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Topographical Specificity of Forebrain Inputs to the Midbrain Periaqueductal Gray: Evidence for Discrete Longitudinally Organized Input Columns

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The Midbrain Periaqueductal Gray Matter

Part of the book series: NATO ASI Series ((NSSA,volume 213))

Abstract

Over two decades ago it was discovered that electrical stimulation of the periaqueductal gray (PAG) caused profound analgesia (Reynolds, 1969). It was subsequently found that “PAG-analgesia” is, at least in part, mediated by opiate and neurotensin systems acting via PAG projections to the rostral medulla (Basbaum and Fields, 1984; Behbehani, 1981; Behbehani and Fields, 1979; Behbehani and Pert, 1984; Behbehani et al., 1987; Lakos and Basbaum, 1988; Reichling et al., 1988; Shipley et al., 1987). As a result of the observation that a discrete CNS structure exerted such a potent regulation of pain, much subsequent research has focused on the role of PAG in antinociception. At the same time there has been growing evidence that PAG plays a key role in the “defense reaction” (Bandler and Carrive, 1988; Bandler and Depaulis, this volume; Bandler et al., 1985a, 1991; Depaulis and Vergnes, 1986; Depaulis et al., 1989; Zhang et al., 1990), vocalization (Jürgens, 1976; Jürgens and Richter, 1986; Larson, 1985; Larson and Kistler, 1984; 1986), and in certain sexual behaviors (Ogawa et al., this volume; Sakuma and Pfaff; 1979a,b).

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References

  • Bandler, R. and Carrive, P., Integrated defence reaction elicited by excitatory amino acid microinjection in the midbrain periaqueductal grey region of the unrestrained cat, Brain Res., 439 (1988) 95–106.

    Article  CAS  PubMed  Google Scholar 

  • Bandler, R., Carrive, P. and Zhang, S.P., Integration of somatic and autonomic reactions within the midbrain periaqueductal grey: Viscerotopic, somatotopic and functional organization, Prog. Brain. Res., 87 (1991) 269–305.

    Article  CAS  PubMed  Google Scholar 

  • Bandler, R., Depaulis, A. and Vergnes, M., Identification of midbrain neurons mediating defensive behavior in the rat by microinjections of excitatory amino acids, Behav. Brain Res., 15 (1985a) 107–119.

    Article  CAS  PubMed  Google Scholar 

  • Bandler, R., McCulloch, T. and Dreher, B., Afferents to a midbrain periaqueductal grey region involved in the “defense reaction” in the cat as revealed by horseradish peroxidase. I. The telencephalon, Brain Res., 330 (1985b) 109–119.

    Article  CAS  PubMed  Google Scholar 

  • Basbaum, A.I. and Fields, H.L., Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry, Annu. Rev. Neurosci., 7 (1984) 309–338.

    Article  CAS  PubMed  Google Scholar 

  • Behbehani, M.M., Effect of chronic morphine treatment on the interaction between the periaqueductal grey and the nucleus raphe magnus of the rat, Neuropharmacol., 20 (1981) 581–586.

    Article  CAS  Google Scholar 

  • Behbehani, M.M. and Fields, H.L., Evidence that an excitatory connection between the periaqueductal gray and nucleus raphe magnus mediates stimulation produced analgesia, Brain Res., 170 (1979) 85–93.

    Article  CAS  PubMed  Google Scholar 

  • Behbehani, M.M. and Pert, A., A mechanism for the analgesic effect of neurotensin as revealed by behavioral and electrophysiological techniques, Brain Res., 324 (1984) 35–42.

    Article  CAS  PubMed  Google Scholar 

  • Behbehani, M.M., Shipley, M.T. and McLean, J.H., Effect of neurotensin on neurons in the periaqueductal gray: An in vitro study, J. Neurosci., 7 (1987) 2035–2040.

    CAS  PubMed  Google Scholar 

  • Beitz, A.J., The midbrain periaqueductal gray in the rat. I. Nuclear volume, cell number, density, orientation, and regional subdivisions, J. Comp. Neurol., 237 (1985) 444–469.

    Google Scholar 

  • Beitz, A.J., The organization of afferent projection to the midbrain periaqueductal gray of the rat, Neurosci., 7 (1982) 133–159.

    Article  CAS  Google Scholar 

  • Beitz, A.J., Mullett, M.A. and Weiner, L.L., The periaqueductal gray projections to the rat spinal trigeminal, raphe magnus, gigantocellular pars alpha and paragigantocellular nuclei arise from separate neurons, Brain Res., 288 (1983) 307–314.

    Article  CAS  PubMed  Google Scholar 

  • Beitz, A.J. and Shepard, R.D., The midbrain periaqueductal gray in the rat. II. A golgi analysis, J. Comp. Neurol., 237 (1985) 460–475.

    Article  CAS  PubMed  Google Scholar 

  • Burns, S.M. and Wyss, M.J., The involvement of the anterior cingulate cortex in blood pressure control, Brain Res., 340 (1985) 71–77.

    Article  CAS  PubMed  Google Scholar 

  • Carlton, S.M., Leichnetz, G.R., Young, E.G. and Mayer, D.J., Supramedullary afferents of the nucleus raphe magnus in the rat: a study using the transcannula HRP gel and autoradiographic techniques, J. Comp. Neurol., 214 (1983) 43–58.

    Article  CAS  PubMed  Google Scholar 

  • Carrive, P. and Bandler, R., Viscerotopic organization of neurons subserving hypotensive reactions within the midbrain periaqueductal grey: A correlative functional and anatomical study, Brain Res., 541 (1991) 206–215.

    Article  CAS  PubMed  Google Scholar 

  • Carrive, P., Bandler, R. and Dampney, R.A, Anatomical evidence that hypertension associated with the defence reaction in the cat is mediated by a direct projection from a restricted portion of the midbrain periaqueductal grey to the subretrofacial nucleus of the medulla, Brain Res., 460 (1988) 339–345.

    Article  CAS  PubMed  Google Scholar 

  • Carrive, P., Bandler, R. and Dampney, R.A., Somatic and autonomic integration in the midbrain of the unanesthetized decerebrate cat: a distinctive pattern evoked by excitation of neurones in the subtentorial portion of the midbrain periaqueductal grey, Brain Res., 483 (1989a) 251–258.

    Article  CAS  PubMed  Google Scholar 

  • Carrive, P., Bandler, R. and Dampney, R.A, Viscerotopic control of regional vascular beds by discrete groups of neurons within the midbrain periaqueductal gray, Brain Res., 493 (1989b) 385–390.

    Article  CAS  PubMed  Google Scholar 

  • Carrive, P., Dampney, R.A.L. and Bandler, R., Excitation of neurones in a restricted portion of the midbrain periaqueductal grey elicits both behavioral and cardiovascular components of the defence reaction in the unanaesthetised decerebrate cat, Neurosci. Lett., 81 (1987) 273–278.

    Article  CAS  PubMed  Google Scholar 

  • Carstens, C., MacKinnon, J.D. and Guinan, M.J., Inhibition of spinal dorsal horn neuronal responses to noxious skin heating by medial preoptic and septal stimulation in the cat, J. Neurophysiol., 46 (1982) 981–991.

    Google Scholar 

  • Cechetto, D.F. and Chen, S.J, Subcortical sites mediating sympathetic responses from insular cortex in rats, Am. J. Physiol., 258 (1990) R245–R255.

    CAS  PubMed  Google Scholar 

  • Clemens, J.A., Smalstig, E.B. and Sawyer, C.H., Studies on the role of the preoptic area in the control of reproductive function in the rat, Endocrinol., 99 (1976) 728–735.

    Article  CAS  Google Scholar 

  • Depaulis, A., Bandler, R. and Vergnes, M., Characterization of pretentorial periaqueductal gray matter neurons mediating intraspecific defensive behaviors in the rat by microinjections of kainic acid, Brain Res., 486 (1989) 121–132.

    Article  CAS  PubMed  Google Scholar 

  • Depaulis, A. and Vergnes, M., Elicitation of intraspecific defensive behaviors in the rat by microinjection of picrotoxin, a gamma-aminobutyric acid antagonist, into the midbrain periaqueductal gray matter, Brain Res., 367 (1986) 87–95.

    Article  CAS  PubMed  Google Scholar 

  • Ennis, M. and Shipley, M.T., Cortical inputs to the midbrain periaqueductal gray in the rat. I. Distribution and architectonics, in preparation.

    Google Scholar 

  • Ennis, M. and Shipley M.T., Organization of cortical inputs to the midbrain periaqueductal gray in the rat. II. Topography of cortical innervation, in preparation.

    Google Scholar 

  • Ennis, M. Rizvi, T., Shipley, M. and Behbehani, M., Organization of some forebrain inputs to the midbrain periaqueductal gray, Soc. Neurosci. Abstr., 16 (1990) 635.

    Google Scholar 

  • Fardin, V., Oliveras, J.L. and Besson, J.M., Projections from the periaqueductal gray matter to the B3 cellular area (nucleus raphe magnus and nucleus reticularis paragigantocellularis) as revealed by the retrograde transport of horseradish peroxidase in the rat, J. Comp. Neurol., 223 (1984) 483–500.

    Article  CAS  PubMed  Google Scholar 

  • Frenk, H., McCarty, B.L. and Liebeskind, J.C., Different brain areas mediate the analgesic and epileptic properties of enkephalin, Science, 200 (1978) 335–337.

    Article  CAS  PubMed  Google Scholar 

  • Gerfen, C.R. and Sawchenko, P.E., 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 (1985) 219–238.

    Article  Google Scholar 

  • Gioia, M., Tredici, G. and Bianchi, R., A Golgi study of the periaqueductal gray matter in the cat. Neuronal types and their distribution, Exp. Brain Res., 58 (1985) 318–332.

    Article  CAS  PubMed  Google Scholar 

  • Gorski, R.A., Harlan, R.E., Jacobson, C.D., Shryne, J.E. and Southam, A.M., Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat, J. Comp. Neurol., 193 (1980) 529–539.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, B.L., Cytoarchitectural subdivisions of the periaqueductal gray matter in the cat, J. Comp. Neurol.,149 (1973) 1–28.

    Article  CAS  PubMed  Google Scholar 

  • Hardy, S.G.P., Analgesia elicited by prefrontal stimulation, Brain Res., 339 (1985) 281–284.

    Article  CAS  PubMed  Google Scholar 

  • Hardy, S.G.P., Projections to the midbrain from the medial versus the lateral prefrontal cortices of the rat, Neurosci. Lett., 63 (1986) 159–164.

    Article  CAS  PubMed  Google Scholar 

  • Hardy, S.G.P. and Holmes, D.E., Prefrontal stimulus-produced hypotension in rat, Exp. Brain Res., 73 (1988) 249–255.

    Article  CAS  PubMed  Google Scholar 

  • Hitchcock, J. and Davis, M., Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with a potentiated startle paradigm, Behav. Neurosci., 100 (1986) 11–22.

    Article  CAS  PubMed  Google Scholar 

  • Hopkins, D.A. and Holstege, G., Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat, Exp. Brain Res., 32 (1978) 529–547.

    Article  CAS  PubMed  Google Scholar 

  • Hopkins, D.A., McLean, J.H. and Takeuchi, Y., Amygdalotegmental projections: Light and electron microscopic studies utilizing anterograde degeneration and anterograde and retrograde transport of HRP, In: The amygdaloid complex, Ben Ari Y. (Ed.), INSERM Symposium No. 20., Elsevier- Biomedical press, North Holland, 1981, pp. 133–147.

    Google Scholar 

  • Jürgens, U., Reinforcing concomitants of electrically elicited vocalizations, Exp. Brain Res., 26 (1976) 203–214.

    Article  PubMed  Google Scholar 

  • Jürgens, U. and Richter, K., Glutamate-induced vocalization in the squirrel monkey, Brain Res., 373 (1986) 349–358.

    Article  PubMed  Google Scholar 

  • Kaada, B., Stimulation and regional ablation of the amygdaloid complex with reference to functional representations, In: The Neurobiology of the Amygdala, Eleftheriou B.E. (Ed.), Plenum press, New York, 1972, pp. 145–204.

    Google Scholar 

  • Kalivas, P.W., Gau, B.A., Nemeroff, C.B. and Prange, A.J.Jr., Antinociception after microinjection of neurotensin into the central nucleus of the amygdala, Brain Res., 243 (1982) 279–286.

    Article  CAS  PubMed  Google Scholar 

  • Kapp, B.S., Gallaghen, M., Underwood, M.D., McNall, C.L., and Whitehorn, D., Cardiovascular responses elicited by electrical stimulation of the amygdalar central nucleus in rabbit, Brain Res., 234 (1982) 251–262.

    Article  CAS  PubMed  Google Scholar 

  • Krettek, J.E. and Price, J.L., The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat, J. Comp. Neurol., 171 (1977) 157–192.

    Article  CAS  PubMed  Google Scholar 

  • Lakos, S. and Basbaum, A.I., An ultrastructural study of the projections from the midbrain periaqueductal gray to spinally projecting, serotonin-immunoreactive neurons of the medullary nucleus raphe magnus in the rat, Brain Res., 443 (1988) 383–388.

    Article  CAS  PubMed  Google Scholar 

  • Larson, C.R., The midbrain periaqueductal gray: A brainstem structure involved in vocalization, J. Speech. Hear. Res., 28 (1985) 241–249.

    CAS  PubMed  Google Scholar 

  • Larson, C.R. and Kistler, M.K., Periaqueductal gray neuronal activity associated with laryngeal EMG and vocalization in the awake monkey Neurosci. Lett., 46 (1984) 261–266.

    CAS  Google Scholar 

  • Larson, C.R. and Kistler, M.K., The relationship of periaqueductal gray neurons to vocalization and laryngeal EMG in the behaving monkey, Exp. Brain Res., 63 (1986) 596–606.

    Article  CAS  PubMed  Google Scholar 

  • Mantyh, P.W., Forebrain projections to the periaqueductal gray in the monkey, with observations in the cat and rat, J. Comp. Neurol., 206 (1982a) 146–158.

    Article  CAS  PubMed  Google Scholar 

  • Mantyh, P.W., The midbrain periaqueductal gray in the rat, cat, and monkey: a nissl, weil, and golgi analysis, J. Comp. Neurol., 204 (1982b) 349–363.

    Article  CAS  PubMed  Google Scholar 

  • Marchand, J.E. and Hagino, N., Afferents to the periaqueductal gray in the rat. A horseradish peroxidase study, Neurosci., 9 (1983) 95–106.

    Article  CAS  Google Scholar 

  • Marlsbury, C.W., Facilitation of male copulatory behavior by electrical stimulation of the medial preoptic area, Physiol. Behav, 7 (1971) 797–805.

    Article  Google Scholar 

  • McGinty, D. and Szymusiak, R., Keeping cool: a hypothesis about the mechanisms and functions of slow-wave sleep, Trends Neurosci., 13 (1990) 480–486.

    Article  CAS  PubMed  Google Scholar 

  • Meiler, S.T. and Dennis, B.J., Afferent projection to the periaqueductal gray in the rabbit, Neurosci., 19 (1986) 927–964.

    Article  Google Scholar 

  • Nance, D.M., Christensen, L.W., Shryne, J.E. and Gorski, R.A., Modifications in gonadotropin control and reproductive behavior in the female rat by hypothalamic and preoptic lesions, Brain Res. Bull., 2 (1969) 307–312.

    Google Scholar 

  • Neafsey, E.J., Hurley-Guis, K.M. and Arvanitis, D., The topographical organization of neurons in the rat medial frontal, insular and olfactory cortex projecting to the solitary nucleus, olfactory bulb, periaqueductal gray and superior colliculus, Brain Res., 377 (1986) 261–270.

    Article  CAS  PubMed  Google Scholar 

  • Post, S., and Mai, K., Contribution to the amygdaloid projection fields in the rat: A quantitative autoradiographic study, J. Hirnforsch., 21 (1980) 199–225.

    CAS  PubMed  Google Scholar 

  • Price, J.L., Russchen, F.T. and Amaral, D.G., The limbic region. II. The amygdaloid complex, In: Handbook of Chemical Neuroanatomy. Vol.5: Integrated Systems in the CNS, Part I. Hypothalamus, Hippocampus, Amygdala, and Retina, Björklund A., Hökfelt T. and Swanson L.W. (Eds.), Elsevier, Amsterdam, 1987, pp. 279–388.

    Google Scholar 

  • Reichling, D.B., Kwiat, G.C. and Basbaum, A.I., Anatomy, physiology and pharmacology of the periaqueductal gray contribution to antinociceptive controls, Prog. Brain Res., 77 (1988) 31–46.

    Article  CAS  PubMed  Google Scholar 

  • Reynolds, D., Surgery in the cat during electrical analgesia induced by focal brain stimulation, Science, 164 (1969) 444–445.

    Article  CAS  PubMed  Google Scholar 

  • Rizvi, T., Ennis, M., Behbehani, M. and Shipley, M., Reciprocal projections between the medial preoptic area and midbrain periaqueductal gray, Soc. Neurosci. Abstr., 16 (1990) 562.

    Google Scholar 

  • Rizvi, T. A., Ennis, M., Shipley, M.T. and Behbehani, M., Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity, J. Comp. Neurol., 303 (1991) 121–131.

    Article  CAS  PubMed  Google Scholar 

  • Ruggiero, D.A., Mraovitch, S., Granata, A.R., Anwar, M. and Reis, D.J., A role of insular cortex in cardiovascular function, J. Comp. Neurol., 257 (1987) 189–207.

    Article  CAS  PubMed  Google Scholar 

  • Sakuma, Y. and Pfaff, D.W., Facilitation of female reproductive behavior from mesencephalic central grey in the rat, Am. J. Physiol., 236 (1979a) R278–R284.

    Google Scholar 

  • Sakuma, Y. and Pfaff, D.W., Mesencephalic mechanisms for integration of female reproductive behavior in the rat, Am. J. Physiol., 237 (1979b) R285–R290.

    CAS  PubMed  Google Scholar 

  • Sesack, S.R., Deutch, A.Y., Roth, R.H. and Bunney, B.S., Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin, J. Comp. Neurol., 290 (1989) 213–242.

    Article  CAS  PubMed  Google Scholar 

  • Shipley, M.T., Ennis, M. and Behbehani, M., Acetylcholinesterase and Nissl staining in the same histological section, Brain Res., 504 (1989) 347–353.

    Article  CAS  PubMed  Google Scholar 

  • Shipley, M.T., McLean, J.H. and Behbehani, M.M., Heterogeneous distribution of neurotensin-like immunoreactive fibers in the midbrain periaqueductal grey of the rat, J. Neurosci., 7 (1987) 2025–2034.

    CAS  PubMed  Google Scholar 

  • Simerly, R.B. and Swanson, L.W., The organization of neural inputs to the medial preoptic nucleus of the rat, J. Comp. Neurol., 246 (1986) 312–341.

    Article  CAS  PubMed  Google Scholar 

  • Simerly, R.B., Swanson, L.W. and Gorski, R.A., Demonstration of a sexual dimorphism in the distribution of serotonin-immunoreactive fibers in the medial preoptic nucleus of the rat, J. Comp. Neurol., 225 (1984) 151–166.

    Article  CAS  PubMed  Google Scholar 

  • Terreberry, R.R. and Neafsey, E J., The rat medial frontal cortex projects directly to autonomic regions of the brainstem, Brain Res. Bull., 19 (1987) 639–649.

    Article  CAS  PubMed  Google Scholar 

  • Van Bockstaele, E., Aston-Jones, G., Pieribone, V.A., Ennis, M. and Shipley, M.T., Periaqueductal gray and perioculomotor neurons innervate specific subdivisions of the rostral ventrolateral medulla in the rat: Anterograde studies using phaseolus vulgaris — leucoagglutinin, J. Comp. Neurol., 1991, in press.

    Google Scholar 

  • Wang, S.Q. and Ranson, S.W., The role of the hypothalamus and preoptic region in the regulation of heart rate, Am. J. Physiol., 132 (1941) 5–8.

    Google Scholar 

  • Wyss, J.M. and Sripanidkulchai, K., The topography of the mesencephalic and pontine projections from the cingulate cortex of the rat, Brain Res., 293 (1984) 1–15.

    Article  CAS  PubMed  Google Scholar 

  • Yasui, Y., Breder, C.D., Saper, C.B. and Cechetto, D.F., Autonomic responses and efferent pathways from the insular cortex in the rat, J. Comp. Neurol., 303 (1991) 355–374.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, S.P., Bandler, R. and Carrive, P., Right and immobility evoked by excitatory amino acid microinjection within distinct parts of the subtentorial midbrain periaqueductal gray of the cat, Brain Res., 520 (1990) 73–82.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy and Cell Biology, University of Cincinnati College of Medicine, Cincinnati, USA

    Michael T. Shipley, Matthew Ennis & Tilat A. Rizvi

  2. Department of Physiology and Biophysics, University of Cincinnati College of Medicine, Cincinnati, USA

    Michael M. Behbehani

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  1. Michael T. Shipley
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Editors and Affiliations

  1. L.N.B.C, Centre de Neurochimie du CNRS, 5 rue Blaise Pascal, 67084, Strasbourg Cedex, France

    Antoine Depaulis

  2. Dept. of Anatomy, University of Sydney, 2006, Sydney, NSW, Australia

    Richard Bandler

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Shipley, M.T., Ennis, M., Rizvi, T.A., Behbehani, M.M. (1991). Topographical Specificity of Forebrain Inputs to the Midbrain Periaqueductal Gray: Evidence for Discrete Longitudinally Organized Input Columns. In: Depaulis, A., Bandler, R. (eds) The Midbrain Periaqueductal Gray Matter. NATO ASI Series, vol 213. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3302-3_22

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