Skip to main content
SpringerLink
Log in

Cholinergic and non-cholinergic neurons in the rat pedunculopontine tegmental nucleus

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

Choline acetyltransferase immunhistochemistry was employed at light and electron microscopic levels in order to determine the distribution of cholinergic neurons in two subdivisions of the rat pedunculopontine tegmental nucleus that were previously defined on cytoarchitectonic grounds, and to compare the synaptic inputs to cholinergic and non-cholinergic somata in the subnucleus dissipatus, which receives major input from the substantia nigra. Large cholinergic neurons were found in both the pars compacta and the pars dissipata of the pedunculopontine nucleus. However, they were intermingled with non-cholinergic neurons and did not respect the cytoarchitectural boundaries of the nucleus. Ultrastructural study showed that all cholinergic neurons in the subnucleus dissipatus exhibited similar features. The majority had large somata (largest diameter ⩾20 μm) containing abundant cytoplasmic organelles and nuclei displaying a few shallow invaginations. Synaptic terminals on the cholinergic cell bodies were scarce and unlabeled boutons containing spherical synaptic vesicles and establishing asymmetric synaptic junctions were the dominant type. In contrast, the non-cholinergic neurons presented prominent differences in the size of their somata as well as in the distribution of axosomatic synapses. Two almost equally represented classes of non-cholinergic neurons which are referred to as large (largest diameter ⩾20 μm) and small (largest diameter <20 μm) were recognized. Large non-cholinergic cell bodies were ultrastructurally similar to the cholinergic ones, but they received rich synaptic input by unlabeled nerve terminals which contained pleomorphic vesicles and were engaged in symmetric synaptic junctions. Small non-cholinergic cell bodies were characterized by deeply invaginated nuclei surrounded by a narrow rim of cytoplasm, and were often found near or in direct apposition to the cholinergic somata. Their major input consisted of axosomatic boutons containing round synaptic vesicles. These results demonstrate that cells in the pedunculopontine tegmental nucleus are differentiated with regard to their axosomatic synaptic inputs which may influence their firing properties. Furthermore, they support previous suggestions that nigral afferents may be preferentially distributed to a subpopulation of the pedunculopontine neurons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

cp :

cerebral peduncle

CG :

central gray

CNF :

cunei-form nucleus

LPB :

lateral parabrachial nucleus

ml :

medial lemn-iscus

MPB :

medial parabrachial nucleus

me5 :

mesencephalic tri-geminal tract

Me5 :

nucleus of the mesencephalic tract of the trige-minal nerve

Mo5 :

motor trigeminal nucleus

PPNc :

pedunculo-pontine nucleus, subnucleus compactus

PPNd :

pedunculopontinenucleus subnucleus dissipatus

rs :

rubrospinal tract

RPo :

pontinereticular nucleus, oral portion

RR :

retrorubral nucleus

RRF :

re-trorubral field

scp :

superior cerebellar peduncle

SNr :

substantianigra, pars reticulata

SPTg :

subpeduncular tegmental nucleus

3n :

oculomotor nerve

References

  • Armstrong DA, Saper CB, Levey AI, Wainer BH, Terry RD (1983) Distribution of cholinergic neurons in the rat brain demonstrated by immunohistochemical localization of choline acetyl-transferase. J Comp Neurol 216:53–68

    Google Scholar 

  • Beckstead RM (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

    Google Scholar 

  • Beckstead RM, Frankfurter A (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

    Google Scholar 

  • Beninato M, Spencer RF (1986) Cholinergic projections to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry. J Comp Neurol 253:525–538

    Google Scholar 

  • Beninato M, Spencer RF (1987) A cholinergic projection to the rat substantia nigra from the pedunculopontine tegmental nucleus. Brain Res 412:169–174

    Google Scholar 

  • Beninato M, Spencer RF (1988) The cholinergic innervation of the rat substantia nigra: a light and electron microscopic immunohistochemical study. Exp Brain Res 72:178–184

    Google Scholar 

  • Bolam JP, Francis CM, Henderson Z (1991) Cholinergic input to dopaminergic neurons in the substantia nigra: a double immunocytochemical study. Neuroscience 41:483–494

    Article  CAS  PubMed  Google Scholar 

  • Carpenter MB, Strominger NL (1967) Efferent fiber projections of the subthalamic nucleus in the rhesus monkey. A comparison of the efferent projections of the subthalamic nucleus, substantia nigra and globus pallidus. Am J Anat 121:41–72

    Google Scholar 

  • Carpenter MB, Carleton SC, Keller JT, Conte P (1981) Connections of the subthalamic nucleus in the monkey. Brain Res 224:1–29

    Google Scholar 

  • Clarke PBS, Hommer DW, Pert A, Skirboll LR (1987) Innervation of substantia nigra neurons by cholinergic afferents from the pedunculopontine nucleus in the rat: Neuroanatomical and electrophysiological evidence. Neuroscience 23:1011–1019

    Article  CAS  PubMed  Google Scholar 

  • De Lima AD, Singer W (1987) The brainstem projection to the lateral geniculate nucleus in the cat: Identification of cholinergic and monoaminergic elements. J Comp Neurol 259:91–121

    Google Scholar 

  • DeVito JL, Anderson ME (1982) An autoradiographic study of efferent connections of the globus pallidus in Macaca mulatta. Exp Brain Res 46:107–117

    Google Scholar 

  • DeVito JL, Anderson ME, Walsh KE, (1980) A horseradish peroxidase study of afferent connections of the globus pallidus in Macaca mulatta. Exp Brain Res 38:65–73

    Google Scholar 

  • Fitzpatrick D, Diamond IT, Raczkowski D (1989) Cholinergic and monoaminergic innervation of the cat thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. J Comp Neurol 288:647–675

    Google Scholar 

  • Goldsmith M, van der Kooy D(1988) Separate non-cholinergic descending projections and cholinergic ascending projections from the nucleus tegmenti pedunculopontinus. Brain Res 445:386–391

    Google Scholar 

  • Gould E, Butcher L (1986) Cholinergic neurons in the rat substantia nigra. Neurosci Lett 63:315–319

    Google Scholar 

  • Gould E, Woolf NJ, Butcher LL (1989) Cholinergic projections to the substantia nigra from the pedunculopontine and laterodorsal tegmental nuclei. Neuroscience 28:611–623

    Google Scholar 

  • Grofova I, Keane S (1991) Descending brainstem projections of the pedunculopontine tegmental nucleus in the rat. Anat Embryol 183:275–290

    Google Scholar 

  • Grofova I, Rinvik E (1974) Cortical and pallidal projections to the nucleus ventralis lateralis thalami. Electron microscopical studies in the cat. Anat Embryol 146:113–132

    Google Scholar 

  • Hall WC, Fitzpatrick D, Klatt LL, Raczkowski D (1989) Cholinergic innervation of the superior colliculus in the cat. J Comp Neurol 287:495–514

    Google Scholar 

  • Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262:105–124

    Google Scholar 

  • Henderson Z (1987) Overlap in the distribution of cholinergic and catecholaminergic neurons in the ferret. J Comp Neurol 265:581–592

    Google Scholar 

  • Henderson Z, Greenfield SA (1987) Does the substantia nigra have a cholinergic innervation? Neurosci Lett 73:109–113

    Google Scholar 

  • Isaacson LG, Tanaka D (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

    Google Scholar 

  • 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

    Google Scholar 

  • Jacobsohn L (1909) Über die Kerne des menschlichen Hirnstamms. Verlag der Königl Akademie der Wissenschaften, Berlin

    Google Scholar 

  • Jones BE, Beaudet A (1987) Distribution of acetylcholine and catecholamine neurons in the cat brainstem: a choline acetyltransferase and tyrosine hydroxylase immunohistochemical study. J Comp Neurol 261:15–32

    CAS  PubMed  Google Scholar 

  • Jones BE, Yang T-Z (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242:56–92

    Google Scholar 

  • Kang Y, Kitai ST (1990) Electrophysiological properties of pedunculopontine neurons and their postsynaptic responses following stimulation of substantia nigra reticulata. Brain Res 535:79–95

    Google Scholar 

  • Kim R, Nakano K, Jayaraman A, Carpenter MB (1976) Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey. J Comp Neurol 169:263–289

    Google Scholar 

  • Kultas-Ilinsky K, Ilinsky I, Warton S, Smith KR (1983) Fine structure of nigral and pallidal afferents in the thalamus: an EM autoradiography study in the cat. J Comp Neurol 216:390–405

    Google Scholar 

  • Lee HJ, Rye DB, Hallanger AE, Levey AI, Wainer BH (1988) Cholinergic vs non-cholinergic efferents from the mesopontine tegmentum to the extrapyramidal motor system nuclei. J Comp Neurol 275:469–492

    Google Scholar 

  • Leonard CS, Llinas R (1988) Electrophysiology of thalamic-projecting brainstem neurons and their inhibition by ACH. Soc Neurosci Abstr 14:297

    Google Scholar 

  • Martinez-Murillo R, Villalba RM, Rodrigo J (1989a) Electron microscopic localization of cholinergic terminals in the rat substantia nigra: an immunocytochemical study. Neurosci Lett 96:121–126

    Google Scholar 

  • Martinez-Murillo R, Villalba RM, Montero-Caballero MI, Rodri-go J (1989b) Cholinergic somata and terminals in the rat substantia nigra: an immunocytochemical study with optical and electron microscopic techniques. J Comp Neurol 281:397–415

    Google Scholar 

  • Mesulam MM (1988) Central cholinergic pathways. In: Avoli et al. (eds) Neurotransmitters and cortical function: from molecules to mind. Plenum Press, New York, pp 237–260

    Google Scholar 

  • Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1983) Central cholinergic pathways in the rat: an overview based on alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185–1201

    Google Scholar 

  • 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 immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12:669–686

    Google Scholar 

  • Mesulam MM, Geula C, Bothwell MA, Hersh LB (1989) Human reticular formation: Cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons. J Comp Neurol 283:611–633

    Google Scholar 

  • Mitani A, Ito K, Hallanger AE, Wainer BH, Kataoka K, McCarley RW (1988) Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat. Brain Res 451:397–402

    Google Scholar 

  • Mizukawa K, McGeer PL, Tago H, Peng JH, McGeer EG, Kimura H (1986) The cholinergic system of the human hindbrain studied by choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Brain Res 379:39–55

    Google Scholar 

  • Moon-Edley SM, Graybiel M (1983) The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus, pars compacta. J Comp Neurol 217:187–215

    Google Scholar 

  • Moriizumi T, Nakamura Y, Tokuno H, Kudo M, Kitao Y (1989) Synaptic organization of the pedunculopontine tegmental nucleus of the cat. Brain Res 478:315–325

    Google Scholar 

  • Nakamura Y, Tokuno H, Moriizumi 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

    Google Scholar 

  • Nauta HJW, Mehler WR (1966) Projections of the lentiform nucleus in the monkey. Brain Res 1:3–42

    Google Scholar 

  • Olzewski J, Baxter D (1954) Cytoarchitecture of the human brain stem. 2nd edn. (1982) Karger, Basel München Paris London New York Sydney, p 195

    Google Scholar 

  • Pare D, Smith Y, Parent A, Steriade M (1988) Projections of brain-stem core cholinergic and non-cholinergic neurons of cat to intralaminar and reticular thalamic nuclei. Neuroscience 25:69–86

    Google Scholar 

  • Parent A, Mackey A, Smith Y, Boucher R (1983) The output organization of the substantia nigra in primate as revealed by a retrograde double labeling method. Brain Res Bull 10:529–537

    Google Scholar 

  • Pickel VM, Chan J (1991) Plasmalemmal appositions between cholinergic and non-cholinergic neurons in rat caudate-putamen nuclei. Neuroscience 41:459–472

    Google Scholar 

  • Rinvik E, Grofova I, Hammond C, Feger J, Deniau JM (1979) A study of the afferent connections to the subthalamic nucleus in the monkey and the cat using the HRP technique. In: Poirier LJ, Sourkes TL, Bedard PJ (eds) Advances in neurology. Raven Press, New York, pp 53–70

    Google Scholar 

  • Rye DB, Spacer CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus in the rat: Cytoarchitecture, cytochemistry and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483–528

    Google Scholar 

  • Rye DB, Lee HJ, Saper CB, Wainer BH (1988) Medullary and spinal efferents of the pedunculopontine tegmental nucleus and adjacent mesopontine tegmentum in the rat. J Comp Neurol 269:315–341

    Google Scholar 

  • Sakai K, Yoshimoto Y, Luppi PH, Fort P, El Mansari M, Salvert D, Jouvet M (1990) Lower brainstem afferents to the cat posterior hypothalamus: A double-labeling study. Brain Res Bull 24:437–455

    Google Scholar 

  • Satoh K, Fibiger HC (1985) Distribution of central cholinergic neuron in the baboon (Papio papio). I. General morphology. J Comp Neurol 236:197–214

    Google Scholar 

  • Satoh K, Armstrong DM, Fibiger HC (1983) A comparison of the distribution of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltransferase immunohistochemistry. Brain Res Bull 11:693–720

    Google Scholar 

  • Semba k,Fibiger HC (1989) Organization of central cholinergic systems. In: Nordberg et al. (eds) Prog Brain Res 79:37–63

  • Smith Y, Parent A (1984) Distribution of acetylcholinesterase-con-227 taining neurons in the basal forebrain and upper brainstem of the squirrel monkey (Saimiri sciureus). Brain Res Bull 12:95–104

    Google Scholar 

  • Smith Y, Bolam JP (1990) The output neurones and the dopaminergic neurones of the substantia nigra receive a GABA-containing input from the globus pallidus in the rat. J Comp Neurol 296:47–64

    Google Scholar 

  • Smith Y, Hazrati LN, Parent A (1990) Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J Comp Neurol 294:306–323

    Google Scholar 

  • Sofroniew MV, Priestly JV, Consolazione A, Eckenstien F, Cuello AC (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

    Google Scholar 

  • Spann BM, Grofova I (1989) Origin of ascending and spinal pathways from the nucleus tegmenti pedunculopontinus in the rat. J Comp Neurol 283:13–27

    Google Scholar 

  • Spann B, Grofova I (1990) Ultrastructure of cholinergic neurons of the nucleus tegmenti pedunculopontinus in the rat. Soc Neurosci Abstr 16:238

    Google Scholar 

  • Spann BM, Grofova I (1991) Nigropedunculopontine projection in the rat: an anterograde tracing study with Phaseolus vulgaris leucoagglutinin (PHA-L). J Comp Neurol 311:375–388

    Google Scholar 

  • Steriade M, Pare D, Parent A, Smith Y (1988) Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and Macaque monkey. Neuroscience 25:47–67

    Google Scholar 

  • Sugimoto T, Mizukawa K, Hattori T, Konishi A, Kaneko T, Mizuno N (1984) Cholinergic neurons in the nucleus tegmenti pedunculopontinus pars compacta and the caudoputamen of the rat: a light and electron microscopic immnunohistochemical study using a monoclonal antibody to choline acetyltransferase. Neurosci Lett 51:113–117

    Google Scholar 

  • Swanson LW, Mogenson GJ, Gerfen CR, Robinson P (1984) Evidence for a projection from the lateral preoptic area and substantia innominata to the “mesencephalic locomotor region” in the rat. Brain Res 295:161–178

    Google Scholar 

  • Woolf NJ, Butcher LL (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

    Google Scholar 

  • Woolf NJ, Butcher LL (1989) Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum. Brain Res Bull 23:519–540

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Michigan State University, 48824-1316, East Lansing, MI, USA

    Bryan M. Spann & Irena Grofova

Authors
  1. Bryan M. Spann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Irena Grofova
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spann, B.M., Grofova, I. Cholinergic and non-cholinergic neurons in the rat pedunculopontine tegmental nucleus. Anat Embryol 186, 215–227 (1992). https://doi.org/10.1007/BF00174143

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00174143

Key words

Search

Navigation