Evolution of cerebral cortex involvement in the acquisition of associative learning

Behavioral Neuroscience

Volumn 120, Issue 5, 2006, Pages 1043-1056

  Jiménez Díaz, Lydia ^a   Sancho Bielsa, Francisco ^b   Gruart, Agnès ^c   López García, Carlos ^d   García Delgado, José M ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^c UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Associative learning; c Fos; Cerebral cortex; Limbic system; Somatosensorial cortex

Indexed keywords

PROTEIN C FOS;

ANIMAL BEHAVIOR; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN REGION; CONDITIONING; ENTORHINAL CORTEX; IMMUNOHISTOCHEMISTRY; NONHUMAN; OCCIPITAL CORTEX; PARIETAL LOBE; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PYRIFORM CORTEX; RABBIT; SOMATOSENSORY CORTEX; STATE DEPENDENT LEARNING; SUBICULUM; TISSUE DISTRIBUTION;

ANIMALS; ASSOCIATION LEARNING; BLINKING; BRAIN MAPPING; CEREBRAL CORTEX; CONDITIONING, CLASSICAL; DOMINANCE, CEREBRAL; ENTORHINAL CORTEX; FEMALE; HIPPOCAMPUS; MALE; MENTAL RECALL; OCCIPITAL LOBE; PARAHIPPOCAMPAL GYRUS; PARIETAL LOBE; PROTO-ONCOGENE PROTEINS C-FOS; RABBITS; SOMATOSENSORY CORTEX;

EID: 33750081440     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.120.5.1043     Document Type: Article

References (66)

1. Allen, M. T., Chelius, L., & Gluck, M. A. (2002). Selective entorhinal and nonselective cortical-hippocampal region lesions, but not selective hippocampal lesions, disrupt learned irrelevance in rabbit eyeblink conditioning. Cognitive and Affective Behavioral Neuroscience, 2, 214-226.
2. Allen, M. T., Chelius, L., Masand, V., Gluck, M. A., Myers, C. E., & Schnirman, G. A. (2002). A comparison of latent inhibition and learned irrelevance pre-exposure effects in rabbit and human eyeblink conditioning. Integrative Physiological and Behavioral Science, 37, 188-214.
3. Amir, S., & Stewart, J. (1999). Conditioned and unconditioned aversive stimuli enhance light-induced fos expression in the primary visual cortex. Neuroscience, 89, 323-327.
4. Anton, F., Herdegen, T., Peppel, P., & Leh, J. D. (1991). C-fos-like immunoreactivity in rat brainstem neurons following noxious chemical stimulation of the nasal mucosa. Neuroscience, 41, 629-641.
5. Aou, S., Woody, C. D., & Birt, D. (1992). Changes in the activity of units of the cat motor cortex with rapid conditioning and extinction of a compound eye blink movement. Journal of Neuroscience, 12, 549-559.
6. Asanuma, H., & Pavlides, C. (1997). Neurobiological basis of motor learning in mammals. NeuroReport, 8, i-vi.
7. Beck, C. H., & Fibiger, H. C. (1995). Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: With and without diazepam pretreatment. Journal of Neuroscience, 15, 709-720.
8. Beggs, J. M., Moyer, J. R., McGann, J. P., & Brown, T. H. (2000). Prolonged synaptic integration in perirhinal cortical neurons. Journal of Neurophysiology, 32, 94-98.
9. Bertaina-Anglade, V., Tramu, G., & Destrade, C. (2000). 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. European Journal of Neuroscience, 12, 3803-3812.
10. Blaxton, T. A., Zeffiro, T. A., Gabrieli, J. D., Bookheimer, S. Y., Carrillo, M. C., Theodore, W. H., & Disterhoft, J. F. (1996). Functional mapping of human learning: A positron emission tomography activation study of eyeblink conditioning. Journal of Neuroscience, 16, 4032-4040.
11. Bonardi, C., Hall, G., & Ong, S. Y. (2005). Analysis of the learned irrelevance effect in appetitive Pavlovian conditioning. Quarterly Journal of Experimental Psychology: B. Comparative and Physiological Psychology, 58, 141-162.
12. Brown, M. W., & Aggleton, J. P. (2001). Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nature Reviews Neuroscience, 2, 51-61.
13. Burwell, R. D. (2000). The parahippocampal region: Corticocortical connectivity. Annals of the New York Academy of Sciences, 911, 25-42.
14. Burwell, R. D., Bucci, D. J., Sanborn, M. R., & Jutras, M. J. (2004). Perirhinal and postrhinal contributions to remote memory for context. Journal of Neuroscience, 24, 11023-11028.
15. Carrive, P., Kehoe, E. J., Macrae, M., & Paxinos, G. (1997). Fos-like immunoreactivity in locus coeruleus after classical conditioning of the rabbit's nictitating membrane response. Neuroscience Letters, 223, 33-36.
16. Chowdhury, G. M., Fujioka, T., & Nakamura, S. (2000). Induction and adaptation of Fos expression in the rat brain by two types of acute restraint stress. Brain Research Bulletin, 52, 171-182.
17. Coutureau, E., Galani, R., Gosselin, O., Majchrzak, M., & Di Scala, G. (1999). Entorhinal but not hippocampal or subicular lesions disrupt latent inhibition in rats. Neurobiology of Learning and Memory, 72, 143-157.
18. Datiche, F., Roullet, F., & Cattarelli, M. (2001). Expression of Fos in the piriform cortex after acquisition of olfactory learning: An immunohistochemical study in the rat. Brain Research Bulletin, 55, 95-99.
19. Delgado-García, J. M., & Gruart, A. (2002). The role of interpositus nucleus in eyelid conditioned responses. Cerebellum, 1, 289-308.
20. Domínguez-del-Toro, E., Rodríguez-Moreno, A., Porras-García, E., Sánchez-Campusano, R., Blanchard, V., Laville, M., Bohme, G. A., Benavides, J., & Delgado-García, J. M. (2004). An in vitro and in vivo study of early deficits in associative learning in transgenic mice that over-express a mutant form of human APP associated with Alzheimer's disease. European Journal of Neuroscience, 20, 1945-1952.
21. Fleischhauer, K., Zilles, K., & Schleidher, A. (1980). A revised cytoarchitectonic map of the neocortex of the rabbit (Oryctolagus cuniculus). Anatomy and Embryology, 161, 121-143.
22. Fontán-Lozano, A., Troncoso, J., Múnera, A., Carrión, A. M., & Delgado-García, J. M. (2005). Cholinergic septo-hippocampal innervation is required for trace eyeblink classical conditioning. Learning and Memory, 12, 557-563.
23. Gormezano, I., Keohe, E. J., & Marshall-Goodell, B. S. (1983). Twenty years of classical conditioning research with the rabbit. Progress in Psychobiology and Physiology, 10, 197-275.
24. Gruart, A., Blázquez, P., & Delgado-García, J. M. (1995). Kinematics of spontaneous, reflex, and conditioned eyelid movements in the alert cat. Journal of Neurophysiology, 74, 226-248.
25. Gruart, A., Guillazo-Blanch, G., Fernández-Mas, R., Jiménez-Díaz, L., & Delgado-García, J. M. (2000). Cerebellar posterior interpositus nucleus as an enhancer of classically conditioned eyelid responses in alert cats. Journal of Neurophysiology, 84, 2680-2690.
26. Gruart, A., Morcuende, S., Martínez, S., & Delgado-García, J. M. (2000). Involvement of cerebral cortical structures in the classical conditioning of eyelid responses in rabbits. Neuroscience, 4, 719-730.
27. Gruart, A., Muñoz, M. D., & Delgado-García, J. M. (2005). Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. Journal of Neuroscience, 26, 1077-1087.
28. Gruart, A., Schreurs, B. G., Domínguez-del-Toro, E., & Delgado-García, J. M. (2000). Kinetic and frequency-domain properties of reflex and conditioned eyelid responses in the rabbit. Journal of Neurophysiology, 83, 836-852.
29. Herdegen, T., & Leah, J. D. (1998). Inducible and constitutive transcription factors in the mammalian nervous system: Control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Research Reviews, 28, 370-490.
30. Inda, M. C., Delgado-García, J. M., & Carrión, A. M. (2005). Acquisition, consolidation, reconsolidation, and extinction of eyelid conditioning responses require de novo protein synthesis. Journal of Neuroscience, 25, 2070-2080.
31. Irwin, K. B., Craig, A. D., Bracha, V., & Bloedel, J. R. (1992). Distribution of c-fos expression in brainstem neurons associated with conditioning and pseudo-conditioning of the rabbit nictitating membrane reflex. Neuroscience Letters, 148, 71-75.
32. Jiménez-Díaz, L., de Navarro-López, J., D., Gruart, A., & Delgado-García, J. M. (2004). Role of cerebellar interpositus nucleus in the genesis and control of reflex and conditioned eyelid responses. Journal of Neuroscience, 24, 9138-9145.
33. Johnson, D. M., Illig, K. R., Bahan, M., & Haberly, L. B. (2000). New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that "primary" olfactory cortex functions like "association" cortex in other sensory systems. Journal of Neuroscience, 20, 6974-6982.
34. Johnston, D., & Amaral, D. G. (2004). Hippocampus. In G. M. Shepherd (Ed.), The synaptic organization of the brain (pp. 455-498). Oxford, United Kingdom: Oxford University Press.
35. Kim, J. J., Clark, R. E., & Thompson, R. F. (1995). Hippocampectomy impairs the memory of recently but not remotely, acquired trace eyeblink conditioned responses. Behavioral Neuroscience, 109, 195-203.
36. Kleim, J. A., Lussnig, E., Schwarz, E. R., Comery, T. A., & Greenough, W. T. (1996). Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. Journal of Neuroscience, 16, 4529-4535.
37. Krupa, D. J., Thompson, J. K., & Thompson, R. F. (1993). Localization of a memory trace in the mammalian brain. Science, 260, 989-991.
38. Leal-Campanario, R., Barradas-Bribiescas, J. A., Delgado-García, J. M., & Gruart, A. (2004). Relative contributions of eyelid and eye-retraction motor systems to reflex and classically conditioned blink responses in the rabbit. Journal of Applied Physiology, 96, 1541-1554.
39. Logan, C. G., & Grafton, S. T. (1995). Functional anatomy of human eyeblink conditioning determined with regional cerebral glucose metabolism and positron-emission tomography. Proceedings of the National Academy of Sciences USA, 92, 7500-7504.
40. Martina, M., Royer, S., & Pare, D. (2001). Propagation of neocortical inputs in the perirhinal cortex. Journal of Neuroscience, 21, 2878-2888.
41. Martínez, S., & Belmonte, C. (1996). c-Fos expression in trigeminal nucleus neurons after chemical irritation of the cornea: Reduction by selective blockage of nociceptor chemosensitivity. Experimental Brain Research, 109, 56-62.
42. McEchron, M. D., & Disterhoft, J. F. (1997). Sequence of single neuron changes in CA1 hippocampus of rabbits during acquisition of trace eyeblink conditioned responses. Journal of Neurophysiology, 78, 1030-1044.
43. Mileusnic, R., Anokhin, K., & Rose, S. P. (1996). Antisense oligodeoxynucleotides to c-fos are amnestic for passive avoidance in the chick. NeuroReport, 7, 1269-1272.
44. Molchan, S. E., Sunderland, T., McIntosh, A. R., Herscovitch, P., & Schreurs, B. G. (1994). A functional anatomical study of associative learning in humans. Proceedings of the National Academy of Sciences USA, 91, 8122-8126.
45. Múnera, A., Gruart, A., Muñoz, M. D., Fernández-Mas, R., & Delgado-García, J. M. (2001). Hippocampal pyramidal cell activity encodes conditioned stimulus predictive value during classical conditioning in alert cats. Journal of Neurophysiology, 86, 2571-2582.
46. Naber, P. A., Witter, M. P., & Lopes da Silva, F. H. (2000). Networks of the hippocampal memory system of the rat: The pivotal role of the subiculum. Annals of the New York Academy of Sciences, 911, 392-403.
47. Nordquist, R. E., Pennartz, C. M., Uylings, H. B., Joosten, R. N., Jonker, A. J., Groenewegen, H. J., & Voorn, P. (2003). C-fos activation patterns in rat prefrontal cortex during acquisition of a cued classical conditioning task. Behavioural Brain Research, 146, 65-75.
48. O'Mara, S. M., Commins, S., Anderson, M., & Gigg, J. (2001). The subiculum: A review of form, physiology and function. Progress in Neurobiology, 64, 129-155.
49. Porras-García, E., Cendelin, J., Domínguez-del-Toro, E., Vozeh, F., & Delgado-García, J. M. (2005). Purkinje cell loss affects differentially the execution, acquisition and prepulse inhibition of skeletal and facial motor responses in Lurcher mice. European Journal of Neuroscience, 21, 979-988.
50. Radulovic, J., Kammermeier, J., & Spiess, J. (1998). Relationship between Fos production and classical fear conditioning: Effects of novelty, latent inhibition, and unconditioned stimulus preexposure. Journal of Neuroscience, 18, 7452-7461.
51. Rammani, N., Toni, I., Josephs, O., Ashburner, J., & Passingham, R. E. (2000). Learning- and expectation-related changes in the human brain during motor learning. Journal of Neurophysiology, 84, 3026-3035.
52. Ruigrok, T. J. H., van der Burg, H., & Sabel-Goedknegt, E. (1996). Locomotion coincides with c-Fos expression in related areas of inferior olive and cerebellar nuclei in the rat. Neuroscience Letters, 214, 119-122.
53. Ryou, J. W., Cho, S. Y., & Kim, H. T. (2001). Lesions of the entorhinal cortex impair acquisition of hippocampal-dependent trace conditioning. Neurobiology of Learning and Memory, 75, 121-127.
54. Sacchetti, B., Baldi, E., Lorenzini, C. A., & Bucherelli, C. (2002). Differential contribution of some cortical sites to the formation of memory traces supporting fear conditioning. Experimental Brain Research, 146, 223-232.
55. Schreurs, B., & Alkon, D. L. (1990). US-US conditioning of the rabbit's nictitating membrane response: Emergence of a conditioned response without alpha conditioning. Psychobiology, 18, 312-320.
56. Schreurs, B., & Alkon, D. L. (2001). Imaging learning and memory: Classical conditioning. Anatomical Record (The New Anatomist), 265, 257-273.
57. Schreurs, B. G., McIntosh, A. R., Bahro, M., Herscovitch, P., Sunderland, T., & Molchan, S. E. (1997). Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eye-blink response. Journal of Neurophysiology, 77, 2153-2163.
58. Shohamy, D., Allen, M. T., & Gluck, M. A. (2000). Dissociating entorhinal and hippocampal involvement in latent inhibition. Behavioral Neuroscience, 114, 867-874.
59. Suzuki, W. A. (1996). The anatomy, physiology and functions of the perirhinal cortex. Current Opinion in Neurobiology, 6, 179-186.
60. Swank, M. W., Ellis, A. E., & Cochran, B. N. (1996). c-Fos antisense blocks acquisition and extinction of conditioned taste aversion in mice. NeuroReport, 7, 1866-1870.
61. Warburton, E. C., Koder, T., Cho, K., Massey, P. V., Duguid, G., Barker, G. R., Aggleton, J. P., Bashir, Z. I., & Brown, M. W. (2003). Cholinergic neurotransmission is essential for perirhinal cortical plasticity and recognition memory. Neuron, 38, 987-996.
62. Wikgren, J., Ruusuvirta, T., & Korhonen, T. (2003). Activity in the rabbit somatosensory cortex reflects the active procedural memory trace of a classically conditioned eyeblink response. Neuroscience Letters, 341, 119-122.
63. Wilson, D. A., & Stevenson, R. J. (2003). The fundamental role of memory in olfactory perception. Trends in Neurosciences, 26, 243-247.
64. Winkler, C., & Potter, A. (1911). An anatomical guide to experimental researches on the rabbit's brain. Amsterdam: Verluys.
65. Winters, B. D., & Bussey, T. J. (2005). Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. Journal of Neuroscience, 25, 52-61.
66. Yeo, C. H., Hardiman, M. J., & Glickstein, M. (1985). Classical conditioning of the nictitating membrane response of the rabbit: I. Lesions of the cerebellar nuclei. Experimental Brain Research, 60, 87-98.