Limbic thalamic, cingulate cortical and hippocampal neuronal correlates of discriminative approach learning in rabbits

Behavioural Brain Research

Volumn 80, Issue 1-2, 1996, Pages 123-136

  Freeman Jr , John H ^a   Cuppernell, Cyndi ^a   Flannery, Karen ^a   Gabriel, Michael ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

cingulate cortex; discrimination; hippocampus; learning; limbic thalamus; rabbit; training induced neuronal activity

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CINGULATE GYRUS; CONTROLLED STUDY; DISCRIMINATION LEARNING; MALE; NONHUMAN; PRIORITY JOURNAL; RABBIT; THALAMUS;

EID: 0030272180     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/0166-4328(96)00027-7     Document Type: Article

References (62)

1. [1] Alvarez, P., Zola-Morgan, S. and Squire, L.R., The animal model of human amnesia: long-term memory impaired and short-term memory intact, PN AS, (1994) 5637-5641.
2. [2] Berger, T.W., Rinaldi, P.C., Weisz, D.J. and Thompson, R.F., Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response, J. Neurophysiol., 50 (1983) 1197-1219.
3. [3] Berry, S.D., Weisz, D.J. and Mamounas, L.A., Neural correlates of acquisition rate. In I. Gormezano, W.F. Prokasy and R.F. Thompson (Eds.), Classical Conditioning, 3rd ed., Erlbaum, New Jersey, 1987, pp. 255-274.
4. [4] Berthier, N.E. and Moore, J.W., Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response, Exp. Brain Res., 63 (1986) 341-350.
5. [5] Berthier, N.E. and Moore, J.W., Activity of deep cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits, Exp. Brain Res., 83 (1990) 44-54.
6. [6] Buchwald, J., Holstein, S.B. and Weber, D.S., Multiple unit recording: technique, interpretation, and experimental applications. In R.F. Thompson and M.M. Patterson (Eds.), Bioelectric Recording Techniques, Part A. Cellular Processes and Brain Potentials, Academic Press, New York, 1973, pp. 202-242.
7. [7] Davis, M., Analysis of aversive memories using the fear-potentiated startle paradigm. In L.R. Squire and N. Butters (Eds.), Neuropsychology of Memory, 2nd ed., Guilford Press, New York, 1992, pp. 470-484.
8. [8] Deadwyler, S.A., Bunn, T. and Hampson, R.E., Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats, J. Neurosci., 16 (1996) 354-372.
9. [9] Deadwyler, S.A. and Hampson, R.E., Ensemble activity and behavior: what's the code? Science, 270 (1995) 1316-1318.
10. [10] Desmond, J.E. and Moore, J.W., A brainstem region essential for the classically conditioned but not unconditioned nictitating membrane response, Physiol. Behav., 28 (1982) 1029-1033.
11. [11] Desmond, J.E. and Moore, J.W., Single-unit activity in red nucleus during the classically conditioned rabbit nictitating membrane response, Neurosci. Res., 10 (1991) 260-279.
12. [12] Desmond, J.E. and Moore, J.W., Dorsolateral pontine tegmentum and the classically conditioned nictitating membrane response: analysis of CR-related single-unit activity, Exp. Brain Res., 65 (1986) 59-74.
13. [13] Disterhoft, J.F., Coulter, D.A. and Alkon, D.L., AHP Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro, PN AS, 83 (1986) 2733-2737.
14. [14] Donovick, P.J., A metachromatic stain for neural tissue, Stain Technol., 49 (1974) 49-51.
15. [15] Eichenbaum, H., The hippocampal system and declarative memory in animals, J. Cogn. Neurosci., 4 (1992) 217-231.
16. [16] Eichenbaum, H., Otto, T. and Cohen, N.J., Two functional components of the hippocampal memory system, Behav. Brain Sci., 17 (1994) 449-517.
17. [17] Fox, C.A. and Eichman, J., A rapid method for locating intracerebral electrode tracks, Stain Technol., 34 (1959) 39-42.
18. [18] Freeman, J.H., Jr., Cuppernell, C., Flannery, K. and Gabriel, M., Context-specific multi-site cingulate cortical, limbic thalamic and hippocampal neuronal activity during concurrent discriminative approach and avoidance training in rabbits, J. Neurosci., 15 (1996) 1538-1549.
19. [19] Gabriel, M., Discriminative avoidance learning: a model system. In B.A. Vogt and M. Gabriel (Eds.), Neurobiology of Cingulate Cortex and Limbic Thalamus: A Comprehensive Handbook, Birkhauser, Boston, 1993, pp. 478-523.
20. [20] Gabriel, M., Kubota, Y., Sparenborg, S., Straube, K. and Vogt, B.A., Effects of cingulate cortical lesions on avoidance learning and training-induced unit activity in rabbits, Exp Brain Res., 86 (1991) 585-600.
21. [21] Gabriel, M., Lambert, R.W., Foster, K., Orona, E., Sparenborg, S. and Maiorca, R.R, Anterior thalamic lesions and neuronal activity in the cingulate and retrosplenial cortices during discriminative avoidance behavior in rabbits, Behav. Neurosci., 97 (1983) 675-696.
22. [22] Gabriel, M. and Moore, J. (Eds.), Learning and Computational Neuroscience: Foundations of Adaptive Networks, MIT Press, Massachusetts, 1990.
23. [23] Gabriel, M., Vogt, V.A., Kubota, Y., Poremba, A. and Kang, E., Training-stage related neuronal plasticity in limbic thalamus and cingulate cortex during learning - a possible key to mnemonic retrieval, Behav. Brain Res., 46 (1991) 175-185.
24. [24] Gallagher, M., Graham, P.W. and Holland, P.C., The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior, J. Neurosci., 10 (1990) 1906-1911.
25. [25] Girgis, M. and Shih-Chang, W., A New Stereotaxic Atlas of the Rabbit Brain, Warren H. Green, St. Louis, MO, 1981.
26. [26] Gormezano, I., Prokasy, W.F. and Thompson, R.F., Classical Conditioning, 3rd ed, Erlbaum, New Jersey, 1987.
27. [27] Hampson, R.E., Heyser, C.J. and Deadwyler, S.A., Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat, Behav. Neurosci., 107 (1993) 715-739.
28. [28] Hopkins, D.A. and Holstege, G., Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat, Exp Brain Res., 32 (1978) 529-574.
29. [29] Huynh, H. and Feldt, L.S., Estimation of the Box correction for degrees of freedom from sample data in randomized block and split-plot designs, J. Edu. Stat., 1 (1976) 69-82.
30. [30] Jarrell, T.W., Romanski, L.M., Gentile, C.G., McCabe, P.M. and Schneiderman, N., Ibotenic acid lesions in the medial geniculate region prevent the acquisition of differential Pavlovian conditioning of bradycardia to acoustic stimuli in rabbits, Brain Res., 382 (1986) 199-203.
31. [31] Jarrell, T.W., Gentile, C.G., Romanski, L.M., McCabe, P.M. and Schneiderman, N., Involvement of cortical and thalamic auditory regions in retention of differential bradycardiac conditioning to acoustic stimuli in rabbits, Brain Res., 412 (1987) 285-294.
32. [32] Kapp, B.S., Wilson, A., Pascoe, J.P., Supple, W. and Whalen, P.J., A neuroanatomical systems analysis of conditioned bradycardia in the rabbit. In M. Gabriel and J. Moore (Eds.), Learning and Computational Neuroscience: Foundations of Adaptive Networks, MIT Press, Massachusetts, 1990, pp. 53-90.
33. [33] Krettek, J.E. and Price, J.L., Projections from the amygdaloid complex to the cerebral cortex and thalamus in rat and cat, J. Comp. Neurol., 172 (1977) 687-722.
34. [34] Krupa, D.J., Thompson, J.K. and Thompson, R.F., Localization of a memory trace in the mammalian brain, Science, 260 (1993) 989-991.
35. [35] Kubota, Y., Wolske, M., Poremba, A., Kang, E. and Gabriel, M., Stimulus-related and movement-related single-unit activity in rabbit cingulate cortex and limbic thalamus during performance of discriminative avoidance behavior, Brain Res., 721 (1996) 22-38.
36. [36] LeDoux JE. Information flow from sensation to emotion: plasticity in the neural computation of stimulus value. In M. Gabriel and J. Moore (Eds.), Learning and Computational Neuroscience: Foundations of Adaptive Networks, Bradford, Cambridge, MA, 1990, pp. 3-51.
37. [37] Ledoux, J.E., Emotional memory: in search of systems and synapses. In F.M. Crinella and J. Yu (Eds.), Brain Mechanisms: Papers in memory of Robert Thompson, Annals of the New York Academy of Sciences, Vol. 702, New York Academy of Sciences, New York, 1993, pp. 149-157.
38. [38] Maren, S., Poremba, A. and Gabriel, M., Basolateral amygdaloid multi-unit neuronal correlates of discriminative avoidance learning in rabbits, Brain Res., 549 (1991) 311-316.
39. [39] Mauk, M.D., Steinmetz, J.E. and Thompson, R.F., Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus, PN AS, 83 (1986) 5349-5353.
40. [40] McCabe, P.M., Gentile, C.G., Markgraf, C.G., Teich, A.H. and Schneiderman, N., Ibotenic acid lesions in the amygdaloid central nucleus but not in the lateral subthalamic area prevent the acquisition of differential Pavlovian conditioning of bradycardia in rabbits, Brain Res., 580 (1992) 155-163.
41. [41] McCormick, D.A. and Thompson, R.F., Cerebellum: essential involvement in the classically conditioned eyelid response, Science, 223 (1984) 296-299.
42. [42] McCormick D.A. and Thompson, R.F., Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response, J. Neurosci., 11 (1984) 2811-2822.
43. [43] McEchron, M.D., Green, E.J., Winters, R.W., Nolen, T.G., Schneiderman, N. and McCabe, P.M., Changes of synaptic efficacy in the medial geniculate nucleus as a result of auditory classical conditioning. J. Neurosci., 16 (1996) 1273-1283.
44. [44] McEchron, M.D., McCabe, P.M., Green, E.J., Llabre, M.M. and Schneiderman, N., Simultaneous single unit recording in the medial nucleus of the medial geniculate nucleus and amygdaloid central nucleus throughout habituation, acquisition, and extinction of the rabbits classically conditioned heart rate, Brain Res., 682 (1995) 157-166.
45. [45] Olds, J., Disterhoft, J., Segal, M., Kornblith, D.L. and Hirsh, R., Learning centers of rat brain mapped by measuring latencies of conditioned unit responses, J. Neurophysiol., 35 (1972) 202-219.
46. [46] Orona, E. and Gabriel, M., Multiple-unit activity of the prefrontal cortex and mediodorsal thalamic nucleus during acquisition of discriminative avoidance behavior in rabbits, Brain Res., 263 (1983) 295-312.
47. [47] Perrett, S.P., Ruiz, B.P. and Mauk, M.D., Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses, J. Neurosci., 13 (1993) 1708-1718.
48. [48] Poremba, A. and Gabriel, M., Amygdala lesions block acquisition of discriminative active avoidance learning in rabbits, Soc. Neurosci. Abstr., 130 (1991) 325.
49. [49] Powell, D.A., Buchanan, S.L. and Gibbs, C.M., Role of the prefrontal-thalamic axis in classical conditioning. In H.B.M. Uylings, C.G. Van Eden, J.P.C. De Bruin, M.A. Corner and M.G.P. Feeustra (Eds.), Progress in Brain Research, Vol 85, Elsevier, Amsterdam, 1990, pp. 433-466.
50. [50] Quirk, G.J., Repa, J.C. and LeDoux, J.E., Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat, Neuron, 15 (1995) 1029-1039.
51. [51] Ryugo, D.K. and Weinberger, N.M., Differential plasticity of morphologically distinct neuron populations in medial geniculate body of the cat during classical conditioning, Behav. Biol., 22 (1978) 275-301.
52. [52] Schoenbaum, G. and Eichenbaum, H., Information coding in the rodent prefrontal cortex, I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex, J. Neurophysiol., 74 (1995) 733-750.
53. [53] Solomon, P.R., Solomon, S.D., Vander Schaaf, E. and Perry, H.E., Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure, Science, 220 (1983) 329-331.
54. [54] Steinmetz, J.E., Logan, C.G., Rosen, D.J., Thompson, J.K., Lavond, D.G. and Thompson, R.F., Initial localization of the acoustic conditioned stimulus projection system to the cerebellum essential for classical eyelid conditioning, PN AS, 84 (1987) 3531-3535.
55. [55] Thompson, R.F., Organization of memory traces in the mammalian brain, Annu. Rev. Neurosci., 17 (1994) 519-549.
56. [56] Weiss, C., Kronforst, M.A. and Disterhoft, J.F., Hippocampal CA1 single neuron activity during trace eyeblink conditioning, Soc. Neurosci. Abstr., 21 (1995) 1931.
57. [57] Weisz, D.J., Harden, D.G. and Xiang, Z., Effects of amygdala lesions on reflex facilitation and conditioned response acquisition during nictitating membrane response conditioning in rabbit, Behav. Neurosci., 106 (1992) 262-273.
58. [58] Winer, B.J., Statistical Principles in Experimental Design, McGraw-Hill, New York, 1962.
59. [59] Weinberger, N.M., Ashe, J.H., Metherate, R., McKenna, T.M., Diamond, D.M., Bakin, J.S., Lennartz, R.C. and Cassady, J.M., Neural adaptive information processing: a preliminary model of receptive-field plasticity in auditory cortex during pavlovian conditioning. In M. Gabriel and J. Moore (Eds.), Learning and Computational Neuroscience: Foundations of Adaptive Networks, Bradford, Cambridge, MA, 1990, pp. 91-138.
60. [60] Yeo, C.H. and Hardiman, M.J., Cerebellar cortex and eyeblink conditioning: a reexamination, Exp. Brain Res., 88 (1992) 623-638.
61. [61] Young, B.J., Otto, T., Fox, G.D. and Eichenbaum, H., Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task, J. Neurosci., 14 (1994) 6553-6563.
62. [62] Zola-Morgan, S. and Squire, L.R., Neuroanatomy of memory, Annu. Rev. Neurosci., 16 (1993) 547-563.