Nigropedunculopontine projection in the rat: An Anterograde tracing study with phaseolus vulgaris-leucoagglutinin (PHA-L)
Bryan M. Spann
Department of Anatomy, Michigan State University, East Lansing, Michigan 48824–1316
Search for more papers by this authorCorresponding Author
Dr. Irena Grofova
Department of Anatomy, Michigan State University, East Lansing, Michigan 48824–1316
Dept. of Anatomy, B-505 West Fee Hall, Michigan State University, East Lansing, MI 48824–1316Search for more papers by this authorBryan M. Spann
Department of Anatomy, Michigan State University, East Lansing, Michigan 48824–1316
Search for more papers by this authorCorresponding Author
Dr. Irena Grofova
Department of Anatomy, Michigan State University, East Lansing, Michigan 48824–1316
Dept. of Anatomy, B-505 West Fee Hall, Michigan State University, East Lansing, MI 48824–1316Search for more papers by this authorAbstract
The termination of the substantia nigra pars reticulata efferents in the nucleus tegmenti pedunculopontinus was studied in the rat by using the anterograde tracer Phaseolusvulgaris-leucoagglutinin (PHA-L). Both large and small injections of PHA-L in various portions of the substantia nigra pars reticulata labeled varicose fibers in the ipsilateral and contralateral nucleus tegmenti pedunculopontinus, subnucleus dissipatus as well as in the ipsilateral nucleus tegmenti pedunculopontinus, subnucleus compactus. However, the bulk of the nigral fibers appeared to terminate in the medial two-thirds of the ipsilateral subnucleus dissipatus of the pedunculopontine nucleus and exhibited a discrete dorsoventral topographical pattern. The terminal plexus displayed patches of uneven density, which was partly due to the numerous fiber bundles passing through the pedunculopontine nucleus, but also to an obvious preference of nigral fibers for some cells. Electron microscopic examination confirmed that nearly all of the varicosities observed in the light microscope contained synaptic vesicles and represented either terminal boutons or boutons en passant. The labeled boutons were elongated (average length: 1.5 μm) and consistently contained a prominent group of mitochondria.
The results suggest that the nigral input to the nucleus tegmenti pedunculopontinus may be directed toward specific subpopulation(s) of pedunculopontine neurons and may influence not only cells in the subnucleus dissipatus, but also in the subnucleus compactus.
LITERATURE CITED
- Arbuthnott, G., and A. K. Wright (1982) Some non-fluorescent connections of the nigroneostriatal dopamine neurons. Brain Res. Bull. 9: 367–378.
- Armstrong, D. A., C. B., Saper, A. I. Levey, B. H. Wainer, and R. D. Terry (1983) Distribution of cholinergic neurons in the rat brain demonstrated by the immunohistochemical localization of choline acetyltransferase. J. Comp. Neurol. 216: 53–68.
- Beckstead, R. M. (1983) Long collateral branches of substantia nigra reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes. Neuroscience 10: 767–769.
- Beckstead, R. M., and A. Frankfurter (1982) The distribution and some morphological features of the substantia nigra neurons that project to the thalamus, superior colliculus and pedunculopontine nucleus in the monkey. Neuroscience 7: 2377–2388.
- Beckstead, R. M., V. B., Domesick, and W. J. H. Nauta (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175: 191–217.
- Beninato, M., and R. F. Spencer (1986) Cholinergic projections to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry. J. Comp. Neurol. 255: 525–538.
- Beninato, M., and R. F. Spencer (1987) A cholinergic projection to the rat substantia nigra from the pedunculopontine tegmental nucleus. Brain Res. 412: 169–174.
- Butcher, L. L., and N. J. Woolf(1984) Histochemical distribution of acetylcholinesterase in the central nervous system: Clues to the localization of cholinergic neurons. In A. Björklund, T. Hökfelt and M. J. Kuhen, (eds): Handbook of Chemical Neuroanatomy. Vol 3: Classical Transmitters and Transmitter Receptors in the CNS 3, Part II. Amsterdam: Elsevier Science, B.V., Ch. I, pp. 1–50.
- Carpenter, M. B., S. C., Carleton, J. T. Keller, and P. Conte (1981) Connections of the subthalamic nucleus in the monkey. Brain Res. 224: 1–29.
- Clarke, P. B. S., D. W., Hommer, A. Pert, and L. R. Skirboll (1987) Innervation of substantia nigra neurons by cholinergic afferents from the pedunculopontine nucleus in the rat: Neuroanatomical and electrophysiological evidence. Neuroscience 23: 1011–1019.
- De Vito, J. L., M. E. Anderson, and K. E. Walsh (1980) A horseradish peroxidase study of afferent connections of the globus pallidus in Macaca mulatto, Exp. Brain Res. 38: 65–73.
- Faull, R. L. M., and W. R. Mehler (1978) The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience 3: 989–1002.
- Garcia-Rill, E. (1986) The basal ganglia and the locomotor region. Brain Res. Rev. 12: 47–63.
- Garcia-Rill, E., and R. D. Skinner (1987a) The mesencephalic locomotor region. I. Activation of a medullary projection site. Brain Res. 411: 1–12.
- Garcia-Rill, E., and R. D. Skinner (1987b) The mesencephalic locomotor region. II. Projections to reticulospinal neurons. Brain Res. 411: 13–20.
- Garcia-Rill, E., C. R., Houser, R. D. Skinner, W. Smith, and D. J. Woodward (1987) Locomotion-inducing sites in the vicinity of the pedunculopontine nucleus. Brain Res. Bull. 18: 731–738.
- Garcia-Rill, E., and R. D. Skinner (1988) Modulation of rhythmic function in the posterior midbrain. Neuroscience 27: 639–654.
- Gerfen, C. R., and P. E. Sawchenko (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: Immunohistochemical localization of an axonally transported plant lectin Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res. 290: 219–238.
- Gerfen, C. R., W. A., Staines, G. W. Arbuthnott, and H. C. Fibiger (1982) Crossed connections of the substantia nigra in the rat. J. Comp. Neurol. 207: 283–303.
- Gonya-Magee, T., and M. E. Anderson (1983) An electrophysiological characterization of projections from the pedunculopontine area to entopeduncular nucleus and globus pallidus in the cat. Exp. Brain Res. 49: 269–279.
- Gould, E., N. J., Woolf, and L. L. Butcher (1989) Cholinergic projections to the substantia nigra from the pedunculopontine and laterodorsal tegmental nuclei. Neuroscience 28: 611–623.
- Groenewegen, H. J., and F. T. Russchen (1984) Organization of the efferent projections of the nucleus accumbens to pallidal, hypothalamic, and mesencephalic structures: A tracing and immunohistochemical study in the cat. J. Comp. Neurol. 223: 347–367.
- Grofova, I., and S. Keane (1991) Descending brainstem projections of the pedunculopontine tegmental nucleus in the rat. Anat. Embryol. (in press). IV.
- Grofova, I., B. M., Spann, and K. Bruce (1991) Involvement of the nucleus tegmenti pedunculopontinus in the descending pathways of the basal ganglia in the rat. In G. Bernard, (ed): Basal Ganglia III: Proceedings of the International Basal Ganglia Society's Third Triennial Meeting. New York: Plenum Press, pp. 153–161.
- Haber, S. N., E., Lynd, C. Klein, and H. J. Groenewegen (1990) Topographical organization of the ventral striatal efferent projections in the rhesus monkey: An anterograde tracing study. J. Comp. Neurol. 293: 282–298.
- Hall, W. C., D., Fitzpatrick, L. L. Klatt, and D. Raczkowski (1989) Cholinergic innervation of the superior colliculus in the cat. J. Comp. Neurol. 287: 495–514.
- Hallanger, A. E., A. I., Levey, H. J. Lee, D. B. Rye, and B. H. Wainer (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J. Comp. Neurol. 262: 105–124.
- Hammond, C., B., Rouzaire-Dubois, J. Féger, A. Jackson, and A. R. Crossman (1983) Anatomical and electrophysiological studies of the reciprocal projections between the subthalamic nucleus and nucleus tegmenti pedunculopontinus in the rat. Neuroscience 9: 41–52.
- Hirsch, E. T., A. M., Graybiel, C. Duyckaerts, and F. Javoy-Agid (1987) Neuronal loss in the pedunculopontine tegmental nucleus in parkinson disease and in progressive supranuclear palsy. Proc. Natl. Acad. Sci. 84: 5976–5980.
- Isaacson, L. G., and D. Tanaka (1986) Cholinergic and non-cholinergic projections from the canine pontomesencephalic tegmentum (Ch5 area) to the caudal intralaminar thalamic nuclei. Exp. Brain Res. 62: 179–188.
- Jackson, A., and A. R. Crossman (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., and A. R. Crossman (1983) Nucleus tegmenti pedunculopontinus: Efferent connections with special references to the basal ganglia, studied in the rat by anterograde and retrograde transport of horseradish peroxidase. Neuroscience 10: 725–726.
- Jellinger K. (1988) The pedunculopontine nucleus in Parkinson's disease, progressive supranuclear palsy and Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 51: 540–543.
- Jones, B. E. (1990) Immunohistochemical study of choline acetyltransferase-immunoreactive processes and cells innervating the pontomedullary reticular formation in the rat. J. Comp. Neurol. 295: 485–514.
- Jones, B. E., and A. Beaudet (1987) Distribution of acetylcholine and catecholamine neurons in the cat brainstem: A choline acetyltransferase and tyrosine hydroxlase immunohistochemical study. J. Comp. Neurol. 261: 15–32.
- Kelland, M. D., and D. Asdourian (1989) Pedunculopontine tegmental nucleus-induced inhibition of muscle activity in the rat. Behav. Brain Res. 34: 213–234.
-
Kilpatrick, I. C., and
M. S. Starr
(1981)
The nucleus tegmenti pedunculopontinus and circling behavior in the rat.
Neurosci. Lett.
26:
11–16.
10.1016/0304-3940(81)90418-3 Google Scholar
- Lee, H. J., D. B., Rye, A. E. Hallanger, A. I. Levey, and B. H. Wainer (1988) Cholinergic vs. noncholinergic efferents from the mesopontine tegmentum to the extrapyramidal motor system nuclei. J. Comp. Neurol. 275: 469–492.
- Mesulam, M.-M., E. J., Mufson, A. I. Levey, and B. H. Wainer (1983) Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10: 1185–1201.
- Mesulam, M.-M., E. J., Mufson, A. I. Levey, and B. H. Wainer (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12: 669–686.
- Mesulam, M.-M., C., Geula, M. A. Bothwell, and L. B. Hersh (1989) Human reticular formation: Cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons. J. Comp. Neurol. 281: 611–633.
- Mitani, A., K., Ito, A. E. Hallanger, B. H. Wainer, K. Kataoka, and R. W. McCarley (1988) Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat. Brain Res. 451: 397–402.
- Mogenson, G. J., L. W., Swanson, and M. Wu (1985) Evidence that projections from substantia innominata to zona incerta and mesencephalic locomotor region contribute to locomotor activity. Brain Res. 334: 65–76.
- Mogenson, G. J., M., Wu, and C. T. Tsai (1989) Subpallidal-pedunculopontine projections but not subpallidal-mediodorsal thalamus projections contribute to spontaneous exploratory locomotor activity. Brain Res. 485: 396–398.
- Moon-Edley, S. M., and M. Graybiel (1983) The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus, pars compacts. J. Comp. Neurol. 217: 187–215.
- Moriizumi, T., Y., Nakamura, H. Tokuno, Y. Kitao, and M. Kudo (1988) Topographic projections from the basal ganglia to the nucleus tegmenti pedunculopontinus pars compacts of the cat with special reference to pallidal projections. Exp. Brain Res. 71: 298–306.
- Nakamura, Y., H., Tokuno, T. Moriizumi, Y. Kitao, and M. Kudo (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.
- Nauta, H. J. W., and W. R. Mehler (1966) Projections of the lentiform nucleus in the monkey. Brain Res. 1: 3–42.
- Noda, T., and H. Oka (1986) Distribution and morphology of tegmental neurons receiving nigral inhibitory input in the cat: An intracellular HRP study. J. Comp. Neurol. 244: 254–266.
- Nomura, S., N., Mizuno, and T. Sugimoto (1980) Direct projections from the pedunculopontine tegmental nucleus to the subthalamic nucleus in the cat. Brain Res. 196: 223–227.
- Olzewski, J., and D. Baxter (1954) Cytoarchitecture of the Human Brain Stem. Philadelphia: J.P. Lippincott.
- Palombo, E., L. J., Porrino, K. S. Bankiewicz, A. M. Crane, L. Sokoloff, and I. J. Kopin (1990) Local cerebral glucose utilization in monkeys with hemiparkinsonism induced by intracarotid infusion of the neurotoxin MPTP. J. Neurosci. 10: 860–869.
- Parent, A. (1986) Comparative Neurobiology of the Basal Ganglia. New York: John Wiley & Sons.
- Parent, A., A., Mackey, Y. Smith, and R. Boucher (1983) The output organization of the substantia nigra in primate as revealed by a retrograde double labeling method. Brain Res. Bull. 10: 529–537.
- Paxinos, G., and L. L. Butcher (1985) Organizational principles of the brain as revealed by choline acetyltransferase and acetylcholinesterase distribution and projections. In G. Paxinos (ed): The Rat Nervous System, Vol. 1: Forebrain and Hindbrain. New York: Academic Press, pp. 487–521.
- Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.
- Rinvik, E., I., Grofova, C. Hammond, J. Feger, and J. M. Deniau (1979) A study of the afferent connections to the subthalamic nucleus in the monkey and the cat using the HRP technique. In L. J. Poirier, T. L. Sourkes, and P. J. Bedard (eds): Advances in Neurology. New York: Raven Press, pp. 53–70.
- Robbins, A., S., Schwartz-Giblin, and D. W. Pfaff (1990) Ascending and descending projections to medullary reticular formation sites which activate deep lumbar back muscles in the rat. Exp. Brain Res. 80: 463–474.
- Rye, D. B., C. B., Saper, H. J. Lee, and B. H. Wainer (1987) Pedunculopontine tegmental nucleus in the rat: Cytoarchitecture, cytochemistry and some extrapyramidal connections of the mesopontine tegmentum. J. Comp. Neurol. 259: 483–528.
- Rye, D. B., H. J., Lee, C. B. Saper, and B. H. Wainer (1988) Medullary and spinal efferents of the pedunculopontine tegmental nucleus and adjacent mesopontine tegmentum in the rat. J. Comp. Neurol. 269: 315–341.
- Sakai, K., Y., Yoshimoto, P. H. Luppi, P. Fort, M. E. Mansari, D. Salvert, and M. Jouvet (1990) Lower brainstem afferents to the cat posterior hypothalamus: A double-labeling study. Brain Res. Bull. 24: 437–455.
- Saper, C. B., and A. D. Loewy (1982) Projections of the pedunculopontine tegmental nucleus in the rat: Evidence for additional extrapyramidal circuitry. Brain Res. 252: 367–372.
- Scarnati, E., E., Campana, and C. Pacitti (1984) Pedunculopontine-evoked excitation of substantia nigra neurons in the rat. Brain Res. 304: 351–361.
- Scarnati, E., A., Gasbarri, E. Campana, and C. Pacitti (1987a) The organization of nucleus tegmenti pedunculopontinus neurons projecting to basal ganglia and thalamus: A retrograde fluorescent double labeling study in the rat. Neurosci. Lett. 79: 11–16.
- Scarnati, E., A. Proia, S. Di Loreta, and C. Pacitti (1987b) The reciprocal electrophysiological influence between the nucleus tegmenti pedunculopontinus and the substantia nigra in normal and decorticated rats. Brain Res. 423: 116–124.
- Schneider, J. S. (1986) Interactions between the basal ganglia, the pontine parabrachial region, and the trigeminal system in the cat. Neuroscience 19: 411–425.
- Sofroniew, M. V., J. V., Priestly, A. Consolazione, F. Eckenstien, and A. C. Cuello (1985) Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry. Brain Res. 329: 213–223.
- Spann, B. M., and I. Grofova (1988) Substantia nigra afferents of the nucleus tegmenti pedunculopontinus in the rat. Neurosci. Abstr. 14: 1027.
- Spann, B. M., and I. Grofova (1989) Origin of ascending and spinal pathways from the nucleus tegmenti pedunculopontinus in the rat. J. Comp. Neurol. 283: 13–27.
- Steriade, M., S., Datta, D. Pare, G. Oakson, and R. Curró Dossi (1990a) Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems J. Neurosci. 10: 2541–2559.
- Steriade, M., D., Pare, S. Datta, G. Oakson, and R. Curró Dossi, (1990b) Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves. J. Neurosci. 10: 2560–2579.
- Sugimoto, T., and T. Hattori (1984) Organization and efferent projections of nucleus tegmenti pedunculopontinus pars compacts with special reference to its cholinergic aspects. Neuroscience 11: 931–946.
- Swanson, L. W., G. J., Mogenson, C. R. Gerfen, and P. Robinson (1984) Evidence for a projection from the lateral preoptic area and substance innominata to the “mesencephalic locomotor region” in the rat. Brain. Res. 295: 161–178.
- Vincent, S. R., K., Satoh, D. M. Armstrong, and H. C. Fibiger (1983) Substance P in the ascending cholinergic reticular system. Nature 306: 688–691.
- Woolf, N. J., and L. L. Butcher (1986) Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia and basal forebrain. Brain Res. Bull. 16: 603–637.
- Zweig, R. M., W. R., Jankel, J. C. Hedreen, R. Mayeux, and D. L. Price (1989) The pedunculopontine nucleus in Parkinson's disease. Ann. Neurol. 26: 41–46.
- Zweig, R. M., P. J., Whitehouse, M. F. Casanova, L. C. Walker, W. R. Jankel, and D. L. Price (1987) Loss of pedunculopontine neurons in progressive supranuclear palsy. Ann. Neurol. 22: 18–25.