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Involvement of opioid and endocanabinoid receptors of the substantia nigra on the activity of Nigro-Tectal GABAergic pathways during defensive behaviour elicited by rodents confronted with venomous snakes

Grant number: 12/03798-0
Support type:Regular Research Grants
Duration: December 01, 2012 - May 31, 2015
Field of knowledge:Biological Sciences - Morphology - Anatomy
Principal researcher:Norberto Cysne Coimbra
Grantee:Norberto Cysne Coimbra
Home Institution: Faculdade de Medicina de Ribeirão Preto (FMRP). Universidade de São Paulo (USP). Ribeirão Preto , SP, Brazil

Abstract

The study of the neuropsychopharmacological bases of the fear- and panic-related behaviour has been the focus of several scientific researches. The mesencephalic tectum (MT) has been considered as responsible for the control of defensive responses evoked during threatening situations. The deep layers of the superior colliculus (dlSC) have been considered important structures for the elaboration of innate fear and defensive behaviour. The substantia nigra, pars reticulata (SNpr) is known to send inputs to the intermediate layers of the superior colliculus (ilSC), that can Works as a sensory channel to tectal neurons responsible for the elaboration of defensive responses in more ventral regions of this neural substrate. The dorsal mesencephalon, however, is connected to both compacta and reticulata divisions of the substantia nigra, through inputs rich in endogenous opioid peptides. This mesencephalic structure is also rich in CB1 and CB2 endocannabinoid receptors, with putative involvement in this neural system that is known for these interactive properties with the opioid system, and has been the focus of interest of scientific community. The purpose of the present work is to investigate the role of µ- and kappa-opioid receptors, of CB1- and CB2-endocannabinoid receptors of SNpr, rich in GABAergic neurons connected to the mesencephalic tectum in the modulation of defensive behavior related to instinctive fear and panic reactions. However, there is co-existence of both classic opioid receptors and nociceptin/orfanin ORL1 receptors in SNpr, and the role of this opioid-like receptores in the nigro-tectal pathways deserves investigation. Thus, it will be also studied the effect of microinjections of µ1- and kappa-opioid receptors selective antagonists, CB1- and CB2-endocannabinoid receptors selective antagonist, ORL1-receptor selective antagonist into SNpr on the elaboration of the defensive behavior elaborated by dorsal mesencephalon induced by GABAA receptor selective blockade in the dlSC of Wistar rats. (AU)

Scientific publications (32)
(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)
ALMADA, RAFAEL CARVALHO; DOS ANJOS-GARCIA, TAYLLON; DA SILVA, JULIANA ALMEIDA; PIGATTO, GLAUCE REGINA; WOTJAK, CARSTEN T.; COIMBRA, NORBERTO CYSNE. The modulation of striatonigral and nigrotectal pathways by CB1 signalling in the substantia nigra pars reticulata regulates panic elicited in mice by urutu-cruzeiro lancehead pit vipers. Behavioural Brain Research, v. 401, MAR 5 2021. Web of Science Citations: 0.
DA SILVA, JULIANA ALMEIDA; ALMADA, RAFAEL CARVALHO; DE PAIVA, YARA BEZERRA; COIMBRA, NORBERTO CYSNE. Endocannabinoid neuromodulation in the neostriatum decreases the GABAergic striato-nigral disinhibitory function and increases the nigro-collicular inhibitory pathway activity. JOURNAL OF NEURAL TRANSMISSION, v. 127, n. 8 JUN 2020. Web of Science Citations: 0.
DOS ANJOS-GARCIA, TAYLLON; COIMBRA, NORBERTO CYSNE. Anandamide in the anterior hypothalamus diminishes defensive responses elicited in mice threatened by Epicrates cenchria constrictor serpents. ACTA NEUROBIOLOGIAE EXPERIMENTALIS, v. 80, n. 2, p. 179-191, 2020. Web of Science Citations: 0.
CALVO, FABRICIO; ALMADA, RAFAEL CARVALHO; DA SILVA, JULIANA ALMEIDA; MEDEIROS, PRISCILA; SOARES, JR., RAIMUNDO DA SILVA; DE PAIVA, YARA BEZERRA; RONCON, CAMILA MARRONI; COIMBRA, NORBERTO CYSNE. The Blockade of mu(1)- and kappa-Opioid Receptors in the Inferior Colliculus Decreases the Expression of Panic Attack-Like Behaviours Induced by Chemical Stimulation of the Dorsal Midbrain. NEUROPSYCHOBIOLOGY, v. 78, n. 4, p. 218-228, NOV 2019. Web of Science Citations: 0.
SOARES, JR., RAIMUNDO DA SILVA; FALCONI-SOBRINHO, LUIZ LUCIANO; ALMADA, RAFAEL CARVALHO; COIMBRA, NORBERTO CYSNE. Dorsal raphe nucleus 5-Hydroxytryptamine 2A receptors are critical for the organisation of panic attack-like defensive behaviour and unconditioned fear-induced antinociception elicited by the chemical stimulation of superior colliculus neurons. European Neuropsychopharmacology, v. 29, n. 7, p. 858-870, JUL 2019. Web of Science Citations: 1.
DOS ANJOS-GARCIA, TAYLION; COIMBRA, NORBERTO CYSNE. Opposing roles of dorsomedial hypothalamic CB1 and TRPV1 receptors in anandamide signaling during the panic-like response elicited in mice by Brazilian rainbow Boidae snakes. Psychopharmacology, v. 236, n. 6, p. 1863-1874, JUN 2019. Web of Science Citations: 2.
CALVO, FABRICIO; ALMADA, RAFAEL CARVALHO; DOS ANJOS-GARCIA, TAYLLON; FALCONI-SOBRINHO, LUIZ LUCIANO; PASCHOALIN-MAURIN, TATIANA; BAZAGLIA-DE-SOUSA, GUILHERME; MEDEIROS, PRISCILA; DA SILVA, JULIANA ALMEIDA; LOBAO-SOARES, BRUNO; COIMBRA, NORBERTO CYSNE. Panicolytic-like effect of mu(1)-opioid receptor blockade in the inferior colliculus of prey threatened by Crotalus durissus terrificus pit vipers. JOURNAL OF PSYCHOPHARMACOLOGY, v. 33, n. 5, p. 577-588, MAY 2019. Web of Science Citations: 2.
MATIAS, JR., IVAIR; ELIAS, DAOUD HIBRAHIM; BERNARDINO GARCIA, CAMILA ARAUJO; SILVA, GUILHERME HENRIQUE; MEJIA, JORGE; CABRAL, FRANCISCO ROMERO; CAMARGO MIRANDA, ANA CLAUDIA; DA SILVA, SERGIO GOMES; LOPES, LUIZA DA SILVA; COIMBRA, NORBERTO CYSNE; MACHADO, HELIO RUBENS. A new model of experimental hemispherotomy in young adult Rattus norvegicus: a neural tract tracing and SPECT in vivo study. JOURNAL OF NEUROSURGERY, v. 130, n. 4, p. 1210-1223, APR 2019. Web of Science Citations: 1.
SOARES JR, RAIMUNDO DA SILVA; FALCONI-SOBRINHO, LUIZ LUCIANO; DOS ANJOS-GARCIA, TAYLLON; COIMBRA, NORBERTO CYSNE. 5-Hydroxytryptamine 2A receptors of the dorsal raphe nucleus modulate panic-like behaviours and mediate fear-induced antinociception elicited by neuronal activation in the central nucleus of the inferior colliculus. Behavioural Brain Research, v. 357, n. SI, p. 71-81, JAN 14 2019. Web of Science Citations: 4.
CALVO, FABRICIO; LOBAO-SOARES, BRUNO; DE FREITAS, RENATO LEONARDO; PASCHOALIN-MAURIN, TATIANA; DOS ANJOS-GARCIA, TAYLLON; MEDEIROS, PRISCILA; DA SILVA, JULIANA ALMEIDA; LOVICK, THELMA ANDERSON; COIMBRA, NORBERTO CYSNE. The endogenous opioid system modulates defensive behavior evoked by Crotalus durissus terrificus: Panicolytic-like effect of intracollicular non-selective opioid receptors blockade. JOURNAL OF PSYCHOPHARMACOLOGY, v. 33, n. 1, p. 51-61, JAN 2019. Web of Science Citations: 4.
DA SILVA, JULIANA ALMEIDA; ALMADA, RAFAEL CARVALHO; DE FIGUEIREDO, REBECA MACHADO; COIMBRA, NORBERTO CYSNE. Blockade of synaptic activity in the neostriatum and activation of striatal efferent pathways produce opposite effects on panic attack-like defensive behaviours evoked by GABAergic disinhibition in the deep layers of the superior colliculus. Physiology & Behavior, v. 196, p. 104-111, NOV 1 2018. Web of Science Citations: 1.
PASCHOALIN-MAURIN, TATIANA; DOS ANJOS-GARCIA, TAYLLON; FALCONI-SOBRINHO, LUIZ LUCIANO; DE FREITAS, RENATO LEONARDO; CYSNE COIMBRA, JADE PISSAMIGLIO; LAURE, CARLOS JULIO; COIMBRA, NORBERTO CYSNE. The Rodent-versus-wild Snake Paradigm as a Model for Studying Anxiety- and Panic-like Behaviors: Face, Construct and Predictive Validities. Neuroscience, v. 369, p. 336-349, JAN 15 2018. Web of Science Citations: 10.
FALCONI-SOBRINHO, LUIZ LUCIANO; DOS ANJOS-GARCIA, TAYLLON; DE OLIVEIRA, RICARDO; COIMBRA, NORBERTO CYSNE. Decrease in NMDA receptor-signalling activity in the anterior cingulate cortex diminishes defensive behaviour and unconditioned fear-induced antinociception elicited by GABAergic tonic inhibition impairment in the posterior hypothalamus. European Neuropsychopharmacology, v. 27, n. 11, p. 1120-1131, NOV 2017. Web of Science Citations: 8.
DA SILVA, JULIANA ALMEIDA; BIAGIONI, AUDREY FRANCESCHI; ALMADA, RAFAEL CARVALHO; DE FREITAS, RENATO LEONARDO; COIMBRA, NORBERTO CYSNE. Panicolytic-like effects caused by substantia nigra pars reticulata pretreatment with low doses of endomorphin-1 and high doses of CTOP or the NOP receptors antagonist JTC-801 in male Rattus norvegicus. Psychopharmacology, v. 234, n. 20, p. 3009-3025, OCT 2017. Web of Science Citations: 7.
COIMBRA, NORBERTO CYSNE; CALVO, FABRICIO; ALMADA, RAFAEL CARVALHO; FREITAS, RENATO LEONARDO; PASCHOALIN-MAURIN, TATIANA; DOS ANJOS-GARCIA, TAYLLON; ELIAS-FILHO, DAOUD HIBRAHIM; UBIALI, WALTER ADRIANO; LOBAO-SOARES, BRUNO; TRACEY, IRENE. OPIOID NEUROTRANSMISSION MODULATES DEFENSIVE BEHAVIOR AND FEAR-INDUCED ANTINOCICEPTION IN DANGEROUS ENVIRONMENTS. Neuroscience, v. 354, p. 178-195, JUN 23 2017. Web of Science Citations: 16.
NORBERTO C. COIMBRA; TATIANA PASCHOALIN-MAURIN; GABRIEL S. BASSI; ALEXANDRE KANASHIRO; AUDREY F. BIAGIONI; TATIANA T. FELIPPOTTI; DAOUD H. ELIAS-FILHO; JOYCE MENDES-GOMES; JADE P. CYSNE-COIMBRA; RAFAEL C. ALMADA; BRUNO LOBÃO-SOARES. Critical neuropsychobiological analysis of panic attack- and anticipatory anxiety-like behaviors in rodents confronted with snakes in polygonal arenas and complex labyrinths: a comparison to the elevated plus- and T-maze behavioral tests. Revista Brasileira de Psiquiatria, v. 39, n. 1, p. -, Mar. 2017.
NORBERTO C. COIMBRA; TATIANA PASCHOALIN-MAURIN; GABRIEL S. BASSI; ALEXANDRE KANASHIRO; AUDREY F. BIAGIONI; TATIANA T. FELIPPOTTI; DAOUD H. ELIAS-FILHO; JOYCE MENDES-GOMES; JADE P. CYSNE-COIMBRA; RAFAEL C. ALMADA; BRUNO LOBÃO-SOARES. Critical neuropsychobiological analysis of panic attack-and anticipatory anxiety-like behaviors in rodents confronted with snakes in polygonal arenas and complex labyrinths: a comparison to the elevated plus-and T-maze behavioral tests. Revista Brasileira de Psiquiatria, v. 39, n. 1, p. 72-83, Mar. 2017. Web of Science Citations: 11.
ULLAH, FARHAD; DOS ANJOS-GARCIA, TAYLLON; MENDES-GOMES, JOYCE; HIBRAHIM ELIAS-FILHO, DAOUD; FALCONI-SOBRINHO, LUIZ LUCIANO; DE FREITAS, RENATO LEONARDO; KHAN, ASMAT ULLAH; DE OLIVEIRA, RICARDO; COIMBRA, NORBERTO CYSNE. Connexions between the dorsomedial division of the ventromedial hypothalamus and the dorsal periaqueductal grey matter are critical in the elaboration of hypothalamically mediated panic-like behaviour. Behavioural Brain Research, v. 319, p. 135-147, FEB 15 2017. Web of Science Citations: 14.
DOS ANJOS-GARCIA, TAYLLON; ULLAH, FARHAD; FALCONI-SOBRINHO, LUIZ LUCIANO; COIMBRA, NORBERTO CYSNE. CB1 cannabinoid receptor-mediated anandamide signalling reduces the defensive behaviour evoked through GABA(A) receptor blockade in the dorsomedial division of the ventromedial hypothalamus. Neuropharmacology, v. 113, n. A, p. 156-166, FEB 2017. Web of Science Citations: 17.
FALCONI-SOBRINHO, LUIZ LUCIANO; DOS ANJOS-GARCIA, TAYLLON; ELIAS-FILHO, DAOUD HIBRAHIM; COIMBRA, NORBERTO CYSNE. Unravelling cortico-hypothalamic pathways regulating unconditioned fear-induced antinociception and defensive behaviours. Neuropharmacology, v. 113, n. A, p. 367-385, FEB 2017. Web of Science Citations: 15.
DE OLIVEIRA, RICARDO; DE OLIVEIRA, RITHIELE CRISTINA; FALCONI-SOBRINHO, LUIZ LUCIANO; SOARES, JR., RAIMUNDO DA SILVA; COIMBRA, NORBERTO CYSNE. 5-Hydroxytryptamine(2A/2C) receptors of nucleus raphe magnus and gigantocellularis/paragigantocellularis pars alpha reticular nuclei modulate the unconditioned fear-induced antinociception evoked by electrical stimulation of deep layers of the superior colliculus and dorsal periaqueductal grey matter. Behavioural Brain Research, v. 316, p. 294-304, JAN 1 2017. Web of Science Citations: 9.
BIAGIONI, AUDREY FRANCESCHI; DE OLIVEIRA, RITHIELE CRISTINA; DE OLIVEIRA, RICARDO; DA SILVA, JULIANA ALMEIDA; DOS ANJOS-GARCIA, TAYLION; RONCON, CAMILA MARRONI; CORRADO, ALEXANDRE PINTO; ZANGROSSI, JR., HELIO; COIMBRA, NORBERTO CYSNE. 5-Hydroxytryptamine(1A) receptors in the dorsomedial hypothalamus connected to dorsal raphe nucleus inputs modulate defensive behaviours and mediate innate fear-induced antinociception. European Neuropsychopharmacology, v. 26, n. 3, p. 532-545, MAR 2016. Web of Science Citations: 17.
BIAGIONI, AUDREY FRANCISCO; DOS ANJOS-GARCIA, TAYLLON; ULLAH, FARHAD; FISHER, ISAAC RENE; FALCONI-SOBRINHO, LUIZ LUCIANO; DE FREITAS, RENATO LEONARDO; FELIPPOTTI, TATIANA TOCCHINI; COIMBRA, NORBERTO CYSNE. Neuroethological validation of an experimental apparatus to evaluate oriented and non-oriented escape behaviours: Comparison between the polygonal arena with a burrow and the circular enclosure of an open-field test. Behavioural Brain Research, v. 298, n. B, p. 65-77, FEB 1 2016. Web of Science Citations: 15.
RONCON, CAMILA MARRONI; ALMADA, RAFAEL CARVALHO; MARASCHIN, JHONATAN CHRISTIAN; AUDI, ELISABETH APARECIDA; ZANGROSSI, JR., HELIO; GRAEFF, FREDERICO GUILHERME; COIMBRA, NORBERTO CYSNE. Pharmacological evidence for the mediation of the panicolytic effect of fluoxetine by dorsal periaqueductal gray matter mu-opioid receptors. Neuropharmacology, v. 99, p. 620-626, DEC 2015. Web of Science Citations: 15.
ULLAH, FARHAD; DOS ANJOS-GARCIA, TAYLLON; DOS SANTOS, IEDA REGINA; BIAGIONI, AUDREY FRANCISCO; COIMBRA, NORBERTO CYSNE. Relevance of dorsomedial hypothalamus, dorsomedial division of the ventromedial hypothalamus and the dorsal periaqueductal gray matter in the organization of freezing or oriented and non-oriented escape emotional behaviors. Behavioural Brain Research, v. 293, p. 143-152, OCT 15 2015. Web of Science Citations: 26.
ALMADA, R. C.; RONCON, C. M.; ELIAS-FILHO, D. H.; COIMBRA, N. C. ENDOCANNABINOID SIGNALING MECHANISMS IN THE SUBSTANTIA NIGRA PARS RETICULATA MODULATE GABAergic NIGROTECTAL PATHWAYS IN MICE THREATENED BY URUTU-CRUZEIRO VENOMOUS PIT VIPER. Neuroscience, v. 303, p. 503-514, SEP 10 2015. Web of Science Citations: 19.
DA SILVA, JULIANA ALMEIDA; BIAGIONI, AUDREY FRANCISCO; ALMADA, RAFAEL CARVALHO; DE SOUZA CRIPPA, JOSE ALEXANDRE; CECILIO HALLAK, JAIME EDUARDO; ZUARDI, ANTONIO WALDO; COIMBRA, NORBERTO CYSNE. Dissociation between the panicolytic effect of cannabidiol microinjected into the substantia nigra, pars reticulata, and fear-induced antinociception elicited by bicuculline administration in deep layers of the superior colliculus: The role of CB1-cannabinoid receptor in the ventral mesencephalon. European Journal of Pharmacology, v. 758, p. 153-163, JUL 5 2015. Web of Science Citations: 12.
TEIXEIRA GONCALVES, THAIS CRISTINA; LONDE, ANNA KARLA; PIRES ALBANO, RAFAEL ISAAC; DE ARAUJO JUNIOR, ARTUR TEIXEIRA; AZEREDO, MARIANA DE AGUIAR; BIAGIONI, AUDREY FRANCISCO; FERREIRA VASCONCELLOS, THIAGO HENRIQUE; DOS REIS FERREIRA, CELIO MARCOS; TEIXEIRA, DULCINEA GONCALVES; DE SOUZA CRIPPA, JOSE ALEXANDRE; VIEIRA, DEBORA; COIMBRA, NORBERTO CYSNE. Cannabidiol and endogenous opioid peptide-mediated mechanisms modulate antinociception induced by transcutaneous electrostimulation of the peripheral nervous system. JOURNAL OF THE NEUROLOGICAL SCIENCES, v. 347, n. 1-2, p. 82-89, DEC 15 2014. Web of Science Citations: 5.
DE FREITAS, RENATO LEONARDO; SALGADO-ROHNER, CARLOS JOSE; CECILIO HALLAK, JAIME EDUARDO; DE SOUZA CRIPPA, JOSE ALEXANDRE; COIMBRA, NORBERTO CYSNE. Involvement of prelimbic medial prefrontal cortex in panic-like elaborated defensive behaviour and innate fear-induced antinociception elicited by GABA(A) receptor blockade in the dorsomedial and ventromedial hypothalamic nuclei: role of the endocannabinoid CB1 receptor. INTERNATIONAL JOURNAL OF NEUROPSYCHOPHARMACOLOGY, v. 16, n. 8, p. 1781-1798, SEP 2013. Web of Science Citations: 23.
BIAGIONI, AUDREY FRANCISCO; DE FREITAS, RENATO LEONARDO; DA SILVA, JULIANA ALMEIDA; DE OLIVEIRA, RITHIELE CRISTINA; DE OLIVEIRA, RICARDO; ALVES, VANI MARIA; COIMBRA, NORBERTO CYSNE. Serotonergic neural links from the dorsal raphe nucleus modulate defensive behaviours organised by the dorsomedial hypothalamus and the elaboration of fear-induced antinociception via locus coeruleus pathways. Neuropharmacology, v. 67, p. 379-394, APR 2013. Web of Science Citations: 29.

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