Interactions of the dorsal hippocampus, medial prefrontal cortex and nucleus accumbens in formation of fear memory: Difference in inhibitory avoidance learning and contextual fear conditioning

Neurobiology of Learning and Memory

Volumn 112, Issue , 2014, Pages 186-194

  Yang, Fang Chi ^a   Liang, K C ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Aversive learning; Emotion; Memory consolidation; Norepinephrine; Rats

Indexed keywords

LIDOCAINE; NORADRENALIN; VOLTAGE GATED SODIUM CHANNEL BLOCKING AGENT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTEXTUAL FEAR CONDITIONING; EXPERIMENTAL BEHAVIORAL TEST; FEAR; HIPPOCAMPUS; INHIBITORY AVOIDANCE LEARNING; LEARNING; LEARNING TEST; MALE; MEMORY CONSOLIDATION; NONHUMAN; NORADRENALIN RELEASE; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; RAT; TASK PERFORMANCE; ANIMAL; AVOIDANCE BEHAVIOR; BRAIN FORNIX; CONDITIONED REFLEX; DRUG EFFECTS; LONG TERM MEMORY; MEMORY; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; FEAR; FORNIX, BRAIN; LIDOCAINE; MALE; MEMORY; NOREPINEPHRINE; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; RATS; RATS, WISTAR; RETENTION (PSYCHOLOGY); VOLTAGE-GATED SODIUM CHANNEL BLOCKERS;

EID: 84901920169     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.07.017     Document Type: Article

References (73)

1. Amorapanth P., LeDoux J.E., Nader K. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nature Neuroscience 2000, 3:74-79.
2. Baeg E.H., Kim Y.B., Jang J., Kim H.T., Mook-Jung I., Jung M.W. Fast spiking and regular spiking neural correlates of fear conditioning in the medial prefrontal cortex of the rat. Cerebral Cortex 2001, 11:441-451.
3. Barros D.M., Mello e Souza T., De David T., Choi H., Aguzzoli A., Madche C., et al. Simultaneous modulation of retrieval by dopaminergic D1, β-noradrenergic, serotonergic-1A and cholinergic muscarinic receptors in cortical structures of the rat. Behavioural Brain Research 2001, 124:1-7.
4. Brog J.S., Salyapongse A., Deutch A.Y., Zahm D.S. The patterns of afferent innervation of the core and shell in the "accumbens" part of the rat ventral striatum: Immnohistochemical detection of retrogradely transported Fluoro-Gold. The Journal of Comparative Neurology 1993, 338:255-278.
5. Brunson K., Chen Y., Avishai-Eliner S., Baram T. Stress and the developing hippocampus. Molecular Neurobiology 2003, 27:121-136.
6. Cammarota M., Bevilaqua L.R.M., Kerr D., Medina J.H., Izquierdo I. Inhibition of mRNA and protein synthesis in the CA1 region of the dorsal hippocampus blocks reinstallment of an extinguished conditioned fear response. The Journal of Neuroscience 2003, 23:737-741.
7. Chang S.D., Chen D.Y., Liang K.C. Infusion of lidocaine into the dorsal hippocampus before or after the shock training phase impaired conditioned freezing in a two-phase training task of contextual fear conditioning. Neurobiology of Learning and Memory 2008, 89:95-105.
8. A and muscarinic receptors in consolidation of context memory and context-shock association in contextual fear conditioning: A double dissociation study. Neurobiology of Learning and Memory 2012, 98:17-24.
9. Conde F., Maire-lepoivre E., Audinat E., Crepel F. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. The Journal of Comparative Neurology 1995, 352:567-593.
10. Davis M. The role of the amygdala in fear and anxiety. Annual Review of Neuroscience 1992, 15:353-375.
11. Fanselow M.S., LeDoux J.E. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 1999, 23:229-232.
12. Finch D.M. Neurophysiology of converging synaptic inputs from the rat prefrontal cortex, amygdala, midline thalamus, and hippocampal formation onto single neurons of the caudate/putamen and nucleus accumbens. Hippocampus 1996, 6:495-512.
13. Gold P.E., van Buskirk R. Effects of posttrial hormone injections on memory processes. Hormones and Behavior 1976, 7:509-517.
14. Gold P.E., van Buskirk R. Posttraining brain norepinephrine concentrations: Correlation with retention performance of avoidance training and with peripheral epinephrine modulation of memory processing. Behavioral Biology 1978, 23:509-520.
15. Goto Y., O'Donnell P. Timing-dependent limbic-motor synaptic integration in the nucleus accumbens. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:13189-13193.
16. Graybiel A.M. Habits, rituals, and the evaluative brain. Annual Review of Neuroscience 2008, 31:359-387.
17. Groenewegen H.J., Trimble M. The ventral striatum as an interface between the limbic and motor systems. CNS Spectrums 2007, 12:887-892.
18. Groenewegen H.J., Wright C.I., Beijer A.V.J., Voorn P. Convergence and segregation of ventral striatal inputs and outputs. Annals New York Academy of Sciences 1999, 877:49-63.
19. Hatfield T., McGaugh J.L. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiology of Learning and Memory 1999, 71:232-239.
20. Hebb D.O. The organization of behavior 1949, John Wiley & Sons, New York.
21. Heidbreder C.A., Groenewegen H.J. The medial prefrontal cortex in the rat: Evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neuroscience & Biobehavioral Reviews 2003, 27:555-579.
22. Hitchcock J.M., Davis M. Fear-potentiated startle using an auditory conditioned stimulus: Effect of lesions of the amygdala. Physiology & Behavior 1987, 39:403-408.
23. Izquierdo I., Medina J.H., Izquierdo L.A., Barros D.M., de Souza M.M., Mello e Souza T. Short- and long-term memory are differentially regulated by monoaminergic systems in the rat brain. Neurobiology of Learning and Memory 1998, 69:219-224.
24. Izquierdo I., Medina J.H., Vianna M.R.M., Izquierdo L.A. Separate mechanisms for short-and long-term memory. Behavioral Brain Research 1999, 103:1-11.
25. Jay T.M., Witter M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris - Leucoagglutinin. The Journal of Comparative Neurology 1991, 313:574-586.
26. Killcross S., Robbins T.W., Everitt B.J. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 1997, 388:377-380.
27. LaLumiere R.T., Nawar E.M., McGaugh J.L. Modulation of memory consolidation by the basolateral amygdala or nucleus accumbens shell requires concurrent dopamine receptor activation in both brain regions. Learning & Memory 2005, 12:296-301.
28. LeDoux J.E. Emotion circuits in the brain. Annual Reviews of Neuroscience 2000, 23:155-184.
29. LeDoux J.E., Schiller D., Cain C. Emotional reaction and action: From threat processing to goal-directed behaivor. The cognitive neurosciences 2009, 905-924. The MIT Press, Cambridge, MA. 4th ed. M.S. Gazzaniga (Ed.).
30. Lee E.H.Y., Lee C.P., Wang H.I., Lin W.R. Hippocampal CRF, NE, and NMDA system interactions in memory processing. Synapse 1993, 14:144-153.
31. Levita L., Dalley J.W., Robbins T.W. Disruption of Pavlovian contextual conditioning by excitotoxic lesions of the nucleus accumbens core. Behavioral Neuroscience 2002, 116:539-552.
32. Levita L., Hoskin R., Champi S. Avoidance of harm and anxiety: A role for the nucleus accumbens. NeuroImage 2012, 62:189-198.
33. Liang K.C. Involvement of the amygdala and its connected structures in formation and expression of inhibitory avoidance memory: Issues and implications. Chinese Journal of Physiology 2009, 52:196-214.
34. Liang K.C. Neural circuitry involved in avoidance learning and memory: The amygdala and beyond. Progress in psychological science around the world 2006, 315-332. Psychology Press, New York. Q. Jing, M.R. Rosenzweig, G. d'Ydewalle, H. Zhang, H.C. Chen, K. Zhang (Eds.).
35. Liang K.C., McGaugh J.L., Martinez J.L., Jensen R.A., Vasquez B.J., Messing R.B. Post-training amygdaloid lesions impair retention of an inhibitory avoidance response. Behavioural Brain Research 1982, 4:237-249.
36. Liang K.C., Yen C.T., Chang C.H., Chen C.C. Involvement of the amygdala in two different forms of the inhibitory avoidance task. Novel trends in brain science 2008, 167-182. Springer, Tokyo. M. Onozuka, C.T. Yen (Eds.).
37. Lorenzini C.A., Baldi E., Bucherelli C., Sacchetti B., Tassoni G. Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response: A tetrodotoxin functional inactivation study. Brain Research 1996, 730:32-39.
38. Lorenzini A.C., Baldi E., Bucherelli C., Tassoni G. Time-dependent deficits of rat's memory consolidation induced by tetrodotoxin injections into the caudate-putamen, nucleus acumbens, and globus pallidus. Neurobiology of Learning and Memory 1995, 63:87-93.
39. Maier S.F., Watkins L.R. Stressor controllability and learned helplessness: The roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neuroscience and Biobehavioral Reviews 2005, 29:829-841.
40. Maier S.F., Watkins L.R. Role of the medial prefrontal cortex in coping and resilience. Brain Research 2010, 1335:52-60.
41. Malin E.L., McGaugh J.L. Differential involvement of the hippocampus, anterior cingulate cortex, and basolateral amygdala in memory for context and footshock. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:1953-1963.
42. Maren S. Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditional fear in rats. The Journal of Neuroscience 1999, 19:8696-8703.
43. Maren S. What the amygdala does and doesn't do in aversive learning. Learning & Memory 2003, 10:306-308.
44. Martin J.H. Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neuroscience Letters 1991, 127:160-164.
45. McGaugh J.L. Memory - A century of consolidation. Science 2000, 287:5451-5455.
46. McGaugh J.L. Memory consolidation and the amygdala: A systems perspective. Trends in Neurosciences 2002, 25:456-462.
47. McGaugh J.L., Cahill L., Roozendaal B. Involvement of the amygdala in memory storage: Interaction with other brain systems. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:13508-13514.
48. McGaugh J.L., Izquierdo I. The contribution of pharmacology to research on the mechanisms of memory formation. Trends in Pharmacological Sciences 2000, 21:208-210.
49. McGaugh J.L., Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion in Neurobiology 2002, 12:205-210.
50. McGaugh J., Roozendaal B. Drug enhancement of memory consolidation: Historical perspective and neurobiological implications. Psychopharmacology 2009, 202:3-14.
51. Mello e Souza T., Vianna M.R.M., Rodrigues C., Quevedo J., Moleta B.A., Izquierdo I. Involvement of the medial precentral prefrontal cortex in memory consolidation for inhibitory avoidance learning in rats. Pharmacology, Biochemistry, and Behavior 2000, 66:615-622.
52. Mogenson G.J., Jones D.L., Yim C.Y. From motivation to action: Functional interface between the limbic system and the motor system. Progress in Neurobiology 1980, 14:69-97.
53. O'Donnell P., Grace A.A. Synaptic interactions among excitatory afferents to nucleus accumbens neurons: Hippocampal gating of prefrontal cortical input. The Journal of Neuroscience 1995, 15:3622-3639.
54. Overmier J.B., Seligman M.E.P. Effects of inescapable shock upon subsequent escape and avoidance responding. Journal of Comparative and Physiological Psychology 1967, 63:28-33.
55. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, Orlando.
56. Pitkanen A., Pikkarainen M., Nurminen N., Ylinen A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. Annals New York Academy of Sciences 2000, 369-391.
57. Robbins T.W., Everitt B.J. Neurobehavioural mechanisms of reward and motivation. Current Opinion in Neurobiology 1996, 6:228-236.
58. Roozendaal B., de-Quervain D.J.F., Ferry B., Setlow B., McGaugh J.L. Basolateral amygdala-nucleus accumbens interactions in mediating glucocorticoid enhancement of memory consolidation. The Journal of Neuroscience 2001, 21:2518-2525.
59. Roozendaal B., McReynolds J.R., Van der Zee E.A., Lee S., McGaugh J.L., McIntyre C.K. Glucocorticoid effects on memory consolidation depend on functional interactions between the medial prefrontal cortex and basolateral amygdala. The Journal of Neuroscience 2009, 29:14299-14308.
60. Roozendaal B., Nguyen B.T., Power A.E., McGaugh J.L. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proceedings of the National Academy of Sciences of the Unites States of America 1999, 96:11642-11647.
61. Salamone J.D. The involvement of nucleus accumbens dopamine in appetitive and aversive motivation. Behavioural Brain Research 1994, 61:117-133.
62. Sandkuhler J., Maisch B., Zimmermann M. The use of local anaesthetic microinjections to identify central pathways: A quantitative evaluation of the time course and extent of the neuronal block. Experimental Brain Research 1987, 68:168-178.
63. Schwabe L., Wolf O.T., Oitzl M.S. Memory formation under stress: Quantity and quality. Neuroscience and Biobehavioral Reviews 2010, 34:584-591.
64. Setlow B. The nucleus accumbens and learning and memory. Journal of Neuroscience Research 1997, 49:515-521.
65. Swanson L.W. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Research 1981, 217:150-154.
66. Thierry A.M., Gioanni Y., Degenetais E., Glowinski J. Hippocampo-prefrontal cortex pathway: Anatomical and electrophysiological characteristics. Hippocampus 2000, 10:411-419.
67. Thomas K.L., Hall J., Everitt B.J. Cellular imaging with zif268 expression in the rat nucleus accumbens and frontal cortex further dissociates the neural pathways activated following the retrieval of contextual and cued fear memory. European Journal of Neuroscience 2002, 16:1789-1796.
68. Tinsley M.R., Quinn J.J., Fanselow M.S. The role of muscarinic and nicotinic cholinergic neurotransmission in aversive conditioning: Comparing Pavlovian fear conditioning and inhibitory avoidance. Learning & Memory 2004, 11:35-42.
69. Varela J.A., Wang J., Christianson J.P., Maier S.F., Cooper D.C. Control over stress, but not stress per se increases prefrontal cortical pyramidal neuron excitability. The Journal of Neuroscience 2012, 32:12848-12853.
70. Wellman C.L., Izquierdo A., Garrett J.E., Martin K.P., Carroll J., Millstein R., et al. Impaired stress-coping and fear extinction and abnormal corticolimibic morphology in serotonin transporter knock-out mice. The Journal of Neuroscience 2007, 27:684-691.
71. Wilensky A.E., Schafe G.E., LeDoux J.E. The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning. The Journal of Neuroscience 2000, 20:7059-7066.
72. Wise R.A. Drug-activation of brain reward pathways. Drug and Alcohol Dependence 1998, 51:13-22.
73. Witter M.P. Organization of cortico-hippocampal networks in rats related to learning and memory. International Congress Series 2003, 1250:131-145.