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Ultrastructural Evidence for Gabaergic Brain Stem Projections to Spinal Motoneurons in the Rat

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Ultrastructural Evidence for Gabaergic Brain Stem Projections to Spinal Motoneurons in the Rat The Journal of Neuroscience, January 1991, if(i): 159-l 67 Ultrastructural Evidence for GABAergic Brain Stem Projections to Spinal Motoneurons in the Rat J. C. Holstege Department of Anatomy, Erasmus University Medical School, 3000 DR Rotterdam. The Netherlands In the present ultrastructural study in the rat, it was deter- The reticular formation of the lower brain stem exerts strong mined whether GABA was present in projections descending excitatory and inhibitory effects on the activity of spinal mo- from the ventromedial reticular formation of the lower brain toneurons. It is generally assumedthat the inhibitory effect on stem to motoneuronal cell groups in the lumbar spinal cord. motoneurons (especially those innervating musclesof the ex- For this purpose, the anterograde transport of WGA-HRP was tremities) is relayed through interneurons in the spinal inter- combined with the postembedding immunogold technique mediate zone (for review, seeWilson and Peterson, 1981). How- for GABA, with the advantage that both markers could be ever, some physiological studies have shown the existence of visualized simultaneously in a single terminal. monosynaptic inhibitory connections between neurons in the In 4 rats, WGA-HRP was injected in the ventromedial part medial lower brain stem and spinal motoneurons (Llinas and of the brain stem reticular formation at levels between the Terzuolo, 1964; cf. Magoun and Rhines, 1946). Anatomical rostra1 inferior olive and the caudal part of the facial nucleus. evidence for direct brain stem projections to motoneuronal cell Vibratome sections were cut from the lumbar spinal cord, groups was given by Dahlstriim and Fuxe (1965) with the his- reacted for WGA-HRP, and processed for electron micros- tofluorescent technique. They showedthe disappearance,below copy. Ultrathin sections containing the lateral motoneuronal a lesion of the cervical cord, of the serotonergic innervation, cell groups were cut and treated following the immunogold including the terminals in the motoneuronal cell groups, with technique using a polyclonal antibody directed against GABA. a concomitant increasein the fluorescenceof serotonergiccells It was found that nearly 40% of the terminal profiles that in the lower brain stem. These findings implied that the direct were labeled with WGA-HRP reaction products from the ven- brain stem projections to motoneurons, which were identified tromedial brain stem were also labeled for GABA (double physiologically, were (at least in part) serotonergic.Anatomical labeled). Most of the double-labeled terminals (81%) were tracing studies with the light microscopical (LM) anterograde F-type (containing many flattened vesicles), 12% were degeneration technique, using silver impregnation, failed to G-type (containing many granular vesicles), and 7% were demonstrate direct projections from the brain stem to spinal S-type (containing many spherical vesicles). The majority of motoneuronal cell groups(Kuypers, 1981). They were first shown the double-labeled terminals contacted proximal dendrites. by meansof the LM autoradiographic tracing technique in the It is argued that the descending GABAergic projection cat (Holstege et al., 1979; G. Holstege and Kuypers, 1982), produces a general inhibitory effect on spinal motoneurons, opossum(Martin et al., 1979) and rat (Jones and Yang, 1985; counteracting the general facilitation produced by the se- Martin et al., 1985).The projections to motoneuronalcell groups rotonergic projection derived from the same brain stem area. were found to originate mainly in the caudal raphe nuclei, the The balance between the activity of the GABAergic and the adjacent ventral part of the medial reticular formation, and the serotonergic fibers may set the level of excitability of the dorsolateral pons, including the area of the locus coeruleusand spinal motoneurons. The presence of GABA in some of the subcoeruleus(for review, seeHolstege and Kuypers, 1987b). WGA-HRP-labeled (presumed serotonergic) G-type termi- An ultrastructural study in the rat (Holstege and Kuypers, nals was interpreted to indicate partial coexistence of GABA 1987a) in which the anterogradetransport of jH-leucine from and serotonin, supporting the hypothesis that these trans- the medial reticular formation was combined with the retro- mitters are closely related in the descending brain stem pro- grade transport of HRP from the hindleg muscles,showed that jections to spinal motoneurons. The results further indicate the terminals derived from neurons in the ventral part of the that other transmitters are likely to play a part in this gain- medial reticular formation contacted HRP-labeled motoneu- setting system, which may be active both during sleep and rons in the lumbar spinal cord. The projections from the ventral wakefulness. part of the medial reticular formation as well as those from the raphe nuclei exhibited 3 different types of terminals: F-type terminals (containing many flattened vesicles),S-type terminals Received May 4, 1990; revised Aug. 30, 1990; accepted Sept. 5, 1990. (containing mainly spherical vesicles), and G-type terminals I would like to thank Dr. J. Vooad for readine the manuscriot: Mrs. C. M. (containing many granular vesicles; Holstege, 1987; Holstege Bijker-Biemond, Mrs. C. M. H. Bong&, and Mrs. G. Goedknegt fo; their technical and Kuypers, 1987a). The G-type terminals were found to be assistance; Mr. E. Dalm for his help with the surgery; and Mrs. P. van Alphen for her help with the photography. This investigation was supported by Grant serotonergic and/or peptidergic (Pelletier et al., 1981; Ulfhake 900-550-072 from the Foundation for Medical Research MEDIGON, which is et al., 1987; for review, see Holstege and Kuypers, 1987b), in subsidized by the Netherlands Research Organization (NWO). agreementwith the histofluorescent findings of Dahlstrom and Correspondence should be addressed to J. C. Holstege, Department ofAnatomy, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands. Fuxe (1965), whereasthe transmitters in the F- and S-type ter- Copyright 0 1991 Society for Neuroscience0270-6474/91/1010159-09$03.00/O minals remained unknown. Retrograde tracing studies com- 160 Holstege l GABAergic Brain Stem Projections to Spinal Motoneurons bined with immunocytochemistry showed that several of the not taken into account for the present analysis (for a discussion of these descending brain stem projections were not serotonergic, but findings, see Holstege, 1987). Each time a WGA-HRP-labeled terminal presumably contained other transmitters such as various pep- was encountered, it was determined (Table 1) to which type the terminal belonged (for a description of the different terminal types, see Holstege tides (Hokfelt et al., 1979; Mantyh and Hunt, 1984), AChE and Kuypers, 1987a), and it was also determined whether the terminal (Bowker et al., 1983; Jones et al., 1986) or GABA (Millhorn et carried a large number ofgold particles (i.e., whether it was GABAergic). al., 1987). However, until now, it could not be determined in This was considered to be the case if the number of gold particles which area of the spinal cord the nonserotonergic fibers actually overlying the terminal was at least 8 times the number of gold particles overlying nearby unlabeled structures (terminals and dendrites). In ad- terminated or which transmitter these fibers contained. dition, it was determined whether a synapse was present, and if so, the Recently, we have combined the anterograde transport of postsynaptic structure was also identified. In the 16 sections analyzed, WGA-HRP with the postembedding immunogold technique for a total of 505 HRP-labeled terminals were encountered. The results GABA (De Zeeuw et al., 1988). This made it possible to address were expressed as percentages per block. These percentages were av- the above questions, because the 2 markers can be visualized eraged, and standard deviations were calculated. If the numbers ob- tained per block were too small, the percentages were calculated from simultaneously in a single terminal, revealing both its origin and total numbers obtained in all 16 sections. its transmitter content. By means of this technique, it is shown in the present study that a substantial part of the descending Results projections from the ventromedial lower brain stem to lumbar motoneuronal cell groups in the rat contains GABA as a trans- Light microscopic examination of the WGA-HRP injection site mitter, indicating the existence of a monosynaptic inhibitory (Fig. 1) showed that the center of the injection was located in (Kmjevic and Schwartz, 1966) projection from the brain stem the ventromedial part of the lower brain stem at levels between to spinal motoneurons. the caudal part of the facial nucleus and the rostra1part of the inferior olive. It included the gigantocellular reticular nucleus pars ventralis and pars alpha, as well as part of the paragigan- Materials and Methods tocellular reticular nucleus as described by Andrezik and Beitz Four Wistar rats (weighing approximately 300 gm) were deeply anes- (1985). Caudally, the injection site included part of the rostra1 thetized with pentobarbital(60 mg/kg), administered by intraperitoneal injection. WGA-HRP (5% in 0.1 ~1 saline) was injected in the ventral inferior olive, and more rostrally, the injection site encroached part of the medial reticular formation at levels between the caudal part upon the nucleus raphe magnus. Ventromedially, in the pe- of the facial nucleus and the rostra1 half of the inferior olive (see
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