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Medial Lemniscal and Spinal Projections to the Macaque Thalamus

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Medial Lemniscal and Spinal Projections to the Macaque Thalamus The Journal of Neuroscience, May 1994, 14(5): 2485-2502 Medial Lemniscal and Spinal Projections to the Macaque Thalamus: An Electron Microscopic Study of Differing GABAergic Circuitry Serving Thalamic Somatosensory Mechanisms Henry J. Ralston III and Diane Daly Ralston Department of Anatomy, W. M. Keck Foundation Center for Integrative Neuroscience, University of California, San Francisco, California, 94143-0452 The synaptic relationships formed by medial lemniscal (ML) jority of these spinal afferents suggests that the transmis- or spinothalamic tract (STT) axon terminals with neurons of sion of noxious information is probably not subject to GA- the somatosensory ventroposterolateral thalamic nucleus of BAergic modulation by thalamic interneurons, in contrast to the macaque monkey have been examined quantitatively by the GABAergic processing of non-noxious information car- electron microscopy. ML and STT axons were labeled by the ried by the ML afferents. The differences in the GABAergic anterograde axon transport of WGA-HRP following injection circuits of the thalamus that mediate ML and STT afferent of the tracer into the contralateral dorsal column nuclei, or information are believed to underlie differential somatosen- the dorsal horn of the spinal cord, respectively. Thalamic sory processing in the forebrain. We suggest that changes tissue was histochemically reacted for the presence of HRP. in thalamic GABAergic dendritic appendages and GABA re- Serial thin sections were stained with a gold-labeled anti- ceptors following CNS injury may play a role in the genesis body to GABA, to determine which neuronal elements ex- of some central pain states. hibited GABA immunoreactivity (GABA-ir). Serially sec- [Key words: thalamus, somatosensory, monkey, GABA, tioned thalamic structures were recorded in electron medial lemniscus, spinothalamic tract, inhibition, interneu- micrographs and reconstructed in three dimensions by com- ron, pain] puter. Individual ML axon terminals form multiple synaptic con- Several studiesof the neuronal and synaptic organization of the tacts with segments of the proximal dendritic trees of thal- thalamus of monkey and of cat have revealed a complex cir- amocortical relay neurons and also synapse upon the den- cuitry for processingafferent information (reviewed in Ralston, dritic appendages of GABA-ir interneurons (local circuit 1983, 199 1; Jones, 1985). Thalamic nuclei contain two neuronal neurons). These GABA-ir dendritic appendages contain syn- cell types: (1) the thalamocortical relay cell, usually about 20- aptic vesicles and are presynaptic (presynaptic dendrites) 40 Km in cell body diameter, which projects to functionally to the same segments of relay neuron dendrites that receive related regions of the cerebral cortex and which constitutes ap- ML contacts. When analyzed in serial sections and recon- proximately 75-90% of the total complement of neurons, and structed by computer, the ML terminals form triadic rela- (2) the interneuron (local circuit neuron), which representsap- tionships (ML, GABA appendage, and relay neuron dendrite) proximately lo-25% of the total neuronal population (Le Vay, or more complex glomerular arrangements involving multiple 197 1; Hamori and Pasik, 1983) and which exhibits GABA im- appendages, all of which then contact the relay neuron den- munoreactivity (GABA-ir; Spreafico et al., 1983). When stained dritic segment. In contrast, multiple STT terminals make syn- by the Golgi method (Guillery, 1966; Szentagothai et al., 1966) aptic contacts along segments of projection neuron den- or labeled by the intracellular iontophoresis of HRP (Hamos et drites and are usually the only type of profile to contact that al., 1985; Yen et al., 1985; Ohara et al., 1987;Wilson, 1989) the segment of dendrite. More than 85% of the spinal afferents intemeurons have been shown to be morphologically distinct form simple axodendritic synapses with relay cells and do from relay cells, being approximately 10-l 5 Frn in cell body not contact GABA-ir appendages. diameter and to possesscomplex dendritic appendages.The The thalamic synaptic relationships of ML terminals are thalamocortical relay cells lack these dendritic appendages. fundamentally different from those formed by the STT. Be- The first electron microscopic study of the primate thalamus cause STT neurons predominately transmit information about (LGN, Colonnier and Guillery, 1964) showed that the retinal noxious stimuli, the simple axodendritic circuitry of the ma- afferents contained rounded synaptic vesiclesand were the larg- est synaptic profile present (designated RL profiles). The RL retinal terminals not only contacted the dendrites of relay cells, Received Apr. 28, 1993; revised Oct. 1, 1993; accepted Oct. 19, 1993. but were also presynaptic to vesicle-containing profiles that, in We thank Ms. Antonia M. Milroy for her expertise in preparing the experimental turn, contacted the relay cell dendrites to form a triadic synaptic material for electron microscopy and Ms. Sandra Canchola for her expert assis- tance in the preparation of the light microscopic material and the photographic relationship. Thesepostsynaptic vesicle-containing profiles were plates. This work was supported by NS 23347 and NS 2 1445 from the National subsequently shown to be the dendritic appendagesof inter- Institutes of Health. Correspondence should be addressed to Henry J. Ralston III, Department of neurons (Ralston and Herman, 1969; Ralston, 1971) to be Anatomy, University of California, San Francisco, CA 94143-0452. GABA-ir (Hendrickson et al., 1983; Ohara et al., 1989; Kultas- Copyright 0 1994 Society for Neuroscience 0270-6474/94/142485-18$05.00/O Ilinsky and Ilinsky, 199l), and to be presynaptic, and have thus 2466 Ralston and Ralston * Thalamic Somatosensory Afferents and GABAergic Circuitry been called presynaptic dendrites. In some cases the retinal (cat The animals were housed and cared for pre- and postoperatively ac- LGN; Rapisardi and Miles, 1984) or lemniscal (cat ventropos- cording to the NIH and the USDA renulations alone with the euidance of the-committee for Animal Research of UCSF and the veterinary terolateral nucleus, VPL, Ralston, 1969; monkey VPL, Ralston, care of the Animal Care Facility of the University of California at San 199 1) afferent axon terminals form complex synaptic structures Francisco. Following approved protocol, the animals were immobilized (glomeruli), in which the afferent synapses upon a relay cell with ketamine hydrochloride (10 ma/kg.- -_ i.m.) and anesthetized with dendritic shaft and multiple intemeuronal dendritic appendages sodium pentobarbital(1: 1 in isotonic saline, i.v.), titrated to an appro- priate anesthetic level for surgery and the anesthesia maintained with simultaneously. The vesicle-filled appendages, in turn, contact a pentobarbital intravenous infusion of 5 mg/kg/hr. the relay cell dendrite. These relationships between afferent, ML projections were studied in four animals, each being placed in a relay cell, and GABA-ir appendages presumably serve a fun- Kopf stereotaxic head holder using an inverted mouthpiece to hold the damental aspect of information transfer in the thalamus, in head in a flexed position. Using sterile surgical techniques, a midline which the afferent axon transmits an excitatory message to the incision and reflection of muscle were performed at the level of the caudal occiput to expose the atlanto-occipital membrane, which was relay cell and to the GABAergic appendages, resulting in feed- then incised in order to visualize the dorsal column nuclei. Five percent forward GABAergic inhibition of the relay cell by the intemeu- wheat germ agglutinin conjugated to horseradish peroxidase (WGA- ronal dendritic appendages (Pare et al., 199 1). HRP) in sterile saline was pressure injected into the cuneate nucleus, Two major somatosensory afferent pathways, the medial lem- using a Hamilton syringe onto which was attached a micropipette with a tip diameter of 40-50 pm. Injections were placed approximately 2 niscus (ML) and the spinothalamic tract (STT), project to the mm apart and each injection consisted of 0.02-0.04 ~1 in volume, the ventroposterolateral nucleus (VPLc; Olszewski, 1952) of the total volume injected being approximately 0.1 ~1. In the seven animals thalamus in the primate (Boivie, 1978, 1979). The projections used for spinothalamic projections, the cervical (n = 4) or the lumbar of the ML to VPLc arise from the dorsal column nuclei of the (n = 3) enlargementof the spinalcord wassurgically exposed after a caudal brainstem. The major modalities conveyed by this sys- laminectomy and 5% WGA-HRP was pressure injected into the dorsal horn of the cord, medial to the dorsal root entry zone. Iniections were tem (e.g., touch, vibration, pressure) arise from rapidly and placed approximately 2 mm apart rostrocaudally and eachinjection was slowly adapting low-threshold (non-noxious) cutaneous mech- 0.024.04 ~1 in volume, the total volume iniected over the enlareement anoreceptors, as well as some inputs from muscles and joints. being approximately 0.14 ~1, labeling about two or three cons&utive A few cells in nucleus gracilis have been shown to receive con- spinal segments. The injections labeled extensive regions of the dorsal and ventral horn gray matter (see Fig. 1 in Ralston and Ralston, 1992). vergent input from low-threshold and high-threshold (noxious) The animals survived for 3-5 d to minimize transneuronal labeling cutaneous mechanoreceptors (Ferrington et al., 1988).
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