Chemical neuroanatomical and psychopharmacological evidence that κ receptor-mediated endogenous opioid peptide neurotransmission in the dorsal and ventral mesencephalon modulates panic-like behaviour

European Journal of Pharmacology

Volumn 698, Issue 1-3, 2013, Pages 235-245

  Da Silva, Juliana Almeida ^a   De Freitas, Renato Leonardo ^a   Eichenberger, Gustavo Cavalcanti Dutra ^a   Maria Padovan, Cláudia ^a   Cysne Coimbra, Norberto ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Innate fear; Intra tectal opioid pathway; Panic attack; Periaqueductal grey matter; Superior colliculus; Tecto nigral opioid pathway

Indexed keywords

BETA ENDORPHIN; KAPPA OPIATE RECEPTOR; NALTREXONE; NORBINALTORPHIMINE; OPIATE PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CHEMICAL NEUROANATOMY; CONTROLLED STUDY; DORSAL MESENCEPHALON; ELECTROSTIMULATION; GABAERGIC SYSTEM; MALE; MESENCEPHALON; NEUROANATOMY; NEUROTRANSMISSION; NONHUMAN; PANIC; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PSYCHOPHARMACOLOGY; RAT; SUBSTANTIA NIGRA; SUPERIOR COLLICULUS; TECTUM; VENTRAL MESENCEPHALON;

ANIMALS; ELECTRIC STIMULATION; GAMMA-AMINOBUTYRIC ACID; INSTINCT; MALE; MESENCEPHALON; NALTREXONE; NEUROANATOMY; NEURONS; OPIOID PEPTIDES; PANIC; PSYCHOPHARMACOLOGY; RATS; RATS, WISTAR; RECEPTORS, OPIOID, KAPPA; SUBSTANTIA NIGRA; SYNAPTIC TRANSMISSION;

EID: 84871926375     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2012.07.038     Document Type: Article

References (61)

1. V.C.Z. Anseloni, N.C. Coimbra, S. Morato, and M.L. Brandão A comparative study of the effects of morphine in the dorsal periaqueductal gray matter and nucleus accumbens of rats submitted to the elevated plus-maze test Exp. Brain Res. 129 1999 260 268 (Pubitemid 29525249)
2. G. Ashabi, S. Oryan, R. Ahmadi, and F. Valizadegan The effects of hippocampal opioidergic and septal GABAergic system interactions on anxiety-like behavior in rats Life Sci. 89 2011 821 826
3. A. Beaudet, and L. Descarries The fine structure of central serotonin neurons J. Physiol. (Paris) 77 1981 193 203 (Pubitemid 11032669)
4. A.F. Biagioni, J.A. Silva, and N.C. Coimbra Panic-like defensive behavior but not fear-induced antinociception is differently organized by dorsomedial and posterior hypothalamic nuclei of Rattus norvegicus (Rodentia, Muridae) Braz. J. Med. Biol. Res. 45 2012 328 336
5. P.J. Birch, A.G. Hayes, M.J. Sheehan, and M.B. Tyers Nor-binaltorphimine: antagonist profile at kappa opioid receptors Eur. J. Pharmacol. 144 1987 405 408 (Pubitemid 18019816)
6. D.C. Blanchard, and R.J. Blanchard Innate and conditioned reactions to threat in rats with amygdaloid lesions J. Comp. Physiol. Psychol. 8 1972 1281 1293
7. D.C. Blanchard, R.J. Blanchard, E.M.C. Lee, and S. Nakamura Defensive behaviours in rats following septal and septal-amygdala lesions J. Comp. Physiol. Phsychol. 93 1979 378 390 (Pubitemid 9149934)
8. A receptors in the dorsal periaqueductal gray Brain Res. 1051 2005 100 111 (Pubitemid 40982631)
9. K.G. Borelli, M.J. Nobre, M.L. Brandão, and N.C. Coimbra Effects of acute and chronic fluoxetine and diazepam on freezing behavior induced by electrical stimulation of dorsolateral and lateral columns of the periaqueductal gray matter Pharmacol. Biochem. Behav. 77 2004 557 566 (Pubitemid 38296816)
10. M.L. Brandão, N.C. Coimbra, and P.C. Leão Borges Effects of morphine and midazolam on reactivity to peripheral noxious and central aversive stimuli Neurosci. Biobehav. Rev. 14 1990 495 499
11. M.L. Brandão, N.C. Coimbra, and M.Y. Osaki Changes in the evoked-potentials by fear-evoking stimulations Physiol. Behav. 72 2001 365 372
12. M.L. Brandão, L.L. Melo, and S.H. Cardoso Mechanisms of defense in the inferior colliculus Behav. Brain Res. 58 1993 49 55 (Pubitemid 24024044)
13. M.L. Brandão, C. Tomaz, P.C. Leão Borges, N.C. Coimbra, and A. Bagri Defence reaction induced by microinjections of bicuculline into the inferior colliculus Physiol. Behav. 44 1988 361 365 (Pubitemid 19006985)
14. A-receptor-mediated systems modulate panic-like-induced behaviors elicited by electric and chemical stimulation of the inferior colliculus Brain Res. 1104 2006 92 102 (Pubitemid 44164433)
15. S.H. Cardoso, N.C. Coimbra, and M.L. Brandão Defensive reactions evoked by activation of NMDA receptors in distinct sites of the inferior colliculus Behav. Brain Res. 63 1994 17 24 (Pubitemid 24238613)
16. P. Carrive The periaqueductal gray and defensive behavior: functional representation and neuronal organization Behav. Brain Res. 58 1993 27 47 (Pubitemid 24024043)
17. E.F. Carvalho-Netto, C. Markham, D.C. Blanchard, R.L. Nunes-de-Souza, and R.J. Blanchard Physical environment modulates the behavioral responses induced by chemical stimulation of dorsal periaqueductal gray in mice Pharmacol. Biochem. Behav. 85 2006 140 147 (Pubitemid 44772916)
18. Castellan-Baldan, L., da Costa Kawasaki, M., Ribeiro, S.J., Calvo, F., Corrêa, V.M.A., Coimbra, N.C., 2006. Topographic and functional neuroanatomical study of GABAergic disinhibitory striatum-nigral inputs and inhibitory nigrocollicular pathways: neural hodology recruiting the substantia nigra, pars reticulata, for the modulation of the neural activity in the inferior colliculus involved with panic-like emotions. J. Chem. Neuroanat. 32, 1-27. (Errata in: J. Chem. Neuranat. 33, 65-66, 2007.) (Pubitemid 44234003)
19. N.C. Coimbra, and M.L. Brandão GABAergic nigro-collicular pathways modulate the defensive behaviour elicited by midbrain tectum stimulation Behav. Brain Res. 59 1993 131 139 (Pubitemid 24064878)
20. N.C. Coimbra, G.C.D. Eichenberger, R.T. Gorchinski, and S. Maisonnette Effects of opioid receptor blockade on defensive reactions elicited by electrical stimulation within the deep layers of the superior colliculus and DPAG Brain Res. 736 1996 348 352 (Pubitemid 26356494)
21. N.C. Coimbra, P.C. Leão-Borges, and M.L. Brandão GABAergic fibers from substantia nigra, pars reticulata, modulate escape behaviour induced by midbrain central gray stimulation Braz. J. Med. Biol. Res. 22 1989 111 114
22. N.C. Coimbra, R. De Oliveira, R.L. Freitas, S.J. Ribeiro, K.G. Borelli, R.C. Pacagnella, J.E. Moreira, L.A. da Silva, L.L. Melo, L.O. Lunardi, and M.L. Brandão Neuroanatomical approaches of the tectum-reticular pathways and immunohistochemical evidence for serotonin-positive perikarya on neuronal substrates of the superior colliculus and periaqueductal gray matter involved in the elaboration of the defensive behavior and fear-induced analgesia Exp. Neurol. 197 2006 93 112 (Pubitemid 41817224)
23. N.C. Coimbra, M.Y. Osaki, G.C.D. Eichenberger, J.G. Ciscato Jr., C.E.B. Jucá, and C.R. Biojone Effects of opioid receptor blockade on defensive behavior elicited by electrical stimulation of the aversive substrates of the inferior colliculus in Rattus norvegicus (Rodentia, Muridae) Psychopharmacology 152 2000 422 430
24. De Oliveira, R. Neuropharmacological Envidence for Interaction between Opioid and GABAergic Pathways in the Lateral Division of the Substantia Nigra on the Elaboration of Defensive Behaviour Organized by Inferior Colliculus, 2011. Scientiae Doctor Thesis (in Portuguese). Ribeirão Preto Medical School of the University of São Paulo, Ribeirão Preto (SP), vol 1, 104p.
25. R. De Oliveira, R.C. De Oliveira, and N.C. Coimbra Morphine microinjections in the substantia nigra, pars lateralis, increase fear evoked by inferior colliculus Eur. Neuropsychopharmacol. 20 2010 S268
26. G.C.D. Eichenberger, S.J. Ribeiro, M.Y. Osaki, R.Y. Maruoka, G.C.C. Resende, L. Castellan-Baldan, S.A.L. Corrêa, L.A. Da Silva, and N.C. Coimbra Neuroanatomical and psychopharmacological evidence for interaction between opioid and GABAergic neuronal pathways in the modulation of fear and defense elicited by electrical and chemical stimulation of deep layers of the superior colliculus and dorsal periqueductal gray matter Neuropharmacology 42 2002 48 59 (Pubitemid 34062821)
27. M.S. Fanselow Conditional and unconditional components of post-shock freezing J. Biol. Sci. 15 1980 177 182 (Pubitemid 11190893)
28. M.S. Fanselow The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety A. Depaulis, R. Bandler, The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Immunohistochemical Organization 1991 Plenum Publishing Corporation New York, NY 151 173
29. A. Fernandez de Molina, and R.W. Hunsperger Central representation of affective reaction in forebrain and brain stem: electrical stimulation of amygdala, stria terminalis and adjacent structures J. Physiol. 145 1959 251 265
30. S.A.G. Fuchs, and A. Siegel Neural pathways mediating hypothalamically elicited flight behaviour in the cat Brain Res. 306 1984 263 281 (Pubitemid 14090465)
31. S.A.G. Fuchs, H.M. Edinger, and A. Siegel The role of the anterior hypothalamus in affective defense behaviour elicited from the ventromedial hypothalamus of the cat Brain Res. 330 1985 93 107 (Pubitemid 15143644)
32. F.G. Graeff Minor tranquilizers and brain defense system Braz. J. Med. Biol. Res. 14 1981 239 265 (Pubitemid 12106975)
33. F.G. Graeff Brain defense systems and anxiety M. Roth, G.D. Burrows, R. Noyes, Handbook of Anxiety vol. 3 1990 Elsevier Science Publishers Amsterdam 307 354
34. F.G. Graeff Serotonin, periaqueductal gray matter and panic disorder Rev. Bras. Psiquiatr. 25 2003 42 45 (Pubitemid 38094853)
35. F.G. Graeff, and C.M. Del-Ben Neurobiology of panic disorder: from animal models to brain neuroimaging Neurosci. Biobehav. Rev. 32 2008 1326 1335
36. I. Grofová, O.P. Ottersen, and E. Rinvik Mesencephalic and diencephalic afferents to the superior colliculus and periaqueductal gray substance demonstrated by retrograde axonal transport of horseradish peroxidase in the rat Brain Res. 146 1978 205 220 (Pubitemid 8330925)
37. M. Halpern Effects of midbrain central gray matter lesions on escape avoidance behavior in rats Physiol. Behav. 3 1968 171 180
38. W. Hess, and M. Bruger Das subkortikale zentrum der affektiven abwereaktion Helv. Physiol. Pharmacol. Acta 1 1943 33 52
39. A. Jayaraman, R.R. Batton III, and M.B. Carpenter Nigrotectal projection in the monkey: an autoradiographic study Brain Res. 135 1977 147 152 (Pubitemid 8194357)
40. P.C. Leão Borges, N.C. Coimbra, and M.L. Brandão Independence of aversive and pain mechanisms in the dorsal periaqueductal gray matter of the rat Braz. J. Med. Biol. Res. 21 1988 1027 1031
41. M. Lyon The role of central midbrain structures in conditioned responding to aversive noise in the rat J. Comp. Neurol. 122 1964 407 429
42. A. Mansour, H. Khachaturian, M.E. Lewis, H. Akil, and S.J. Watson Anatomy of CNS opioid receptors Trends Neurosci. 11 1988 308 314
43. L. Menescal-de-Oliveira, and A. Hoffmann The parabrachial region as a possibile region modulating simultaneously pain and tonic immobility Behav. Brain. Res. 56 1993 127 132 (Pubitemid 23305194)
44. C.B. Metz, S.P. Schneider, and E.W. Fyffe Selective suppression of endogenous peroxidase activity: application for enhancing appearance of HRP-labeled neurons in vitro J. Neurosci. Methods 26 1989 181 188 (Pubitemid 19015513)
45. D. Mobbs, P. Petrovic, J.L. Marchant, D. Hassabis, N. Weiskopf, B. Seymour, R.J. Dolan, and C.D. Frith When fear is near: threat imminence elicits prefrontal-periaqueductal gray shifts in humans Science 317 2007 1079 1083 (Pubitemid 47330191)
46. S. Mori, T. Matsuura, T. Takino, and Y. Sano Light and electron microscopic immunohistochemical studies of serotonin nerve fibers in the substantia nigra of the rat, cat, and monkey Anat. Embryol. 176 1987 13 18
47. 1- and κ-opioid receptor blockade on escape behavior induced by electrical stimulation of the inferior colliculus Brain Res. 992 2003 179 192 (Pubitemid 37415101)
48. J. Panksepp The psychoneurology of fear: evolutionary perspectives and the role of animal models in understanding human anxiety G.D. Burrows, M. Roth, R. Noyers Jr. Handbook of Anxiety 1990 Elsevier Science Publishers Amsterdam 3 58
49. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates. 1997 Academic Press Sydney p. 113
50. L. Pellegrino Amygdaloid lesions and behavioral inhibition in the rat J. Comp. Physiol. Psychol. 56 1968 483 491
51. O.S. Portoghese, A.W. Lipkowski, and A.E. Takemori Binaltorphimine and nor-binaltorphimine, potent and selective kappa-opioid receptor antagonists Life Sci. 40 1987 1287 1292 (Pubitemid 17035103)
52. 1-opioid receptors in the modulation of panic-like reactions elicited by electrical stimulation of the dorsal midbrain J. Chem. Neuroanat. 30 2005 184 200 (Pubitemid 41579110)
53. Y. Shinonaga, M. Takada, and N. Mizumo Direct projections from the central amygdaloid nucleus to the globus pallidus and substantia nigra in the cat Neurosci. 51 1992 691 703
54. A. Siegel, and C.B. Pott Neural substrates of aggression and flight in the cat Prog. Neurobiol. 31 1988 261 283
55. P. Schmitt, P. Carrive, G. Di Scala, F. Jenck, and M.L. Brandão A neuropharmacological study of the periventricular neural substrate involved in flight Behav. Brain Res. 22 1986 181 190 (Pubitemid 17182277)
56. A.E. Takemori, B.Y. Ho, J.S. Naeseth, and P.S. Potoghese Nor-binaltorphimine, a highly selective kappa-opioid antagonist in analgesic and receptor binding assays J. Pharmacol. Exp. Ther. 246 1988 255 258
57. I. Tracey, A. Ploghaus, J.S. Gati, S. Clare, S. Smith, R.S. Menon, and P.M. Matthews Imaging attentional modulation of pain in the periaqueductal gray in humans J. Neurosci 22 2002 2748 2752 (Pubitemid 37465824)
58. A. Uribe-Mariño, A. Francisco, M.A. Castiblanco-Urbina, A. Twardowschy, C.J. Salgado-Rohner, J.A.S. Crippa, J.E.C. Hallak, A.W. Zuardi, and N.C. Coimbra Anti-aversive effects of cannabidiol on innate fear-induced behaviors evoked by an ethological model of panic attacks based on a prey vs. the wild snake Epicrates cenchria crassus confrontation paradigm Neuropsychopharmacology 27 2012 412 421
59. C.L. Veenman, A. Reiner, and M.G. Honig Biotinylated dextran amine as an anterograde tracer for single-labeling and double-labeling studies J. Neurosci. Methods 41 1992 239 254
60. W.B. Wilent, M.Y. Oh, C.M. Buetefisch, J.E. Bailes, D. Cantella, C. Angle, and D.M. Whiting Induction of panic attack by stimulation of the ventromedial hypothalamus J. Neurosurg. 112 2010 1295 1298
61. S.P. Zhang, R. Bandler, and P. Carrive Flight and immobility evoked by excitatory amino acid microinjection within distinct parts of the subtentorial midbrain periaqueductal gray of the cat Brain Res. 520 1990 3 82