Further evidence for involvement of the dorsal hippocampus serotonergic and γ-aminobutyric acid (GABA)ergic pathways in the expression of contextual fear conditioning in rats

Journal of Psychopharmacology

Volumn 27, Issue 12, 2013, Pages 1160-1168

  Almada, Rafael C ^a,b   Albrechet Souza, Lucas ^a,b   Brandão, Marcus L ^a,b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Instituto de Neurociencias and Comportamento INeC   (Brazil)

Author keywords

Contextual fear; dorsal hippocampus; GABA; medial prefrontal cortex; serotonin

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 4 AMINOBUTYRIC ACID; MUSCIMOL; PROTEIN FOS; SEROTONIN; SEROTONIN AGONIST;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATALEPSY; CATECHOLAMINERGIC SYSTEM; CONTROLLED STUDY; FEAR; FEAR POTENTIATED STARTLE; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; MICROINJECTION; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STARTLE REFLEX; ANIMAL; ANIMAL BEHAVIOR; BRAIN; CONDITIONING; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; TIME; WISTAR RAT;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CONDITIONING (PSYCHOLOGY); FEAR; FREEZING REACTION, CATALEPTIC; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MALE; MUSCIMOL; PREFRONTAL CORTEX; RATS; RATS, WISTAR; REFLEX, STARTLE; SEROTONIN; SEROTONIN RECEPTOR AGONISTS; TIME FACTORS;

EID: 84887848774     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881113482840     Document Type: Article

References (67)

1. Albrechet-Souza L, Borelli KG, Almada RC, et al. Midazolam reduces the selective activation of the rhinal cortex by contextual fear stimuli. Behav Brain Res. 2011 ; 216: 631-638
2. Albrechet-Souza L, Carvalho MC, Brandão ML. D1-like receptors in the nucleus accumbens shell regulate the expression of contextual fear conditioning and activity of the anterior cingulate cortex in rats. Int J Neuropsychopharmacol. 2012 ;:
3. Almada RC, Borelli KG, Albrechet-Souza L, et al. Serotonergic mechanisms of the median raphe nucleus-dorsal hippocampus in conditioned fear: Output circuit involves the prefrontal cortex and amygdala. Behav Brain Res. 2009 ; 203: 279-287
4. Amaral OB, Luft T, Cammarota M, et al. Temporary inactivation of the dorsal hippocampus induces a transient impairment in retrieval of aversive memory. Behav Brain Res. 2007 ; 180: 113-118
5. Ammassari-Teule M, Pavone F, Castellano C, et al. Amygdala and dorsal hippocampus lesions block the effects of GABAergic drugs on memory storage. Brain Res. 1991 ; 551: 104-109
6. Avanzi V, Brandão ML. Activation of somatodendritic 5-HT1A autoreceptors in the median raphe nucleus disrupts the contextual conditioning in rats. Behav Brain Res. 2001 ; 126: 175-184
7. Avanzi V, Castilho VM, de Andrade TG, et al. Regulation of contextual conditioning by the median raphe nucleus. Brain Res. 1998 ; 790: 178-184
8. Azmitia EC, Segal M. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol. 1978 ; 179: 641-667
9. Barker GRI, Warburton EC. When is the hippocampus involved in recognition memory?. J Neurosci. 2011 ; 31: 10721-10731
10. Beck CH, Fibiger HC. Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: With and without diazepam pretreatment. J Neurosci. 1995 ; 15: 709-720
11. Berlau DJ, McGaugh JL. Enhancement of extinction memory consolidation: The role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol Learn Mem. 2006 ; 86: 123-132
12. Bevilaqua L, Ardenghi P, Schröder N, et al. Drugs acting upon the cyclic adenosine monophosphate/protein kinase: A signalling pathway modulate memory consolidation when given late after training into rat hippocampus but not amygdala. Behav Pharmacol. 1997 ; 8: 331-338
13. Blum S, Hebert AE, Dash PK. A role for the prefrontal cortex in recall of recent and remote memories. Neuroreport. 2006 ; 17: 341-344
14. Borelli KG, Gárgaro AC, dos Santos JM, et al. Effects of inactivation of serotonergic neurons of the median raphe nucleus on learning and performance of contextual fear conditioning. Neurosci Lett. 2005 ; 387: 105-110
15. Bouton ME, Bolles RC. Conditioned fear assessed by freezing and by the suppression of three different baselines. Anim Learn Behav. 1980 ; 8: 429-434
16. Brandão ML, Borelli KG, Nobre MJ, et al. Gabargic regulation of the neural organization of fear in the midbrain tectum. Neurosci Biobehav Rev. 2005 ; 29: 1299-1311
17. Brioni JD, McGaugh JL. Post-training administration of GABAergic antagonists enhances retention of aversively motivated tasks. Psychopharmacology (Berl). 1988 ; 96: 505-510
18. Chang SD, Liang KC. Roles of hippocampal GABAA and muscarinic receptors in consolidation of context memory and context-shock association in contextual fear conditioning: A double dissociation study. Neurobiol Learn Mem. 2012 ; 98: 17-24
19. Davis M, Falls WA, Campeau S, et al. Fear-potentiated startle: A neural and pharmacological analysis. Behav Brain Res. 1993 ; 58: 175-198
20. Daumas S, Halley H, Francés B, et al. Encoding, consolidation, and retrieval of contextual memory: Differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learn Mem. 2004 ; 12: 375-382
21. Deakin JF, Graeff FG. 5-HT and mechanisms of defence. J Psychopharmacol. 1991 ; 5: 305-315
22. Fanselow MS. What is conditioned fear?. Trends Neurosci. 1984 ; 7: 460-462
23. Fanselow MS. Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res. 2000 ; 110: 73-81
24. Ferino F, Thierry AM, Glowinski J. Anatomical and electrophysiological evidence for a direct projection from Ammon's horn to the medial prefrontal cortex in the rat. Exp Brain Res. 1987 ; 65: 421-426
25. Ferry B, Roozendaal B, McGaugh JL. Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between β- and α1-adrenoceptors. J Neurosci. 1999 ; 19: 5119-5123
26. Fischette CT, Nock B, Renner K. Effects of 5,7-dihydroxytryptamine on serotonin1 and sertotonin2 receptors throughout the rat central nervous system using quantitative autoradiography. Brain Res. 1987 ; 421: 263-279
27. Goosens KA. Hippocampal regulation of aversive memories. Curr Opin Neurobiol. 2011 ; 21: 460-466
28. Goosens KA, Hobin JA, Maren S. Auditory-evoked spike firing in the lateral amygdala and Pavlovian fear conditioning: Mnemonic coding of fear bias?. Neuron. 2003 ; 40: 1013-1022
29. Graeff FG, Rawlins JN. Dorsal periaqueductal gray punishment, septal lesions and the mode of action of minor tranquilizers. Pharmacol Biochem Behavior. 1980 ; 12: 41-45
30. Graeff FG, Schoenfeld RI. Tryptaminergic mechanisms in punished and nonpunished behavior. J Pharmacol Exp Ther. 1970 ; 173: 277-283
31. Graeff FG, Guimarães FS, De Andrade TG, et al. Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav. 1996 ; 54: 129-141
32. Grillon C. Startle reactivity and anxiety disorders: Aversive conditioning, context, and neurobiology. Biol Psychiatry. 2002 ; 52: 958-975
33. Gross CT, Canteras NS. The many paths to fear. Nat Rev Neurosci. 2012 ; 13: 651-658
34. Holt W, Maren S. Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. J Neurosci. 1999 ; 19: 9054-9062
35. Jay TM, Witter MP. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol. 1991 ; 313: 574-586
36. Jay TM, Thierry AM, Wiklund L, et al. Excitatory amino-acid pathway from the hippocampus to the prefrontal cortex: Contribution of AMPA receptors in hippocampo-prefrontal cortex transmission. Eur J Neurosci. 1992 ; 4: 1285-1295
37. Katsurabayashi S, Kubota H, Tokutomi N, et al. A distinct distribution of functional presynaptic 5-HT receptor subtypes on GABAergic nerve terminals projecting to single hippocampal CA1 pyramidal neurons. Neuropharmacology. 2003 ; 44: 1022-1030
38. Kim JJ, Fanselow MS. Modality-specific retrograde amnesia of fear. Science. 1992 ; 256: 675-677
39. Kiser RS, Lebovitz RM. Monoaminergic mechanisms in aversive brain stimulation. Physiol Behav. 1975 ; 15: 47-53
40. Kiser RS, Brown CA, Sanghera MK, et al. Dorsal raphe nucleus stimulation reduces centrally-elicited fearlike behavior. Brain Res. 1980 ; 191: 265-272
41. McEown K, Treit D. Inactivation of the dorsal or ventral hippocampus with muscimol differentially affects fear and memory. Brain Res. 2010 ; 1353: 145-151
42. McGaugh JL, Izquierdo I. The contribution of pharmacology to research on the mechanisms of memory formation. Trends Pharmacol Sci. 2000 ; 21: 208-210
43. McNaughton N, Corr PJ. A two-dimensional neuropsychology of defense: Fear/anxiety and defensive distance. Neurosci Biobehav Rev. 2004 ; 28: 285-305
44. Maren S. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci. 2001 ; 24: 897-931
45. Martinez RCB, De Oliveira A, Brandão ML. Conditioned and unconditioned fear organized in the periaqueductal gray are differentially sensitive to injections of muscimol. Neurobiol Learn Mem. 2006 ; 85: 58-65
46. Matus-Amat P, Higgins EA, Sprunger D, et al. The role of dorsal hippocampus and basolateral amygdala NMDA receptors in the acquisition and retrieval of context and contextual fear memories. Behav Neurosci. 2007 ; 121: 721-731
47. Mendelson SD, McEwen BS. Autoradiographic analyses of the effects of the restraint-induced stress on 5-HT1A, 5-HT1c and 5-HT2 receptors in the dorsal hippocampus of male and female rats. Neuroendocrinology. 1991 ; 54: 454-461
48. Milanovic S, Radulovic J, Laban O, et al. Production of the Fos protein after contextual fear conditioning of C57BL/6N mice. Brain Res. 1998 ; 784: 37-47
49. Mobbs D, Petrovic P, Marchant JL, et al. When fear is near: Threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science. 2007 ; 317: 1079-1083
50. Moreira CM, Masson S, Carvalho MC, et al. Exploratory behaviour of rats in the elevated plus-maze is differentially sensitive to inactivation of the basolateral and central amygdaloid nuclei. Brain Res Bull. 2007 ; 71: 466-474
51. Paxinos G, Watson C The rat brain in stereotaxic coordinates. 2007 ) The rat brain in stereotaxic coordinates, 6th edition.San Diego: Academic Press. San Diego: Academic Press ; 2007:
52. Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci. 1992 ; 106: 274-285
53. Reimer AE, Oliveira AR, Brandão ML. Selective involvement of GABAergic mechanisms of the dorsal periaqueductal gray and inferior colliculus on the memory of the contextual fear as assessed by the fear potentiated startle test. Brain Res Bull. 2008 ; 76: 545-550
54. Roozendaal B, McEwen BS, Chattarji S. Stress, memory and the amygdala. Nature Reviews. 2009 ; 10: 423-433
55. Rossato JI, Bonini JS, Coitinho AS, et al. Retrograde amnesia induced by drugs acting on different molecular systems. Behav Neurosci. 2004 ; 118: 563-568
56. Santos JM, Gárgaro AC, Oliveira AR, et al. Pharmacological dissociation of moderate and high contextual fear as assessed by freezing behavior and fear-potentiated startle. Eur Neuropsychopharmacol. 2005 ; 15: 239-246
57. Schenberg LC, Graeff FG. Role of the periaqueductal gray substance in the antianxiety action of benzodiazepines. Pharmacol Biochem Behav. 1978 ; 9: 287-295
58. Silva RCB, Cruz APM, Avanzi V, et al. Distinct contributions of median raphe nucleus to contextual fear conditioning and fear-potentiated startle. Neural Plast. 2002 ; 9: 233-247
59. Silva RC, Gárgaro AC, Brandão ML. Differential regulation of the expression of contextual freezing and fear-potentiated startle by 5-HT mechanisms of the median raphe nucleus. Behav Brain Res. 2004 ; 151: 93-101
60. Strekalova T, Zörner B, Zacher C, et al. Memory retrieval after contextual fear conditioning induces c-Fos and JunB expression in CA1 hippocampus. Genes Brain Behav. 2003 ; 2: 3-10
61. Swanson LW. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res. 1981 ; 217: 150-154
62. Teixeira CM, Pomedli SR, Maei HR, et al. Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J Neurosci. 2006 ; 26: 7555-7564
63. Tse D, Takeuchi T, Kakeyama M, et al. Schema-dependent gene activation and memory encoding in neocortex. Science. 2011 ; 333: 891-895
64. Weitemier AZ, Ryabinin AE. Subregion-specific differences in hippocampal activity between Delay and Trace fear conditioning: An immunohistochemical analysis. Brain Res. 2004 ; 995: 55-65
65. Winocur G, Rawlins JN, Gray JA. The hippocampus and conditioning to contextual cues. Behav Neurosci. 1987 ; 101: 617-625
66. Wise CD, Berger BD, Stein L. Benzodiazepines: Anxiety-reducing activity by reduction of serotonin turnover in the brain. Science. 1972 ; 177: 180-183
67. Zhao MG, Toyoda H, Lee YS, et al. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron. 2005 ; 47: 859-872