Skip to main content
SpringerLink
Log in

Projection of neurotensin-like immunoreactive neurons from the lateral parabrachial area to the central amygdaloid nucleus of the rat with reference to the coexistence with calcitonin gene-related peptide

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

The origin of neurotensin-like immunoreactive (NTI) fibers in the central amygdaloid nucleus (AC) in the rat was examined using indirect immunofluorescence and retrograde tracing combined with immunocytochemistry. Destruction of the external subdivision of the lateral parabrachial nucleus, which contains a group of NTI neurons, resulted in a marked reduction of these fibers in the ipsilateral AC, which suggests that most of these fibers are of extrinsic origin. This was also supported by the finding that injection of fast blue dye into the AC labeled many neurons in the external subdivision of the lateral parabrachial nucleus ipsilaterally, and that simultaneous treatment with antiserum against NT stained some of these neurons. Subsequent immunohistochemical staining of alternate sections revealed that many of these NTI neurons were also labeled by calcitonin gene-related peptide antiserum.

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

References

  • Block CH, Schwartzbaum JS (1983) Ascending efferent projections of the gustatory parabrachial nuclei in the rabbit. Brain Res 259: 1–9

    Google Scholar 

  • Carraway R, Leeman SE (1973) The isolation of a new hypotensive peptide neurotensin, from bovine hypothalami. J Biol Chem 248: 6854–6861

    Google Scholar 

  • Carraway R, Leeman SE (1975a) The amino acid sequence of hypothalamic peptide, neurotensin. J Biol Chem 250: 1907–1911

    Google Scholar 

  • Carraway R, Leeman SE (1975b) The synthesis of neurotensin. J Biol Chem 250: 1912–1918

    Google Scholar 

  • Carraway R, Leeman SE (1976) Characterization of radioimmunoassayable neurotensin in the rat. J Biol Chem 251: 7045–7052

    Google Scholar 

  • Cechetto DF, Calaresu FR (1983) Response of single units in the amygdala to stimulation of buffer nerves in cat. Am J Physiol 244: R646-R651

    Google Scholar 

  • Coons AH (1958) Fluorescent antibody method. In: Danielli JF (ed) General cytochemical methods. Academic Press, New York, pp 399–422

    Google Scholar 

  • Dahlström A (1968) Effect of colchicine on transport of amine storage granules in sympathetic nerve of rat. Eur J Pharmacol 5: 111–112

    Google Scholar 

  • Fulwiler CE, Saper CB (1984) Subnuclear organization of efferent connections of the parabrachial nucleus in the rat. Brain Res Rev 7: 229–259

    Google Scholar 

  • Galeno TM, van Hoesen GW, Maixner W, Johnson AK, Brody MJ (1982) Contribution of the amygdala to the development of spontaneous hypertension. Brain Res 246: 1–6

    Google Scholar 

  • Grijalva CV, Tache Y, Gunion MW, Walsh JH, Geiselman PJ (1986) Amygdaloid lesions attenuate neurogenic gastric mucosal erosions but do not alter gastric secretory changes induced by intracisternal bombesin. Brain Res Bull 16: 55–61

    Google Scholar 

  • Hamilton RB, Ellenberger H, Liskowsky D, Schneiderman N (1981) Parabrachial area as mediator of bradycardia in rabbits. J Auton Nerv Syst 4: 261–281

    Google Scholar 

  • Henke PG (1980a) The amygdala and restraint ulcers in rats. J Comp Physiol Psychol 94: 313–323

    Google Scholar 

  • Henke PG (1980b) The centromedial amygdala and gastric pathology in rats. Physiol Behav 25: 107–112

    Google Scholar 

  • Henke PG (1980c) Facilitation and inhibition of gastric pathology after lesions in the amygdala of rats. Physiol Behav 25: 575–579

    Google Scholar 

  • Hernandez DE, Nemeroff CB, Orlando RC, Prange Jr AJ (1983) The effect of cemtrally administrated neuropeptides on the development of stress-induced gastric ulcers in the rat. J Neurosci Res 9: 145–157

    Google Scholar 

  • Hernandez DE, Stanley DA, Allen JA, Prange Jr AJ (1985) Role of brain neurotransmitters on neurotensin induced cytoprotection. Pharmacol Biochem Behav 22: 509–513

    Google Scholar 

  • Hernandez DE, Stanley DA, Melvin JA, Prange Jr AJ (1986) Involvement of brain dopamine systems on neurotensininduced protection against stress gastric lesions. Brain Res 381: 159–163

    Google Scholar 

  • Inagaki S, Kawai Y, Matsuzaki T, Shiosaka S, Tohyama M (1983a) Precise terminal fields of the descending somatostatinergic projections from amygdaloid complex of the rat. J Hirnforsch 24: 345–356

    Google Scholar 

  • Inagaki S, Yamano M, Shiosaka S, Takagi H, Tohyama M (1983b) Distribution and origins of neurotensin-containing fibers in the nucleus ventromedialis hypothalami of the rat: an experimental immunohistochemical study. Brain Res 273: 229–235

    Google Scholar 

  • Innes DL, Tansy MF (1980) Gastric mucosal ulceration associated with electrochemical stimulation of limbic brain. Brain Res Bull 5: 33–36

    Google Scholar 

  • Kaada BR (1972) Stimulation and regional ablation of the amygdaloid complex with reference to functional representation. In: Eleftheriou BE (ed) The neurobiology of the amygdala, Plenum Press, New York, pp 205–281

    Google Scholar 

  • Kalivas PW, Gau BA, Nemeroff CB, Prange Jr AJ (1982) Antinociception after microinjection of neurotensin into the central amygdaloid nucleus of the rat. Brain Res 243: 279–286

    Google Scholar 

  • Kawai Y, Inagaki S, Shiosaka S, Senba E, Hara Y, Sakanaka M, Takatsuki K, Tohyama M (1982) Long descending projections from amygdaloid somatostatin-containing cells to the lower brain stem. Brain Res 239: 603–607

    Google Scholar 

  • Kawai Y, Takami K, Shiosaka S, Emson PC, Hillyard CJ, Girgis S, MacIntyre I, Tohyama M (1985) Topographic localization of calcitonin gene-related peptide in the rat brain: an immunohistochemical analysis. Neuroscience 15: 747–763

    Google Scholar 

  • Kobayashi R, Nrown M, Vale W (1977) Regional distribution of neurotensin and somatostatin in the rat. Brain Res 126: 584–588

    Google Scholar 

  • Krettek JE, Price JL (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178: 225–254

    Google Scholar 

  • Kreutzberg G (1969) Neuronal dynamics and flow. IV. Blockage of intraaxonal enzyme transport by colchicine. Proc Natl Acad Sci USA 62: 722–728

    Google Scholar 

  • Milner TA, Pickel VM (1986) Neurotensin in the rat parabrachial region; ultrastructural localization and extrinsic sources of immunoreactivity. J Comp Neurol 247: 326–343

    Google Scholar 

  • Minagawa H, Shiosaka S, Inagaki S, Sakanaka M, Takatsuki K, Ishimoto I, Senba E, Kawai Y, Hara Y, Matsuzaki T, Tohyama M (1983) Ontogeny of neurotensin-containing neuron system of the rat: immunohistochemical analysis. II. Lower brain stem. Neuroscience 8: 467–486

    Google Scholar 

  • Moga MM, Gray TS (1985) Evidence for corticotropin-releasing factor, neurotensin, and somatostatin in the neural pathway from the central nucleus of the amygdala to the parabrachial nucleus. J Comp Neurol 241: 275–284

    Google Scholar 

  • Mraovitch S, Kumada M, Reis DJ (1982) Role of the nucleus parabrachialis in cardiovascular regulation in cat. Brain Res 232: 57–75

    Google Scholar 

  • Nemeroff CB, Hernandez DE, Orlando RC, Prange Jr AJ (1982) Cytoprotective effect of centrally administered neurotensin on stress indued gastric ulcers. Am J Physiol 242: G342-G346

    Google Scholar 

  • Ngulen KQ, Sills MA, Jacobowitz DM (1986) Cardiovascular effects produced by microinjection of calcitonin gene-related peptide into the rat central amygdaloid nucleus. Peptides 7: 337–339

    Google Scholar 

  • Norgren R (1974) Gustatory afferents to ventral forebrain. Brain Res 81: 285–295

    Google Scholar 

  • Norgren R (1976) Taste pathway to hypothalamus and amygdala. J Comp Neurol 166: 17–30

    Google Scholar 

  • Orlando RC, Hernandez DE, Prange Jr AJ, Nemeroff CB (1985) Role of autonoimic nervous system in the cytoprotective effect of neurotensin against gastric stress ulcers in rats. Psychoneuroendocrinol 10: 149–157

    Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • Prange Jr AJ, Charles B, Nemeroff B, Loosen PT (1978) Behavioral effects of hypothalamic peptides. In: Hughes J 0(ed) Centrally acting peptides. Macmillan Press, London, pp 99–118

    Google Scholar 

  • Price JL, Amaral DG (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1: 1242–1259

    Google Scholar 

  • Ray A, Hneke PG, Sullivan RM (1987) The central amygdala and immobilization stress-induced gastric pathology in rats: neurotensin and dopamine. Brain Res 49: 398–402

    Google Scholar 

  • Roberts GW, Woodhams PL, Polak JM, Ceow TJ (1982) Distribution of neuropeptides in the limbic system of the rat: the amygdaloid complex. Neuroscience 7: 99–131

    Google Scholar 

  • Sakanaka M, Shiosak S, Takatsuki K, Inagaki S, Takagi H, Senba E, Kawai Y, Matsuzaki T, Tohyama M (1981) Experimental immunohistochemical studies on the amygdalofugal peptidergic (substance P and somatostatin) fibers in the stria terminalis of the rat. Brain Res 221: 231–242

    Google Scholar 

  • Sakanaka M, Shibasaki T, Lederis K (1986) Distribution and efferent projections of corticotropin-releasing factor-like immunoreactivity in the rat amygdaloid complex. Brain Res 382: 213–238

    Google Scholar 

  • Saper CB, Loewy AD (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res 197: 291–317

    Google Scholar 

  • Sawchenko PE, Swanson LW (1981) A method for tracing biochemically defined pathways in the central nervous system using combined fluorescence retrograde transport and immunohistochemical techniques. Brain Res 210: 31–51

    Google Scholar 

  • Schreiner L, Kling A (1953) Behavioral changes following rhinencephalic injury in cat. J Neurophysiol 16: 643–659

    Google Scholar 

  • Shimada S, Shiosaka S, Emson PC, Hillyard CJ, Girgis S, Maclntyre I, Tohyama M (1985) Calcitonin gene-related peptide projection from parabrachial area to the forebrain and diencephalon in the rat: an immunocytochemical analysis. Neuroscience 16: 607–616

    Google Scholar 

  • Shiosaka S, Sakanaka M, Inagaki S, Senba E, Hara Y, Takatsuki K, Takagi H, Kawai Y, Tohyama M (1983) Putative neurotransmitters in the amygdaloid complex with special reference to peptidergic pathways. In: Emson PD (ed) Chemical neuroanatomy. Raven Press, New York, pp 359–389

    Google Scholar 

  • Skirboll L, Hökfelt T, Norell G, Phillipson O, Kuypers HGJM, Bentivoglio M, Catsman-Berrevoets CE, Visser TJ, Steinbusch H, Veerhofstad AD, Cuello AC, Goldstein M, Brownstein M (1984) A method for specific transmitter identification of retrogradely labeled neurons: immunofluorescence combined with fluorescence tracing. Brain Res 8: 99–127

    Google Scholar 

  • Snyder SH, Uhl GR, Kuhar MJ (1978) Comparative features of enkephalin and neurotensin in the mammalian central nervous system. In: Hughes J (ed) Centrally acting peptide. Macmillan, London, pp 85–97

    Google Scholar 

  • Stock G, Schlor KH, Heidt H, Buss J (1977) Psychomotor behavior and cardiovascular patterns during stimulation of the amygdala. Pflügers Arch 376: 177–184

    Google Scholar 

  • Takeuchi Y, McLean JH, Hopkins DA (1982) Reciprocal connections between the amygdala and parabrachial nuclei: ultrastructural demonstration by degeneration and axonal transport of horseradish peroxidase in the cat. Brain Res 239: 583–588

    Google Scholar 

  • Uhl GR, Snyder SH (1979) Neurotensin: a neuronal pathway projecting from amygdala through stria terminalis. Brain Res 161: 522–526

    Google Scholar 

  • Uhl GR, Goodman RR, Kuhar MJ, Snyder SM (1978) Enkephalin and neurotensin immunohistochemical localization and identification of amygdalofugal pathway. Adv Biochem Psychopharmacol 18: 71–87

    Google Scholar 

  • Veening JG, Swanson LW, Sawchenko PE (1984) The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study. Brain Res 303: 337–357

    Google Scholar 

  • Wray S, Hoffman GW (1983) Organization and interrelationship of neuropeptides in the central amygdaloid nucleus of the rat. Peptides 4: 525–541

    Google Scholar 

  • Zamboni L, De Martino C (1967) Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy. J Cell Biol 35: 148A

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy II, Osaka University Medical School, 4-3-57 Nakanoshima, Kitaku, 530, Osaka, Japan

    M. Yamano & M. Tohyama

  2. Department of Chemical Pathology, University of London, Royal Postgraduate Medical School, Hammersmith Hospital, Ducane Road, W12 0HS, London, UK

    C. J. Hillyard, S. Girgis & I. MacIntyre

  3. MRC Neurochemical Pharmacological Unit, Medical Council, Centre Medical School, Hills Road, CB 2 2QH, Cambridge, UK

    P. C. Emson

Authors
  1. M. Yamano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. J. Hillyard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Girgis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. C. Emson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. I. MacIntyre
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Tohyama
    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

Yamano, M., Hillyard, C.J., Girgis, S. et al. Projection of neurotensin-like immunoreactive neurons from the lateral parabrachial area to the central amygdaloid nucleus of the rat with reference to the coexistence with calcitonin gene-related peptide. Exp Brain Res 71, 603–610 (1988). https://doi.org/10.1007/BF00248753

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00248753

Key words

Search

Navigation