmation of the role of acidic amino acids as primary synaptic potentials and glutamate-evoked responses in dor- sensory transmitters is still lacking. In studies with intact spinal cord sal horn neurons. preparations it has been difficult to distinguish the direct effects of 2-Amino-5-phosphonovalerate, a selective NMDA receptor exogenously applied amino acid transmitter candidates. Moreover, antagonist, was relatively ineffective at antagonizing DRG- pharmacological studies have provided evidence for at least three evoked synaptic potentials and glutamate-evoked re- amino acid receptor subtypes, each of which can be activated by sponses. In contrast, kynurenate was found to be a potent L-glutamate (Watkins and Evans, 1981; Foster and Fagg, 1984). antagonist of amino acid-evoked responses and of synaptic Selective ligands are available for only one of the receptor subtypes: transmission at all DRG-dorsal horn synapses examined. The N-methyl-o-aspartate (NMDA) is a selective agonist and 2-amino-5 blockade of synaptic transmission by kynurenate appeared phosphonovalerate (APV) is a relatively selective antagonist at the to result from a postsynaptic action on dorsal horn neurons. NMDA subclass of receptor (Davies et al., 1981a). The ion channel These findings indicate that glutamate, or a glutamate-like opened by NMDA receptor occupation is subject to a voltage- compound, but not aspartate, is the excitatory transmitter dependent blockade in the presence of micromolar concentrations that mediates fast excitatory postsynaptic potentials at the of magnesium ions (Ault et al., 1980; Mayer et al., 1984; Nowack et DRG-dorsal horn synapses examined in this study. al., 1984) thus providing a second means of distinguishing this receptor subtype. The existence of two additional classes of amino acid receptors has been proposed on the basis of pharmacological The transmission of sensory Information at primary afferent syn- studies with the rigid amino acid analogues quisqualic acid and apses In the sprnal cord involves the release of sensory transmitter(s) kainic acid (Watkins and Evans, 1981; Foster and Fagg, 1984). that elicits both fast and slow excitatory postsynaptic potentials These two receptors are more difficult to distinguish from each other. (EPSPs) in postsynaptic spinal neurons (Eccles, 1964; Urban and They are not blocked by magnesium ions or by APV but may be blocked differentially by y-o-glutamylglycine and piperidine dicarbox- ylic acid (Davis and Watkins, 1981). These compounds, however, Recerved November 19, 1984; Revrsed January 21, 1985, appear to be relatively nonselective since they also block the actions Accepted January 22, 1985 of amino acids at NMDA receptor sites (Francis et al., 1980; Davies ’ We wash to thank Dr. K. Yoshroka for helpful drscussrons and Drs. P. R. et al., 1981 b). Adams, J. Dodd, A. Willard, and K Yoshioka for cntrcal reading of the To provide more direct information on the identity of primary manuscript This work was supported In part by National Institutes of Health sensory transmitters and to characterize the postsynaptic receptors Grants NS 17369, NS 20116, NS 21419, and NS 07051, and by the McKnrght that mediate fast EPSPs at sensory synapses, we examined the Foundatron. a DuPont Faculty Award, and the Muscular Dystrophy Assocra- actions of excitatory amino acid receptor ligands at afferent syn- tron. apses in cell culture. Intracellular recording was used to identify ‘To whom correspondence should be addressed. dorsal horn neurons that receive monosynaptic DRG input and to 2281 2282 Jahr and Jesse11 Vol. 5, No. 8, Aug. 1985 characterize the sensitivity of these neurons to excitatory amino acid Cd’ and 0.9 mM Mg’+ or 5 mM Ca*’ and 3 mM Mg2+ to inhibit polysynaptic agonists. Several excitatory amino acid antagonists have been potentials (see “Results”). examined, and kynurenate (Perkins and Stone, 1982) was identified The use of extracellular electrodes to stimulate the presynaptic neurons as a potent antagonist of synaptic transmissron between DRG and did not allow us to monitor the presynaptic action potential of indivrdual DRG neurons. To provide evidence that successive stimuli resulted In the activation dorsal horn neurons. Kynurenate has been reported to antagonize of the identical set of presynaptrc DRG neurons, the strmulus strength was EPSPs in hippocampal pyramidal neurons and ventral root potentials varied until a range was found in which large changes In the strmulus strength in the rat (Ganong et al., 1983) and frog (Elmslie and Yoshikamr, resulted in no change in the amplitude of the EPSP. The stimulus strength 1983) spinal cord. Our results suggest that L-glutamate or a closely was then confined to the middle of the range for the duration of the dorsal related compound, but not L-aspartate, is likely to be the transmitter horn neuron impalement. The EPSP was closely monitored throughout the released at the sensory synapses examined in the present study. experiment. If sudden changes in EPSP amplitude were detected, the stimulus strength was adjusted and the experiment was restarted. If there Materials and Methods was any ambiguity in the constancy of stimulation, the recording was ended. Dorsal horn neurons were obtained from the dorsal half of spinal cords of Most EPSPs studred were composed of one to four components, each 15day rat embryos. After removal of the dura, the dorsal spinal cord was evoked at a different but constant stimulus strength (see Fig. 4). Changes In chopped in two drrectrons at 200.pm Intervals and then Incubated wrth trypsin the stimulus strength at which individual components were elicited were (0.025%) and DNase (80 fig/ml) (Yamamoto et al., 1981; Jahr and Jessell, tolerated only when alterations in the total divalent cation concentratron were 1983) for 15 min at 37°C. The dorsal sprnal trssue was drssocrated into a made. After such a change, prolonged control records were obtained in srngle cell suspensron by tnturatron with a fire-polrshed Pasteur prpette. order to ensure stability before proceeding with the experiment. Aliquots of the cell suspensron were plated onto collagencoated 35.mm Chemicals were obtained from the following sources: L-glutamate and L- trssue culture dashes containing a confluent monolayer of non-neuronal cells aspartate (Sigma Chemical Co. and Grand Island Biologrcal Co.); qursqualate, (predomrnately astrocytes) derived from 15. to 17.day embryonic rat spinal kainate, and 2-ammo-4-phosphonobutyrate (Cambridge Research Brochem- cord. DRGs were dissected from 16. to 17-day rat embryos, incubated icals); 2-amino-5-phosphonovalerate (Sigma and Cambridge Research BIO- overnrght in arabinosylcytosine (1 Om5 M) to suppress the proliferation of non- chemicals): and kynurenate (Sigma and Aldrich Chemical Corp.). neural cells, and added to cultures of dorsal horn neurons which had been plated 1 to 17 days earlier. Cultures were fed every 2 to 3
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