GABA and Glycine as Inhibitory Neurotransmittersin the Vestibuloocular Reflex" ROBERT F. SPENCERb AND ROBERT BAKER'

bDepartment of Anatomy Medical College of Ktginia 1101 East Marshall Street Richmond, Ktginia 23298-0709 'Department of Physiology and Biophysics New York University Medical Center 550 First Avenue New York, New York 10016 Considerable knowledge has accumulated regarding the morphological, physiological, and functional organization of the vestibular system. The basic three-neurone chain, comprising primary and secondary vestibular neurones and motoneurones in the extraocular motor nuclei, is a necessary component of the vestibuloocular reflex (VOR). It is clear, however, that other neurones in the nucleus prepositus hypoglossi and the cerebellum, as well as vestibular commissural connections, have an important role in its normal operation. Inhibition mediated by second-order vestibular neurones is a fundamentally important aspect of the reciprocal excitatory and inhibitory synaptic inputs to extraocular motoneurones in the VOR. Although inhibition at the level of the motoneurones undoubtedly is important in providing a rapid, effective relaxation of antagonistic extraocular muscles, it appears not to be involved in determining, at least directly, the response properties (e.g., head velocity, eye position sensitivities) and discharge patterns (i.e., burst, burst/tonic) of these neurones. Rather, inhibitory mechanisms at all levels in the vestibuloocular circuitry may be important in shaping the excitatory networks that ultimately control the dynamic properties of the VOR. Even at the level of the extraocular motoneurones, however, inhibition is important to the extent that the reciprocal excitatory and inhibitory inputs overlap with respect to firing threshold, thus creating a larger dynamic response than otherwise would be present with either input alone. The types of ncurotransmitters [i.e., y-aminobutyric acid (GABA), glycine] utilized by inhibitory inputs and the postsynaptic receptors with which they are associated furthermore may translate into differences in the postsynaptic effects of interacting excitatory and inhibitory inputs. Consequently, the identification of the inhibitory neurotransmitters utilized in various circuits in the vestibuloocular system and the various types of receptors with which they are associated is of fundamental importance to further defining the role of such interactions in normal eye movements and the extent to which they are involved in eye movement deficits.

aThis work was supported by U.S. Public Health Service MERIT Award EY02191 and Research Grant EY02007 from the National Eye Institute. 602

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ROLE OF GABA AS AN INHIBITORY NEUROTRANSMITTER IN THE VESTIBULOOCULAR SYSTEM Electrophysiological, pharmacological, and biochemical studies have established that GABA is the inhibitory neurotransmitter utilized by second-order vestibular neurones that establish synaptic connections with motoneurones in the oculomotor and trochlear nuclei. Systemic administration of picrotoxin, an antagonist of GABA, abolishes the depression of the antidromic field potential recorded extracellularly in the oculomotor nucleus following IIIrd nerve stimulation and eliminates the extracelMar positive field potentials that represent the inhibitory postsynaptic currents resulting from ipsilateral VIIIth nerve stimulation.' Iontophoresis of GABA in the vicinity of the oculomotor nucleus depresses the antidromic field potential elicited by IIIrd nerve stimulation and decreases or completely suppresses the spike generation of motoneurones in a manner similar to that produced by electrical stimulation of the ipsilateral VIIIth nerve.' The inhibitory responses elicited by VIIIth nerve stimulation and GABA iontophoresis furthermore are blocked by iontophoresis of picrotoxin in the vicinity of the motoneurones. Picrotoxin also blocks the slow muscle potential recorded from the extraocular muscles in a manner similar to removal of the second-order vestibular input to oculomotor motoneurones following lesions of the dorsolateral brain stem that effectively interrupt the inhibitory vestibular pathway.' These electrophysiological and pharmacological findings are supported further by anatomical studies that have demonstrated synaptic endings in the oculomotor nucleus labeled autoradiographically by high-affinity uptake of [ZH]GABA4.5or immunohistochemically by the localization of GABA'-7 or its synthesizing enzyme glutamate decarboxylase (GAD).6Within the oculomotor nucleus, GABA-immunoreactive synaptic endings are found predominantly within the inferior rectus, superior rectus, and inferior oblique subdivisions. Consistent with the absence of vestibularevoked inhibitory postsynaptic potentials (IPSPs) in medial rectus motoneurones," the medial rectus subdivision is virtually devoid of GABA-/GAD-immunoreactive synaptic endings. The density of GABA-immunoreactive synaptic endings in the various subdivisions of the oculomotor nucleus furthermore is higher in the Rhesus monkey than in the cat. Correlated at least in part with the high density of GABA-immunoreactive terminals within the oculomotor nucleus, GABA-immunoreactive axons also are observed predominantly in the medial portion of the medial longitudinal fasciculus (MLF) lateral to the nucleus (FIGURE 1A). In the trochlear nucleus, systemic administration of picrotoxin significantly reduces or abolishes both the inhibitory synaptic current recorded extracellularly and the IPSPs recorded intracellularly from motoneurones following electrical stimulation of the ipsilateral VIIIth nerve." A similar depressant action on vestibularevoked inhibition is obtained by systemically administered bicuculline. Unilateral section of the MLF, which abolishes the vestibular-evoked inhibitory synaptic currents, reduces the concentration of GABA in the trochlear nucleus. Lesions of the superior vestibular nucleus also produce a marked decrease in GABA synthesis in the ipsilateral trochlear nucleus.'" Of the three extraocular motor nuclei, the trochlear nucleus has the highest density of GABA-immunoreactive synaptic endi n g ~ " .(FIGURE ~ 1C). The soma-dendritic distribution of many GABA-/GADimmunoreactive synaptic endings, combined with the presence of multiple synaptic contact zones associated with individual synaptic endings, is a feature typical of the inhibitory second-order vestibular input to oculomotor and trochlear motoneurones identified previously by ultrastructural reconstructions of physiologically identified axons stained intracellularly with horseradish peroxidase (HRP)." Ventral to the

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trochlear nucleus, GABA-immunoreactive axons are found predominantly in the dorsal half of the MLF, suggesting that the axons are segregated in the MLF according to their origin (e.g., vestibular, abducens internuclear) and/or function (i,e., inhibitory vs. excitatory).

FIGURE 1. Imrnunohistochemical localization of GABA (A, C, and E) and glycine (B, D, and F) in the cat oculomotor (3; A and B), trochlear (4;C and D) and abducens (6; E and F) nuclei and the MLF (mlf). Calibration: 0.5 rnrn.

ROLE OF GLYCINE AS AN INHIBITORY NEUROTRANSMITTER IN THE VESTIBULOOCULAR SYSTEM GABA also was thought initially to be the inhibitory neurotransmitter mediating vestibular-evoked inhibition in the abducens nucleus. Both the antidromic field

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potentials and orthodromic synaptic currents recorded extracellularly following VIth and VIIIth nerve stimulation, respectively, were reduced when picrotoxin was administered systemically in the rabbit.'* A more recent comprehensive autoradiographic, immunohistochemical, and electrophysiological-pharmacologicalanalysis in the cat, however, has revealed that, in contrast to the oculomotor and trochlear nuclei, inhibitory inputs to the abducens nucleus from second-order newones in the vestibular nucleus, as well as from neurones in the dorsolateral medullary reticular formation and the prepositus hypoglossi nucleus, utilize glycine as a neurotransmitter.' The different populations of inhibitory premotor neurones are labeled selectively by retrograde transport of [-'H]glycine, but not [3H]GABA, injected into the abducens nucleus. Correlated with these findings, the abducens nucleus exhibits a high density of glycine-immunoreactive synaptic endings (FIGURE IF), but a paucity of GABA-immunoreactive terminals (FIGURE IE). By contrast, the oculomotor (FIGURE 1B) and trochlear (FIGURE 1D) nuclei contain very few glycine-immunoreactive synaptic endings. In the oculomotor nucleus in the monkey, glycineimmunoreactive terminals are confined specifically to the superior rectus subdivision, whereas in the cat similar terminals appear to be distributed to the other (except medial rectus) motoneurone subdivisions as well. The source of this modest glycinergic input to the oculomotor nucleus presently is unknown. In further contrast to oculomotor and trochlear motoneurones, the vestibular inhibition of abducens motoneurones evoked by selective horizontal canal nerve electrical stimulation is abolished by strychnine, but is unaffected by picrotoxin or bicuculline administered systemically (FIGURE 2A-C). Most, if not all, of the glycine-immunoreactive synaptic endings in the abducens presumably are related to glycine-immunoreactive neurones that are located in the same areas as neurones labeled by retrograde transport of ['Hlglycine from the abducens nucleus. The complementary pattern of GABA and glycine localization in the extraocular motor nuclei is correlated with a distinctive pattern of immunoreactive staining in the MLF. GABA is associated predominantly with ascending axons that project to the oculomotor and trochlear nuclei (FIGURE 1A and C). By contrast, glycine is localized predominantly in descending axons that project to the abducens nucleus and the spinal cord (FIGURES 1F and 3F). Occasional GABA-immunoreactive axons that presumably are of vestibular commissural origin course transversely through the abducens nucleus, and only a few GABA-immunoreactive axons are observed in the MLF at this level of the brain stem. The paradoxical differences in inhibitory neurotransmitters utilized by vertical and horizontal canal-related vestibular neurones also may be correlated with the differential roles of GABA and glycine in vestibular commissural inhibiti~n".'~ and the differential association of GABA, and strychnine-sensitive glycine receptors with neurones in the vestibular nucleus." IMMUNOHISTOCHEMICAL LOCALIZATION OF GABA AND GLYCINE IN THE VESTIBULAR NUCLEI

Immunohistochemical studies of GABA localization only partially support the substantive physiological, biochemical, and pharmacological data cited above regarding the role of GABA as the inhibitory neurotransmitter in vestibuloocular reflex connections. For example, few or no GABA-immunoreactive neurones have been found in the superior vestibular n u c l e ~ s ,despite ~ ~ ' ~ evidence that both anterior and posterior vertical canal-related inhibitory second-order vestibular neurones are located in this region. By contrast, GABA-immunoreactive neurones have been observed predominantly in the medial and inferior vestibular nuclei. A population of

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2 rng/kg Picrotoxin

A 3 mg/kg Strychnine

B fi

2 rng/kg Strychnine

C FIGURE 2. A and B Extracellular recordings demonstrating the different effects of systemically administered picrotoxin (A) and strychnine (B) on inhibitory postsynaptic field potentials in the abducens nucleus following ipsilateral vestibular nerve stimulation. Arrows at 2 mseconds latency indicate the peak of the postsynaptic response. C: intracellular records from an abducens motoneurone following ipsilateral vestibular nerve stimulation demonstrating a rapid decrease in the rise time and peak amplitude of the IPSP following systemic administration of strychnine. Calibrations: 1 mV and 0.5 msecond. Negative polarity is downward.

intrinsic GABAergic neurones also has been described in the dorsal division of the lateral vestibular nucleus." Neurones in the medial and inferior vestibular nuclei that project to the spinal cord also are immunoreactive toward GAD.2'Other evidence, however, suggests that glycine is involved in these vestibulospinal connections. For example, the vestibularevoked disynaptic IPSPs in neck motoneurones are effectively blocked by strychnine, a glycine antagonist.22 Presumed glycinergic inhibitory vestibular neurones that project to the ipsilateral abducens nucleus have axonal branches that descend in the ipsilateral MLF toward the spinal ~ o r d . ~Possibly . * ~ related, at least in part, to these descending inhibitory axons, spinal cord ventral horn motoneurones exhibit a high density of glycine receptors.2s*26 At present, it is difficult to resolve these apparent disparate findings in regard to the locations of known populations of inhibitory vestibular neurones and the

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neurotransmitters with which they are associated. O n the one hand, since verticalcanal-related inhibitory second-order vestibular neurones are projection neurones, it is possible that, like cerebellar Purkinje cells, the concentration of GABA within the somata of the neurones is significantly less than that at their synaptic endings in the oculomotor and trochlear nuclei and cannot be detected immunohistochemically. Consequently, the above studies may not have identified the total population of GABAergic neurones in the vestibular nuclei, particularly within the superior vestibular nucleus. The specificity of various antibodies used for the immunohistochemical localization of GABA and glycine, as well as possible differences between species in the locations of neurotransmitter-specific populations of neurones, also may be a factor. In the cat, both GABA-immunoreactive and glycine-immunoreactive neurones are found in the superior, medial, and descending (inferior) vestibular nuclei. Within the superior vestibular nucleus, the two populations of neurones are located predomi-

FIGURE 3. Immunohistochemical localization of GABA (A, C, and E) and glycine (B, D, and F) in the cat superior (SVN), medial (MVN), and descending (DVN) vestibular nuclei. Calibration: 1 mm.

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nantly in the central region of the nucleus among immunoreactive axons that appear to be derived from the cerebellum and/or the vestibular nuclei (FIGURE3A and B). GABA-immunoreactive neurones significantly outnumber glycine-immunoreactive neurones within this nucleus. Both GABA-immunoreactive (FIGURE3C and E) and glycine-immunoreactive (FIGURE3D and F) neurones also are distributed throughout the rostral-caudal extent of the medial and descending vestibular nuclei. Despite their coexistence within these regions, they appear to comprise separate populations of neurones on the basis of their size and morphology. Consistent with this premise, the descending limb of the MLF at caudal levels of the brain stem contains a large number of glycine-immunoreactive axons (FIGURE3F), but few, if any, GABAimmunoreactive axons (FIGURE3E). The GABA-immunoreactive neurones in the medial and descending vestibular nuclei thus appear to have different connections, possibly related to vestibular commissural interactions. It is also possible that neurones may co-localize GABA and glycine” or that GABAergic synaptic endings are associated with glycine receptor^.^' Thus, neurones in all of the vestibular nuclei may exhibit GABA or GAD immunoreactivity irrespective of whether they utilize GABA as a neurotransmitter. In this regard, the co-localization of GABA and glycine, as well as their co-localization with putative excitatory amino acid neurotransmitters, may indicate a metabolic pool of one that is unrelated to the neurotransmitter function of another. Despite the co-localization of GABA and glycine in single vestibular neurones, in most instances only one or the other appears to have a synaptic effect, as indicated by the specificity of pharmacological antagonism.” This effect presumably is dictated by the type and presence of the postsynaptic receptor with which the input is associated. Indeed, the functional effects produced by a single neurotransmitter appear to be directly dependent on the type of postsynaptic receptor, as demonstrated by the differential roles of GABA acting on GABA, and GABA, receptors in neural integrator and velocity storage mechanisms, respectively, in the vestibular nuclei through vestibular commissural and cerebellar pathway^.^"^"

CONCLUSION It is well established that GABA is the major inhibitory neurotransmitter utilized by prernotor neurones involved in vertical vestibuloocular eye movements. By contrast, glycine is the inhibitory neurotransmitter of most premotor neurones that are related to horizontal eye movements. The significance of this dichotomy in inhibitory neurotransmitters utilized in the vertical and horizontal eye movement systems presently is unclear. On the one hand, it might reflect functional differences between different types of neurones, distinguishing, for example, between secondorder vestibular neurones that participate only in eye movement (e.g., GABAergic inhibitory neurones in the superior vestibular nucleus that project only to the trochlear and/or oculomotor nuclei) versus those that are involved in gaze (e.g., glycinergic inhibitory neurones in the medial vestibular nucleus that project to both the abducens nucleus and the spinal cord). Although the postsynaptic effect of GABA or glycine acting on its respective receptor is the same, namely, inhibition of the motoneurones, the secondary effects of the two neurotransmitters, however, may be quite different. For example, the excitatory effects of glutamate activating N-methyl-D-aspartic acid (NMDA) receptors are augmented by glycine acting on strychnine-insensitive glycine receptors. These factors, however, probably do not

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translate into apparent differences in the way motoneurones produce vertical o r horizontal eye movements. O n the other hand, these differences in neurotransmitters utilized in the vertical and horizontal eye movement systems may have an embryological basis, which, in the simplest case, might reflect that the medulla, in which most of the horizontal premotor neurones are located, is a rostra1 extension of the spinal cord where glycine is the major inhibitory neurotransmitter, while the midbrain, which is the location o r site of termination of the vertical premotor neurones, is more closely associated with the forebrain where GABA is the major inhibitory neurotransmitter. The association of specific homeodomain proteins with specific neuromeric segments during embryogenesis is correlated with the rhombomeric origin of ascending vestibuloocular and descending vestibulospinal neurones (reviewed in Reference 31). For example, Hox 2.9 is associated only with rhombomere 4 from which vestibulospinal neurones originate, while Wnt-1 is associated with rhombomeres 5 and 6 from which vestibuloocular neurones originate. These DNA-binding proteins are likely to be causal factors that promote the expression by up or down regulation of families of genes that cause a cell to differentiate into a particular type of neurone. As part of this differentiation process, a neurone will express a particular neurotransmitter and will project its axon to a particular location. Thus, the organization of vestibuloocular and vestibulospinal projections into coherent groups is a type of regional specificity that further suggests an early embryonic specification of neurotransmitters. Given the findings from our studies in the adult, this hypothesis could be tested directly by comparing the developmental pattern of identified inhibitory neurones that utilize glycine or GABA as a neurotransmitter and that project to the abducens nucleus and spinal cord o r the oculomotor and trochlear nuclei, respectively.

ACKNOWLEDGMENTS

W e are grateful to Dr. Robert J. Wenthold for generously providing the antibodies to GABA and glycine. The excellent technical assistance of Lynn Davis also is greatly appreciated.

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GABA and glycine as inhibitory neurotransmitters in the vestibuloocular reflex.

GABA and Glycine as Inhibitory Neurotransmittersin the Vestibuloocular Reflex" ROBERT F. SPENCERb AND ROBERT BAKER' bDepartment of Anatomy Medical Co...
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