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Tachykinin immunoreactivity in terminals of trigeminal afferent fibers in adult and fetal monkey thalamus

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Summary

Immunocytochemistry of fetal and adult monkey thalamus reveals a dense concentration of tachykinin immunoreactive fibers and terminals in the dorsolateral part of the VPM nucleus in which the contralateral side of the head, face and mouth is represented. The immunoreactive fibers enter the VPM nucleus from the thalamic fasciculus and electron microscopy reveals that they form large terminals resembling those of lemniscal axons and terminating in VPM on dendrites of relay neurons and on presynaptic dendrites of interneurons. Double labeling strategies involving immunostaining for tachykinins after retrograde labeling of brainstem neurons projecting to the VPM failed to reveal the origin of the fibers. The brainstem trigeminal nuclei, however, are regarded as the most likely sources of the VPM-projecting, tachykinin positive fibers.

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Abbreviations

AB:

ambiguus nucleus

AN:

abducens nucleus

C:

cuneate nucleus

CD:

dorsal cochlear nucleus

CL:

central lateral nucleus

CM:

centre médian nucleus

D:

dendrite

DR:

dorsal raphe

DV:

dorsal vagal nucleus

EC:

external cuneate nucleus

FM:

medial longitudinal fasciculus

FN:

facial nucleus

G:

gracile nucleus

Gc:

gigantocellular reticular formation

HN:

hypoglossal nucleus

ICP:

inferior cerebellar peduncle

IO:

inferior olivary complex

LC:

locus coeruleus

LL:

lateral lemniscus

LM:

medial lemniscus

M5:

motor trigeminal nucleus

NS:

solitary nucleus

OS:

superior olivary complex

P:

dendritic protrusion

Pb:

parabrachial nucleus

Pc:

parvocellular reticular formation

PLa:

anterior pulvinar nucleus

Pp:

prepositus hypoglossi nucleus

Ps:

presynaptic region

Py:

pyramidal tract

P5:

principal sensory trigeminal nucleus

R:

reticular nucleus

RF:

reticular formation

RL:

lateral reticular nucleus

S5:

spinal trigeminal nucleus

T:

terminal

T5:

spinal trigeminal tract

VL:

lateral vestibular nucleus

VM:

medial vestibular nucleus

VMb:

basal ventral medial nucleus

VPI:

ventral posterior inferior nucleus

VPL:

ventral posterior lateral nucleus

VPM:

ventral posterior medial nucleus

VR:

ventral raphe

VS:

superior vestibular nucleus

VSp:

spinal vestibular nucleus

ZI:

zona incerta

5:

trigeminal nerve

6:

abducens nerve

7:

facial nerve

References

  1. Battaglia G, Spreafico R, Rustioni A (1988) Substance P-immunoreactivity fibers in the thalamus from ascending somatosensory pathways. In: Bentivoglio M, Spreafico R (eds) Cellular thalamic mechanisms. Elsevier, Amsterdam, pp 365–374

  2. Chalupa LM, Hendry SHC, Jones EG, Killackey HP, Molinari M (1986) Localized substance P immunoreactivity in the VPM thalamic nucleus of adult and fetal monkeys. Neurosci Abstr 12:328

  3. Consolazione A, Priestley JV, Cuello AC (1984) Serotonin-containing projections to the thalamus in the rat revealed by a horseradish peroxidase and peroxidase antiperoxidase double-staining technique. Brain Res 322:233–244

  4. Cropper EC, Eisenman JS, Azmitia EC (1984) An immunocytochemical study of the serotonergic innervation of the thalamus of the rat. J Comp Neurol 224:38–50

  5. Cuello AC, Kanazawa I (1978) The distribution of substance P immunoreactive fibers in the rat central nervous system. J Comp Neurol 178:129–156

  6. DeLima AD, Montero VM, Singer W (1985) The cholinergic innervation of the visual thalamus: an EM immunocytochemical study. Exp Brain Res 59:206–212

  7. 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

  8. Hendry SHC, Jones EG, DeFelipe J, Schmechel D, Brandon C, Emson PC (1985) Neuropeptide containing neurons of the cerebral cortex are also GABAergic. Proc Natl Acad Sci USA 81:6526–6530

  9. Hirai T, Jones EG (1989) Distribution of tachykinin- and enkephalin-immunoreactive fibers in the human thalamus. Brain Res Rev 14:35–52

  10. Hirai T, Schwark H, Yen C-T, Honda CN, Jones EG (1988) Morphology of physiologically characterized medial lemniscal axons terminating in cat ventral posterior thalamic nucleus. J Neurophysiol 60:1439–1459

  11. Hökfelt T, Johannson O, Goldstein M (1984) Chemical anatomy of the brain. Science 225:1326–1334

  12. Hunt CA, Seroogy KB, Gall CM, Jones EG (1987) Cholecystokinin innervation of rat thalamus, including fibers to ven- troposterolateral nucleus from dorsal column nuclei. Brain Res 426:257–269

  13. Inagaki S, Kubota Y, Shinoda K, Kawai Y, Tohyama M (1983) Neurotensin-containing pathway from the endopiriform nuclues and the adjacent prepiriform cortex to the dorsomedial thalamic nucleus in the rat. Brain Res 260:143–146

  14. Jones EG, Hendry SHC (1986) Co-localization of GABA and neuropeptides in neocortical neurons. Trends Neurosci 9:71–76

  15. Jones EG, Powell TPS (1969) Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat. Proc R Soc Lond [Biol] 121:153–171

  16. Jones EG, Wise SP, Coulter JD (1979) Differential thalamic relatioships of sensory motor and parietal cortical fields in monkeys. J Comp Neurol 183:833–882

  17. Jones EG, Friedman DP, Hendry SHC (1982) Thalamic basis of place and modality-specific columns in monkey somatosensory cortex: a correlative anatomical and physiological study. J Neurophysiol 48:545–568

  18. Jones EG, Schwark HD, Callahan PJ (1986a) Extent of the ipsilateral representation in the ventral posterior medial nucleus of the monkey thalamus. Exp Brain Res 63:310–320

  19. Jones EG, Hendry SHC, Brandon C (1986b) Cytochrome oxidase staining reveals functional organization of monkey somatosensory thalamus. Exp Brain Res 62:438–442

  20. Jones EG, DeFelipe J, Hendry SHC, Maggio JE (1988) A study of tachykinin-immunoreactive neurons in monkey cerebral cortex. J Neurosci 8:1206–1224

  21. Killackey HP, Chalupa LM (1986) Ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey. J Comp Neurol 244:331–348

  22. Kiyama H, Shiosaka S, Takami K, Tateishi K, Hashimura E, Hamaoka T, Tohyama M (1984) CCK pathway from supramammillary region to the nucleus anterior ventralis thalami of the young rat. Peptides 5:889–893

  23. Lembeck F, Zetler G (1962) Substance P: a polypeptide of possible physiological significance, especially within the nervous system. Int Rev Neurobiol 4:159–215

  24. Ljungdahl A, Hökfelt T, Nilsson G (1978) Distribution of substance P-like immunoreactivity in the central nervous system of the rat. I. Cell bodies and nerve terminals. Neuroscience 3:861–943

  25. Magnusson KR, Clements JR, Larson AA, Madl JE, Beitz AJ (1987) Localization of glutamate in trigeminothalamic projection neurons: a combined retrograde transport-immunohistochemical study. Somatosensory Res 4:177–190

  26. Mesulam M-M, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185–1202

  27. Molinari M, Hendry SHC, Jones EG (1987) Distributions of certain neuropeptides in the primate thalamus. Brain Res 426:270–289

  28. Otsuka M, Takahashi T (1977) Putative peptide neurotransmitters. Annu Rev Pharmacol Toxicol 17:425–439

  29. Parent A, Paré D, Smith Y, Steriade M (1988) Basal forebrain cholinergic and noncholinergic projections to the thalamus and brainstem in cats and monkeys. J Comp Neurol 277:281–301

  30. Pernow B (1953) Studies on substance P: purification, occurrence and biological actions. Acta Physiol Scand 29:1–90

  31. Peschanski M, Besson JM (1984) Diencephalic connections of the raphe nuclei of the rat brain-stem: an anatomical study with reference to the somatosensory system. J Comp Neurol 224:503–534

  32. Ralston HJ (1969) The synaptic organization of lemniscal projections to the ventrobasal thalamus of the cat. Brain Res 14:99–115

  33. Ralston HJ (1971) Evidence for presynaptic dendrites and a proposal for their mechanism of action. Nature 230:585–587

  34. Ralston HJ, Herman MM (1969) The fine structure of neurons and synapses in the ventrobasal thalamus of the cat. Brain Res 14:77–97

  35. Ralston HJ, Ohara PT, Ralston DD, Chazal G (1988) The neuronal and synaptic organization of the cat and primate somataosensory thalamus. In: Bentivoglio M, Spreafico R (eds) Cellular thalamic mechanisms. Elsevier, Amsterdam, pp 127–141

  36. Steriade M, Paré 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 25:47–68

  37. Swanson LW, Hartman BK (1975) The central adrenergic system: an immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-B-hydroxylase as a marker. J Comp Neurol 163:467–506

  38. Villar MJ, Vitale ML, Hökfelt T, Verhofstad AAJ (1988) Dorsal raphe serotoninergic branching neurons projecting both to the lateral geniculate body and superior colliculus: a combined retrograde tracing-immunohistochemical study in the rat. J Comp Neurol 277:126–140

  39. Wong-Riley M (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11–28

  40. Woolf NJ, Butcher LL (1981) Cholinergic neurons in the caudate-putamen complex proper are intrinsically organized: a combined Evans blue and acetylcholinesterase analysis. Brain Res Bull 7:487–508

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Correspondence to E. G. Jones.

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Liu, X.-., Jones, E.G., Huntley, G.W. et al. Tachykinin immunoreactivity in terminals of trigeminal afferent fibers in adult and fetal monkey thalamus. Exp Brain Res 78, 479–488 (1989). https://doi.org/10.1007/BF00230236

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Key words

  • Tachykinin
  • Immunocytochemistry
  • Thalamus
  • Trigeminal
  • Monkey