C-fos activation patterns in rat prefrontal cortex during acquisition of a cued classical conditioning task

Behavioural Brain Research

Volumn 146, Issue 1-2, 2003, Pages 65-75

  Nordquist, R E ^a,b   Pennartz, C M A ^b   Uylings, H B M ^a,b   Joosten, R N J M A ^b   Jonker, A J ^a   Groenewegen, H J ^a   Voorn, P ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Appetitive classical conditioning; Associative learning; C fos; Immediate early gene; Immunocytochemistry; Regions of prefrontal cortex

Indexed keywords

PROTEIN C FOS;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BRAIN DEPTH STIMULATION; CELL NUCLEUS; CONDITIONING; CONTROLLED STUDY; FOOD; IMMUNOREACTIVITY; LIGHT; MALE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STATISTICAL SIGNIFICANCE; TASK PERFORMANCE;

EID: 0345688601     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2003.09.014     Document Type: Article

References (74)

1. Baldwin A.E., Holahan M.R., Sadeghian K., Kelley A.E. N-Methyl-D-aspartate receptor-dependent plasticity within a distributed corticostriatal network mediates appetitive instrumental learning. Behav. Neurosci. 114:2000;84-98.
2. Baldwin A.E., Sadeghian K., Kelley A.E. Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex. J. Neurosci. 22:2002;1063-1071.
3. Balsam P.D., Gibbon J. Formation of tone-US associations does not interfere with the formation of context-US associations in pigeons. J. Exp. Psychol. Anim. Behav. Process. 14:1988;401-412.
4. Barbas H., Pandya D.N. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 286:1989;353-375.
5. Berendse H.W., Galis-de Graaf Y., Groenewegen H.J. Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. Comp. Neurol. 316:1992;314-347.
6. Bertaina-Anglade V., Tramu G., Destrade C. Differential learning-stage dependent patterns of c-fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice. Eur. J. Neurosci. 12:2000;3803-3812.
7. Brown E.E., Robertson G.S., Fibiger H.C. Evidence for conditional neuronal activation following exposure to a cocaine-paired environment: role of forebrain limbic structures. J. Neurosci. 12:1992;4112-4121.
8. Bussey T.J., Everitt B.J., Robbins T.W. Dissociable effects of cingulate and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat: implications for the neurobiology of emotion. Behav. Neurosci. 111:1997;908-919.
9. Cahill L., Weinberger N.M., Roozendaal B., McGaugh J.L. Is the amygdala a locus of "conditioned fear"? Some questions and caveats. Neuron. 23:1999;227-228.
10. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26:2002;321-352.
11. Corcoran K.A., Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J. Neurosci. 21:2001;1720-1726.
12. Cousens G., Otto T. Both pre- and posttraining excitotoxic lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning. Behav. Neurosci. 112:1998;1092-1103.
13. De Bruin J.P., Feenstra M.G., Broersen L.M., Van Leeuwen M., Arens C., De Vries S.et al. Role of the prefrontal cortex of the rat in learning and decision making: effects of transient inactivation. Prog. Brain Res. 126:2000;103-113.
14. Delatour B., Witter M.P. Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways. Eur. J. Neurosci. 15:2002;1400-1407.
15. Feenstra M.G., Vogel M., Botterblom M.H., Joosten R.N., de Bruin J.P. Dopamine and noradrenaline efflux in the rat prefrontal cortex after classical aversive conditioning to an auditory cue. Eur. J. Neurosci. 13:2001;1051-1054.
16. Ferry A.T., Ongur D., An X., Price J.L. Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J. Comp. Neurol. 425:2000;447-470.
17. 2+, cAMP-responsive element binding proteins, and mitogen-activated protein kinase signaling. J. Neurosci. 17:1997;7252-7266.
18. Floyd N.S., Price J.L., Ferry A.T., Keay K.A., Bandler R. Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J. Comp. Neurol. 422:2000;556-578.
19. Goldman-Rakic P.S. Cellular basis of working memory. Neuron. 14:1995;477-485.
20. Granon S., Vidal C., Thinus-Blanc C., Changeux J.P., Poucet B. Working memory, response selection, and effortful processing in rats with medial prefrontal lesions. Behav. Neurosci. 108:1994;883-891.
21. Groenewegen H.J., Uylings H.B. The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog. Brain Res. 126:2000;3-28.
22. Hall J., Thomas K.L., Everitt B.J. Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J. Neurosci. 21:2001;2186-2193.
23. Holland P.C., Bouton M.E. Hippocampus and context in classical conditioning. Curr. Opin. Neurobiol. 9:1999;195-202.
24. Izaki Y., Hori K., Nomura M. Dopamine and acetylcholine elevation on lever-press acquisition in rat prefrontal cortex. Neurosci. Lett. 258:1998;33-36.
25. Jay T.M., Glowinski J., Thierry A.M. Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res. 505:1989;337-340.
26. Lacroix L., Spinelli S., Heidbreder C.A., Feldon J. Differential role of the medial and lateral prefrontal cortices in fear and anxiety. Behav. Neurosci. 114:2000;1119-1130.
27. Maren S., Aharonov G., Fanselow M.S. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res. 88:1997;261-274.
28. Maren S., Aharonov G., Fanselow M.S. Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: absence of a temporal gradient. Behav. Neurosci. 110:1996;718-726.
29. McDonald A.J. Organization of amygdaloid projections to the mediodorsal thalamus and prefrontal cortex: a fluorescence retrograde transport study in the rat. J. Comp. Neurol. 262:1987;46-58.
30. McDonald A.J. Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience. 44:1991;1-14.
31. McLaughlin J., Powell D.A. Pavlovian heart rate and jaw movement conditioning in the rabbit: effects of medial prefrontal lesions. Neurobiol. Learn. Mem. 71:1999;150-166.
32. Melia K.R., Ryabinin A.E., Schroeder R., Bloom F.E., Wilson M.C. Induction and habituation of immediate-early gene expression in rat brain by acute and repeated restraint stress. J. Neurosci. 14:1994;5929-5938.
33. Miller E.K. The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1:2000;59-65.
34. Miller E.K. The prefrontal cortex: complex neural properties for complex behavior. Neuron. 22:1999;15-17.
35. Morgan M.A., LeDoux J.E. Contribution of ventrolateral prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Neurobiol. Learn Mem. 72:1999;244-251.
36. Morgan M.A., LeDoux J.E. Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav. Neurosci. 109:1995;681-688.
37. Morgan M.A., Romanski L.M., LeDoux J.E. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci. Lett. 163:1993;109-113.
38. Morrow B.A., Elsworth J.D., Rasmusson A.M., Roth R.H. The role of mesoprefrontal dopamine neurons in the acquisition and expression of conditioned fear in the rat. Neuroscience. 92:1999;553-564.
39. Muir J.L., Everitt B.J., Robbins T.W. The cerebral cortex of the rat and visual attentional function: dissociable effects of mediofrontal, cingulate, anterior dorsolateral, and parietal cortex lesions on a five-choice serial reaction time task. Cereb Cortex. 6:1996;470-481.
40. Mulder A.B., Nordquist R., Orgut O., Pennartz C.M. Plasticity of neuronal firing in deep layers of the medial prefrontal cortex in rats engaged in operant conditioning. Prog. Brain Res. 126:2000;287-301.
41. Neisewander J.L., Baker D.A., Fuchs R.A., Tran-Nguyen L.T., Palmer A., Marshall J.F. Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J. Neurosci. 20:2000;798-805.
42. Ono T., Nishino H., Fukuda M., Sasaki K., Nishijo H. Single neuron activity in dorsolateral prefrontal cortex of monkey during operant behavior sustained by food reward. Brain Res. 311:1984;323-332.
43. Parkinson J.A., Willoughby P.J., Robbins T.W., Everitt B.J. Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems. Behav. Neurosci. 114:2000;42-63.
44. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. London: Academic Press; 1986. p. 319.
45. Petrovich G.D., Gallagher M. Amygdala subsystems and control of feeding behavior by learned cues. Ann. N.Y. Acad. Sci. 985:2003;251-262.
46. Phillips G.D., Setzu E., Vugler A., Hitchcott P.K. Immunohistochemical assessment of mesotelencephalic dopamine activity during the acquisition and expression of Pavlovian versus instrumental behaviours. Neuroscience. 117:2003;755-767.
47. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106:1992;274-285.
48. Phillips R.G., LeDoux J.E. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn. Mem. 1:1994;34-44.
49. Radulovic J., Kammermeier J., Spiess J. Relationship between fos production and classical fear conditioning: effects of novelty, latent inhibition, and unconditioned stimulus preexposure. J. Neurosci. 18:1998;7452-7461.
50. Reep R.L., Winans S.S. Afferent connections of dorsal and ventral agranular insular cortex in the hamster Mesocricetus auratus. Neuroscience. 7:1982;1265-1288.
51. Rescorla R.A. Associative changes with a random CS-US relationship. Q. J. Exp. Psychol. B. 53:2000;325-340.
52. Rolls E.T., Critchley H.D., Browning A.S., Hernadi I., Lenard L. Responses to the sensory properties of fat of neurons in the primate orbitofrontal cortex. J. Neurosci. 19:1999;1532-1540.
53. Schultz W. Multiple reward signals in the brain. Nat. Rev. Neurosci. 1:2000;199-207.
54. Selden N.R., Everitt B.J., Jarrard L.E., Robbins T.W. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience. 42:1991;335-350.
55. Sesack S.R., Deutch A.Y., Roth R.H., Bunney B.S. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 290:1989;213-242.
56. Sgambato V., Pages C., Rogard M., Besson M.J., Caboche J. Extracellular signal-regulated kinase (ERK) controls immediate-early gene induction on corticostriatal stimulation. J. Neurosci. 18:1998;8814-8825.
57. Sheafor P.J. "Pseudoconditioned" jaw movements of the rabbit reflect associations conditioned to contextual background cues. J. Exp. Psychol. Anim. Behav. Process. 1:1975;245-260.
58. Sheng M., Greenberg M.E. The regulation and function of c-fos and other immediate-early genes in the nervous system. Neuron. 4:1990;477-485.
59. Sotty F., Sandner G., Gosselin O. Latent inhibition in conditioned emotional response: c-fos immunolabelling evidence for brain areas involved in the rat. Brain Res. 737:1996;243-254.
60. Tanji J., Hoshi E. Behavioral planning in the prefrontal cortex. Curr. Opin. Neurobiol. 11:2001;164-170.
61. 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. Eur. J. Neurosci. 16:2002;1789-1796.
62. Tronel S., Sara S.J. Mapping of olfactory memory circuits: region-specific c-fos activation after odor-reward associative learning or after its retrieval. Learn. Mem. 9:2002;105-111.
63. Turgeon S.M., Reichstein D.A. Decreased striatal c-fos accompanies latent inhibition in a conditioned taste aversion paradigm. Brain Res. 924:2002;120-123.
64. Tzschentke T.M., Schmidt W.J. Functional heterogeneity of the rat medial prefrontal cortex: effects of discrete subarea-specific lesions on drug-induced conditioned place preference and behavioural sensitization. Eur. J. Neurosci. 11:1999;4099-4109.
65. Uylings H.B., van Eden C.G. Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog. Brain Res. 85:1990;31-62.
66. Van Eden C.G., Buijs R.M. Functional neuroanatomy of the prefrontal cortex: autonomic interactions. Prog. Brain Res. 126:2000;49-62.
67. Van Eden C.G., Hoorneman E.M., Buijs R.M., Matthijssen M.A., Geffard M., Uylings H.B. Immunocytochemical localization of dopamine in the prefrontal cortex of the rat at the light and electron microscopical level. Neuroscience. 22:1987;849-862.
68. Van Eden C.G., Uylings H.B. Cytoarchitectonic development of the prefrontal cortex in the rat. J. Comp. Neurol. 241:1985;253-267.
69. Vazdarjanova A., McGaugh J.L. Basolateral amygdala is involved in modulating consolidation of memory for classical fear conditioning. J. Neurosci. 19:1999;6615-6622.
70. Verwer R.W., Van Vulpen E.H., Van Uum J.F. Postnatal development of amygdaloid projections to the prefrontal cortex in the rat studied with retrograde and anterograde tracers. J. Comp. Neurol. 376:1996;75-96.
71. Watanabe M. Prefrontal unit activity during associative learning in the monkey. Exp. Brain Res. 80:1990;296-309.
72. Watanabe M. Reward expectancy in primate prefrontal neurons. Nature. 382:1996;629-632.
73. Wilkinson L.S., Humby T., Killcross A.S., Torres E.M., Everitt B.J., Robbins T.W. Dissociations in dopamine release in medial prefrontal cortex and ventral striatum during the acquisition and extinction of classical aversive conditioning in the rat. Eur. J. Neurosci. 10:1998;1019-1026.
74. Yokoyama C., Sasaki K. Regional expressions of Fos-like immunoreactivity in rat cerebral cortex after stress; restraint and intraperitoneal lipopolysaccharide. Brain Res. 816:1999;267-275.