NMDA and AMPA/kainate glutamatergic receptors in the prelimbic medial prefrontal cortex modulate the elaborated defensive behavior and innate fear-induced antinociception elicited by GABAA receptor blockade in the medial hypothalamus

Cerebral Cortex

Volumn 24, Issue 6, 2014, Pages 1518-1528

  De Freitas, Renato Leonardo ^a   Salgado Rohner, Carlos José ^a   Biagioni, Audrey Francisco ^a   Medeiros, Priscila ^a,c   Hallak, Jaime Eduardo Cecílio ^b,d   Crippa, José Alexandre S ^b,d   Coimbra, Norberto Cysne ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Departamento de Neurociências e Ciências Do Comportamento Setor de Psiquiatria   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Amino 3 hydroxy 5 methyl isoxazole 4 proprionate kainate receptors; aminobutyric acid A receptors; Dorsomedial hypothalamus; Innate fear induced antinociception; N methyl D aspartate receptors; Paniclike behavior; Prelimbic medial prefrontal cortex

Indexed keywords

6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; BICUCULLINE; DECAHYDRO 6 PHOSPHONOMETHYL 3 ISOQUINOLINECARBOXYLIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; SODIUM CHLORIDE; 2,3-DIOXO-6-NITRO-7-SULFAMOYLBENZO(F)QUINOXALINE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR BLOCKING AGENT; AMPA RECEPTOR; ISOQUINOLINE DERIVATIVE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; QUINOXALINE DERIVATIVE;

ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DEFENSIVE BEHAVIOR; DRUG EFFECT; FEAR; MALE; MEDIAL PREFRONTAL CORTEX; MEDIOBASAL HYPOTHALAMUS; MICROINJECTION; NEUROTRANSMISSION; NONHUMAN; PANIC; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STIMULATION; WISTAR RAT; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; METABOLISM; NOCICEPTION; NOCICEPTIVE PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; BEHAVIOR, ANIMAL; BICUCULLINE; EXCITATORY AMINO ACID ANTAGONISTS; FEAR; GABA-A RECEPTOR ANTAGONISTS; HYPOTHALAMUS, MIDDLE; ISOQUINOLINES; MALE; NOCICEPTIVE PAIN; PAIN PERCEPTION; PANIC; PREFRONTAL CORTEX; QUINOXALINES; RATS, WISTAR; RECEPTORS, AMPA; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 84900821087     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht001     Document Type: Article

References (71)

1. Aimone LD, Bauer CA, Gebhart GF. 1988. Brainstem relays mediating stimulation-produced antinociception from the lateral hypothala-mus in the rat. J Neurosci. 8:2652-2663.
2. Beitz AJ. 1982. The organisation of afferent projections to the mid-brain periaqueductal gray of the rat. Neuroscience. 7:133-135.
3. Biagioni AF, de Freitas RL, da Silva JA, de Oliveira RC, de Oliveira R, Alves MA, Coimbra NC. 2013. 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. Neurophar-macology. 67:379-394.
4. Biagioni AF, Silva JA, Coimbra NC. 2012. Panic-like defensive behavior but not fear-induced antinociception is differently organized by dorsomedial and posterior hypothalamic nuclei of Rattus nor-vegicus (Rodentia, Muridae). Braz J Med Biol Res. 45:328-336.
5. Bueno CH, Zangrossi HJ, Viana MB, Zanoveli J. 2007. GABA/benzo-diazepine receptors in the ventromedial hypothalamic nucleus regulate both anxiety and panic-related defensive responses in the elevated T-maze. Brain Res Bull. 74:134-141.
6. Calejesan AA, Kim SJ, Zhuo M. 2000. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur J Pain. 4:83-96.
7. Cameron AA, Khan IA, Westlund KN, Cliffer KD, Willis WD. 1995. The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris-leucoagglutinin study. I. Ascending projections. J Comp Neurol. 351:568-584.
8. Cameron AA, Khan IA, Westlund KN, Willis WD. 1995. The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris-leucoagglutinin study. II. Descending projections. J Comp Neurol. 351:585-601.
9. Coimbra NC, Brandão ML. 1993. GABAergic nigro-collicular pathways modulate the defensive behaviour elicited by midbrain tectum stimulation. Behav Brain Res. 59:131-139.
10. Coimbra NC, De Oliveira R, Freitas RL, Ribeiro SJ, Borelli KG, Pacag-nella RC, Moreira JE, da Silva LA, Melo LL, Lunardi LO et al. 2006. Neuroanatomical approaches of the tectum-reticular pathways and immunohistochemical evidence for serotonin-positive perikarya on neuronal substrates of the superior colliculus and periaqueduc-tal gray matter involved in the elaboration of the defensive behavior and fear-induced analgesia. Exp Neurol. 197:93-112.
11. de Freitas RL, Salgado-Rohner CJ, Hallak JEC, Crippa JAS, Coimbra NC. 2011. Medial pre-frontal cortex and CB1 endocannabinoid receptors in the antinociception induced by elaborated escape behaviour caused by disinhibition of hypothalamus. Eur J Pain. 5:107-108.
12. DiMicco JA, Stotz-Potter EH, Monroe AJ, Morin SM. 1996. Role of dor-somedial hypothalamus in the cardiovascular response to stress. Clin Exp Pharmacol Physiol. 23:171-176.
13. Ducrocq F, Vaiva G, Cottencin O, Molenda S, Bailly D. 2001. Post-traumatic stress, post-traumatic depression and major depressive episode: literature. Encéphale. 2:159-168.
14. Eichenberger GCD, Ribeiro SJ, Osaki MY, Maruoka RY, Resende GCC, Castellan-Baldan L, Corrêa SA, Da Silva LA, Coimbra NC. 2002. Neuroanatomical and psychopharmacological evidence for interaction between opioid and GABAergic neural pathways in the modulation of fear and defense elicited by electrical and chemical stimulation of the deep layers of the superior colliculus and dorsal periaqueductal gray matter. Neuropharmacology. 42:48-59.
15. Fleck MW, Henze DA, Barrionuevo G, Palmer AM. 1993. Aspartate and glutamate mediate excitatory synaptic transmission in area CA1 of the hippocampus. J Neurosci. 13:3944-3955.
16. Freitas RL, Salgado-Rohner CJ, Hallak JEC, Crippa JAS, Coimbra NC. 2011. Role of medial prefrontal cortex in the GABAergic modulation of elaborated defensive behaviour organised by medial hypothalamus. Eur Neuropsychopharmacol. 21:S300.
17. A receptor blockade in dorsomedial and ventromedial nuclei of the hypothalamus evokes panic-like elaborated defensive behaviour followed by innate fear-induced antino-ciception. Brain Res. 1305:118-131.
18. Frysztak RJ, Neafsey EJ. 1994. The effect of medial frontal cortex lesions on cardiovascular conditioned emotional responses in the rat. Brain Res. 643:181-193.
19. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ. 2005. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol. 492:145-177.
20. Gigg J, Tan AM, Finch DM. 1994. Glutamatergic hippocampal formation projections to prefrontal cortex in the rat are regulated by GABAergic inhibition and show convergence with glutamatergic projections from the limbic thalamus. Hippocampus. 4:189-198.
21. Graff-Guerrero A, González-Olvera J, Fresán A, Gómez-Martín D, Méndez-Núñez JC, Pellicer F. 2005. Repetitive transcranial magnetic stimulation of dorsolateral prefrontal cortex increases tolerance to human experimental pain. Brain Res. 25:153-160.
22. Heidbreder CA, Groenewegen HJ. 2003. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci Biobehav Rev. 27:555-579.
23. Hollmann M, Heinemann S. 1994. Cloned glutamate receptors. Ann Rev Neurosci. 17:31-108. Review.
24. Hurley KM, Herbert H, Moga MM, Saper CB. 1991. Efferent projections of the infralimbic cortex of the rat. J Comp Neurol. 308:249-276.
25. Jasmin L, Rabkin SD, Granato A, Boudah A, Ohara PT. 2003. Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature. 424:316-320.
26. Jingami H, Nakanishi S, Morikawa K. 2003. Structure of the metabotro-pic glutamate receptor. Curr Opin Neurobiol. 13:271-278. Review.
27. Johnson PL, Lowry CA, Truitt W, Shekhar A. 2008. Disruption of GABAergic tone in the dorsomedial hypothalamus attenuates responses in a subset of serotonergic neurons in the dorsal raphe nucleus following lactate-induced panic. J Psychopharmacol. 22:642-652.
28. Johnson PL, Shekhar A. 2006. Panic-prone state induced in rats with GABA dysfunction in the dorsomedial hypothalamus is mediated by NMDA receptors. J Neurosci. 26:7093-7104.
29. Kemp JA, McKernan RM. 2002. NMDA receptor pathways as drug targets. Nat Neurosci. 5:1039-1042.
30. Khodorov B. 2004. Glutamate-induced deregulation of calcium homeostasis and mitochondrial dysfunction in mammalian central neurones. Progr Biophys Mol Biol. 86:279-351.
31. Kita H, Oomura Y. 1981. Reciprocal connections between the lateral hypothalamus and the frontal complex in the rat: electrophysio-logical and anatomical observations. Brain Res. 213:1-16.
32. Lacroix L, Spinelli S, Heidbreder CA, Feldon J. 2000. Differential role of the medial and lateral prefrontal cortices in fear and anxiety. Behav Neurosci. 114:1119-1130.
33. LeDoux JE. 1993. Emotional memory systems in the brain. Behav Brain Res. 58:69-79. Review.
34. Lee HS, Kim MA, Waterhouse BD. 2005. Retrograde double-labeling study of common afferent projections to the dorsal raphe nucleus and the nuclear core of the locus coeruleus in the rat. J Comp Neurol. 481:179-193.
35. Leonard CL, Baum SR, Pell MD. 2001. The effect of compressed speech on the ability of right-hemisphere-damaged patients to use context. Cortex. 37:327-344.
36. Lumb BM. 2004. Hypothalamic and midbrain circuitry that distinguishes between escapable and inescapable pain. News Physiol Sci. 19:22-26.
37. Malin EL, Ibrahim DY, Tu JW, McGaugh JL. 2007. Involvement of the rostral anterior cingulate cortex in consolidation of inhibitory avoidance memory: interaction with the basolateral amygdala. Neurobiol Learn Mem. 87:295-302.
38. Malizia AL. 1999. What do brain imaging studies tell us about anxiety disorders? J Psychopharmacol. 13:372-378.
39. McDonald AJ, Mascagni F, Guo L. 1996. Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neurosci. 71:55-75.
40. Moghaddam B. 1993. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem. 60: 1650-1657.
41. Morgan MA, LeDoux JE. 1995. Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav Neurosci. 109:681-688.
42. Morrow BA, Elsworth JD, Inglis FM, Roth RH. 1999. An antisense oli-gonucleotide reverses the footshock-induced expression of Fos in the rat medial prefrontal cortex and the subsequent expression of conditioned fear-induced immobility. J Neurosci. 13:5666-5673.
43. Morrow BA, Elsworth JD, Lee EJ, Roth RH. 2000. Divergent effects of putative anxiolytics on stress-induced for expression in the meso-prefrontal system of the rat. Synapse. 36:143-154.
44. Morshedi MM, Meredith GE. 2008. Repeated amphetamine administration induces Fos in prefrontal cortical neurons that project to the lateral hypothalamus but not the nucleus accumbens or baso-lateral amygdala. Psychopharmacology. 197:179-189.
45. Nicolle MM, Baxter MG. 2003. Glutamate receptor binding in the frontal cortex and dorsal striatum of aged rats with impaired atten-tional set-shifting. Eur J Neurosci. 18:3335-3342.
46. Paxinos G, Watson C. 1997. The rat brain in sterotaxic coordinates. London: Academic Press.
47. Petrovic P, Carlsson K, Petersson KM, Hansson P, Ingvar M. 2004. Context-dependent deactivation of the amygdala during pain. J Cogn Neurosci. 16:1289-1301.
48. Prado WA, Roberts MHT. 1985. An assessment of the antinociceptive and aversive effects of stimulating identified sites in the rat brain. Brain Res. 340:219-228.
49. Quirk GJ, Likhtik E, Pelletier JG, Paré D. 2003. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci. 24:8800-8807.
50. Radley JJ, Gosselink KL, Sawchenko PE. 2009. A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuro-endocrine stress response. J Neurosci. 29:7330-7340.
51. Resstel LB, Corrêa FMA. 2006. Injection of l-glutamate into medial prefrontal cortex induces cardiovascular responses through NMDA receptor-nitric oxide in rat. Neuropharmacology. 51:160-167.
52. Resstel LB, Corrêa FMA, Guimarães FS. 2008. The expression of contextual fear conditioning involves activation of an NMDA receptor-nitric oxide pathway in the medial prefrontal cortex. Cereb Cortex. 18:2027-2035.
53. Erratum in: Cerebral Cortex. 2009;19:992.
54. Salgado-Rohner CJ, de Freitas RL, Coimbra NC. 2011. Noradrenergic pathways between locus coeruleus and dorsal raphe nucleus mediate analgesia induced by defensive behaviour evoked by lateral hypothalamus. Eur J Pain. 5:205
55. Schmitt P, Carrive P, Discala G, Jenck F, Brandão ML, Bagri A, Moreau JL, Sandner G. 1986. A neuropharmacological study of the periventricular neural substrate involved in flight. Behav Brain Res. 22:181-190.
56. Schulkin J, Morgan MA, Rosen JB. 2005. A neuroendocrine mechanism for sustaining fear. Trends Neurosci. 28:629-635.
57. Sesack SR, Deustch AY, Roth RH, Bunney BS. 1989. Topographical organisation of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol. 290:213-242.
58. Shah AA, Treit D. 2003. Excitotoxic lesions of the medial prefrontal cortex attenuate fear responses in the elevated-plus maze, social interaction and shock probe burying tests. Brain Res. 969: 183-194.
59. Shekhar A. 1993. GABA blockade in the region of the dorsomedial hypothalamus regulates "anxiety" in rats in the elevated plus maze: I. Behavioral measures. Brain Res. 627:9-16.
60. Shekhar A, DiMicco JA. 1987. Defense reaction elicited by injection of GABA antagonists and synthesis inhibitors into the posterior hypothalamus in rats. Neuropharmacology. 26:407-417.
61. Shekhar A, Keim SR. 1997. The circumventricular organs form a potential neural pathway for lactate sensitivity: implication for panic disorder. J Neurosci. 17:9726-9735.
62. Shekhar A, Keim SR, Simon JR, McBride WJ. 1996. Physiological arousal elicited by sodium lactate infusion in rats with dorsomedial hypothalamic GABA dysfunction. Pharmacol Biochem Behav. 55:249-256.
63. Sierra-Mercado D Jr, Corcoran KA, Lebrón-Milad K, Quirk GJ. 2006. Inactivation of the ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. Eur J Neurosci. 24:1751-1758.
64. Stamford JA. 1995. Descending control of pain. Br J Anaesth. 75:217-227.
65. Sullivan RM, Gratton A. 1999. Lateralized effects of medial prefrontal cortex lesions on neuroendocrine and autonomic stress responses in rats. J Neurosci. 19:2834-2840.
66. Swanson LW. 1981. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res. 217:150-154.
67. Tavares RF, Corrêa FMA, Resstel LB. 2009. Opposite role of infralim-bic and prelimbic cortex in the tachycardiac response evoked by acute restraint stress in rats. J Neurosci Res. 19:2834-2840.
68. Thompson RH, Canteras NS, Swanson LW. 1996. Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J Comp Neurol. 376:143-173.
69. Verberne AJM, Owens NC. 1998. Cortical modulation of the cardiovascular system. Prog Neurobiol. 54:149-156.
70. Wilent WB, Oh MY, Buetefisch CM, Bailes JE, Cantella D, Angle C, Whiting DM. 2010. Induction of panic attack by stimulation of the ventromedial hypothalamus. J Neurosurg. 112:1295-1298.
71. Zhang L, Zhang Y, Zhao ZQ. 2005. Anterior cingulate cortex contributes to the descending facilitatory modulation of pain via dorsal reticular nucleus. Eur J Neurosci. 22:1141-1148.