Summary
Responses of 43 pedunculopontine area (PPN area) neurons to electrical stimulation of the substantia nigra (SN) were studied in anesthetized rats. An intracellular recording technique was used to demonstrate that SN stimulation evoked hyperpolarizing potentials, which were identified by intracellular injections as inhibitory postsynaptic potentials (IPSPs). These IPSPs were often followed by a rebound depolarization that originates several spike potentials. These IPSPs were characterized as monosynaptic, with latencies varying from 1.0 to 8.5 ms. Similar results were observed in some animals with chronic unilateral coronal lesion just rostral to subthalamic nucleus (STH), which severed the rostral afferents. PPN area neurons were also antidromically activated by SN stimulation. Two PPN area projection neurons were clearly identified. Mean latency of one group was 0.71 ms; mean latency of the second group was 5.16 ms. The morphological analysis of a neuron inhibited by SN stimulation and labeled with horseradish peroxidase (HRP) demonstrated that the soma was fusiform in shape, with the axon originating in the soma and collaterals and a large dendritic field extending in the ventrodorsalis direction. The results indicate that the PPN area is reciprocally connected with the SN, which elicits an inhibitory effect on PPN area neurons.
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Armstrong DA, Saper CB, Levey AI, Wainer BH, Terry RD (1983) Distribution of cholinergic neurons in the rat brain demonstrated by the immunohistochemical localization of cholineacetyltransferase. J Comp Neurol 200: 53–68
Beckstead RM (1983) Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes. Neuroscience 10: 767–779
Beckstead RM, Domesick VB, Nauta WJH (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175: 191–217
Beninato M, Spencer RF (1987) A cholinergic projection to the rat substantia nigra from the pedunculopontine tegmental nucleus. Brain Res 412: 169–174
Butcher LL, Marchand R, Parent A, Poirier LJ (1977) Morphological characteristics of acetylcholinesterase containing neurons in the CNS of DFP treated monkeys. J Neurol Sci 32: 169–185
Carpenter MB, Betton RR, Carleton SC, Keller JT (1981a) Inter connections and organization of pallidal and subthalamic nucleus neurons in the monkey. J Comp Neurol 197: 579–603
Carpenter MB, Carleton S, Keller JT, Conte P (1981b) Connections of the subthalamic nucleus in the monkey. Brain Res 224: 1–29
Chevalier G, Thierry AM, Shibazaki T, Feger J (1981) Evidence for a GABAergic inhibitory nigrotectal pathway in the rat. Neurosci Lett 21: 67–70
Chevalier G, Vacher S, Deniau JM, Desban M (1985) Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tectospinal/tectodiencephalic neurons. Brain Res 334: 215–226
Clarke PBS, Hommer DW, Pert A, Skirboll LR (1987) Innervation of substantia nigra neurons by cholinergic afferents from pedunculo-pontine nucleus in the rat: neuroanatomical and electrophysiological evidence. Neuroscience 23: 1011–1019
Coombs JS, Eccles JC, Fatt P (1955) The specific ion conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J Physiol (Lond) 130: 326–373
Deniau JM, Chevalier G (1985) Disinhibition as a basic process in the expression of striatal functions. II. The striat-onigral influence on thalamocortical cells of the ventromedial thalamic nucleus. Brain Res 334: 227–233
Deschenes M, Hu B (1990) Membrane resistance increase induced in thalamic neurons by stimulation of brainstem cholinergic afferents. Brain Res 513: 339–342
Di Chiara G, Porceddu NL, Morelli M, Mulas ML, Gessa GL (1979) Evidence for a GABAergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat. Brain Res 176: 273–284
Fonnum F, Storm-Mathisen J (1978) Location of GABAergic neurons in the CNS. In: Iversen LL, Iversen SD, Snyder SH (eds) Handbook of psychopharmacology, chemical pathways in the brain, Vol 9. Plenum Press, New York, pp 357–401
Gould E, Woolf NJ, Butcher LL (1989) Cholinergic projections to the substantia nigra from the pedunculopontine and laterodorsal tegmental nuclei. Neuroscience 28: 611–623
Granata AR, Kitai ST (1989) Intracellular analysis of excitatory subthalamic inputs to the pedunculopontine neurons. Brain Res 488: 57–72
Hammond C, Rouzaire-Dubois B, Feger J, Jackson A, Crossman AR (1983) Anatomical and electrophysiological studies on the reciprocal projections between the subthalamic nucleus and nucleus legmenti pedunculopontinus in the rat. Neuroscience 9: 41–52
Hu B, Steriade M, Deschenes M (1989) The effects of brainstem peribrachial stimulation on neurons of the lateral geniculate nucleus. Neuroscience 31: 13–24
Jackson A, Crossman AR (1981) Basal ganglia and other afferent projections to the peribrachial region in the rat: a study using retrograde and anterograde transport of horseradish peroxidase. Neuroscience 6: 1537–1549
Jackson A, Crossman AR (1983) Nucleus tegmenti pedunculopontinus: efferent connections with special reference to the basal ganglia, studied in the rat by anterograde and retrograde transport of horseradish peroxidase. Neuroscience 10: 725–765
Kang YN, Kitai ST (1990) Electrophysiological properties of pedunculopontine neurons and their postsynaptic responses following stimulation of substantia nigra reticulata. Brain Res 535: 79–95.
Kimura H, McGeer PL, Peng JH, McGeer EG (1981) The central cholinergic system studied by choline acetyltransferase immuno-histochemistry in the cat. J Comp Neurol 200: 151–201
Kita H, Kitai ST (1987) Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260: 435–452
Kitai ST, Kita H (1987) Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia. In: Carpenter MB, Jayaraman A (eds) The basal ganglia II. Plenum Publishing Corp New York, pp 357–373
Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immuno histochemistry and acetylcholinesterase histochemistry. Neuroscience 12: 669–686
Moon-Edley S, Graybiel AM (1983) The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus, pars compacta. J Comp Neurol 217: 187–215
Nakamura Y, Tokumo H, Morizumi T, Kitao Y, Kudo M (1989) Monosynaptic nigral inputs to the pedunculopontine tegmental nucleus neurons which send their axons to the medial reticular formation in the medulla oblongata. An electron microscopic study in the cat. Neurosci Lett 103: 145–150
Nakanishi H, Kita H, Kitai ST (1987) Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res 437: 45–55
Nauta HJW (1979) Projections of the pallidal complex: an auto radiographic study in the cat. Neuroscience 4: 1853–1873
Noda T, Oka H (1984) Nigral inputs to the pedunculopontine region: intracellular analysis. Brain Res 322: 332–336
Noda T, Oka H (1986) Distribution and morphology of tegmental neurons receiving nigral inhibitory inputs in the cat: an intra cellular HRP study. J Comp Neurol 244: 254–266
Nomura S, Mizuno N, Sugimoto T (1980) Direct projections from the pedunculopontine tegmental nucleus to the subthalamic nucleus in the cat. Brain Res 196: 223–227
Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, New York
Saper CB, Loewy AD (1982) Projections of the pedunculopontine tegmental nucleus in the rat: evidence for additional extra pyramidal circuitry. Brain Res 252: 367–372
Satoh K, Fibinger HC (1985a) Distribution of central cholinergic neurons in the baboon (papio papio). I. General Morphology. J Comp Neurol 236: 197–214
Satoh K, Fibinger HC (1985b) Distribution of central cholinergic neurons in the baboon (papio papio). II. A topographic atlas correlated with catecholamine neurons. J Comp Neurol 236: 215–233
Scarnati E, Campana E, Pacitti, C (1984) Pedunculopontine evoked excitation of substantia nigra neurons in the rat. Brain Res 304: 351–361
Scarnati E, Proia A, Campana E, Pacitti C (1986) A microiontophoretic study of the putative neurotransmitter involved in the pedunculopontine substantia nigra pars compacta excitatory pathway of the rat. Exp Brain Res 62: 470–478
Scarnati E, Proia A, Di Loreto S, Pacitti C (1987) The reciprocal electrophysiological influence between the nucleus tegmenti pedunculopontinus and the substantia nigra in normal and decorticated rats. Brain Res 423: 116–124
Spann B, Grofova I (1988) Substantia nigra afferents of the nucleus tegmenti pedunculopontinus in the rat. Soc Neurosci Abstr 14: 1027
Spann B, Grofova I (1989) The origin of ascending and spinal pathways from the nucleus tegmenti pedunculopontinus in the rat. J Comp Neurol 283: 13–27
Sugimoto T, Hattori T (1984) Organization and efferent projections of nucleus tegmenti pedunculopontinus pars compacta with special reference to its cholinergic aspects. Neuroscience 11: 931–946
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Granata, A.R., Kitai, S.T. Inhibitory substantia nigra inputs to the pedunculopontine neurons. Exp Brain Res 86, 459–466 (1991). https://doi.org/10.1007/BF00230520
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DOI: https://doi.org/10.1007/BF00230520