Cross-modal transfer of the conditioned eyeblink response during interstimulus interval discrimination training in young rats

Developmental Psychobiology

Volumn 50, Issue 7, 2008, Pages 647-664

  Brown, Kevin L ^a,b   Stanton, Mark E ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b TEMPLE UNIVERSITY   (United States)

Author keywords

Cross modal transfer; Development; Eyeblink conditioning; ISI discrimination; Rats

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BLINKING; CONDITIONED REFLEX; CONTROLLED STUDY; DISCRIMINATION LEARNING; EYELID REFLEX; FEMALE; INTERSTIMULUS INTERVAL; MALE; MOTOR PERFORMANCE; NONHUMAN; ONTOGENY; PERINATAL PERIOD; RAT; STIMULUS RESPONSE; TASK PERFORMANCE;

ACOUSTIC STIMULATION; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; AUDITORY PERCEPTION; CONDITIONING, EYELID; DISCRIMINATION LEARNING; ELECTROSHOCK; FEMALE; MALE; PHOTIC STIMULATION; RATS; RATS, LONG-EVANS; REACTION TIME; TIME PERCEPTION; TRANSFER (PSYCHOLOGY); UNCERTAINTY; VISUAL PERCEPTION;

RATTUS;

EID: 56849112194     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20335     Document Type: Article

References (88)

1. Altman, J., & Bayer, S. A. (1997). Development of the cerebellar system in relation to its evolution, structure, and functions. Boca Raton, FL: CRC Press.
2. Anderson, W. A., & Flumerfelt, B. A. (1985). Purkinje cell growth beyond the twenty-third postnatal day. Developmental Brain Research, 17, 195-200.
3. Bahrick, L. E., & Lickliter, R. (2000). Intersensory redundancy guides attentional selectivity and perceptual learning in infancy. Developmental Psychology, 36, 190-201.
4. Bao, S., Chen, L., Kim, J. J., & Thompson, R. F. (2002). Cerebellar cortical inhibition and classical eyeblink conditioning. Proceedings of the National Academy of Sciences of the United States of America, 99, 1592-1597.
5. Bao, S., Chen, L., & Thompson, R. F. (2000). Learning- and cerebellum-dependent neuronal activity in the lateral pontine nucleus. Behavioral Neuroscience, 114, 254-261.
6. Berry, M., & Bradley, P. (1976). The growth of dendritic trees of Purkinje cells in the cerebellum of the rat. Brain Research, 112, 1-35.
7. Brandon, S. E., Vogel, E. H., & Wagner, A. R. (2003). Stimulus representation in SOP: I. Theoretical rationalization and some implications. Behavioural. Processes, 62, 5-25.
8. Bower, T. G. R. (1989). The rational infant - Learing in infancy. New York: W.H. Freeman and Company.
9. Brodal, A. (1967). Anatomical studies of cerebellar fibre connections with special reference to problems of functional localization. Progress in Brain Research, 25, 135-173.
10. Brown, K. L., Calizo, L. H., Goodlett, C. R., & Stanton, M. E. (2007). Neonatal alcohol exposure impairs acquisition of eyeblink conditioned responses during discrimination learning and reversal in weanling rats. Developmental Psychobiology, 49, 243-257.
11. Brown, K. L., Calizo, L. H., & Stanton, M. E. (2008). Dose dependent deficits in dual interstimulus interval classical eyeblink conditioning tasks following neonatal binge alcohol exposure in rats. Alcoholism: Clinical & Experimental Research, 32, 277-293.
12. Brown, K. L., Pagani, J. H., & Stanton, M. E. (2006). The ontogeny of interstimulus interval (ISI) discrimination of the conditioned eyeblink response in rats. Behavioral Neuroscience, 120, 1057-1070.
13. Campolattaro, M., & Freeman, J. H. (2006). Cerebellar inactivation during cross-modal transfer. Society for Neuroscience Abstracts, 667.2.
14. Chen, L., Bao, S., Lockard, J. M., Kim, J. J., & Thompson, R. F. (1996). Impaired classical eyeblink conditioning in cerebellar-lesioned and Purkinje cell degeneration (pcd) mutant mice. Journal of Neuroscience, 16, 2829-2838.
15. Choi, J., & Moore, J. W. (2003). Cerebellar neuronal activity expresses the complex topography of conditioned eyeblink responses. Behavioral Neuroscience, 117, 1211-1219.
16. Christian, K. M., & Thompson, R. F. (2003). Neural substrates of eyeblink conditioning: Acquisition and retention. Learning & Memory, 11, 427-455.
17. Clark, R. E., Gohl, E. B., & Lavond, D. G. (1997). The learning-related activity that develops in the pontine nuclei during classical eyeblink conditioning is dependent on the interpositus nucleus. Learning & Memory, 3, 532-544.
18. Coleman, S. R., & Gormezano, I. (1971). Classical conditioning of the rabbit's (Oryctolagus cuniculus) nictitating membrane response under symmetrical CS-US interval shifts. Journal of Comparative & Physiological Psychology, 77, 447-455.
19. Duong, H. B., Brown, K. L., & Stanton, M. E. (2007). Cross-modal transfer of timing of the classically conditioned eyeblink response in weanling rats. International Society for Developmental Psychobiology Abstracts, 15.
20. Freeman, J. H., Barone, S., & Stanton, M. E. (1995). Disruption of cerebellar maturation by an antimitotic agent impairs the ontogeny of eyeblink conditioning in rats. Journal of Neuroscience, 15, 7301-7314.
21. Freeman, J. H., & Nicholson, D. A. (2004). Developmental changes in the neural mechanisms of eyeblink conditioning. Behavioral & Cognitive Neuroscience Reviews, 3, 3-13.
22. Freeman, J. H., Nicholson, D. A., Muckler, A. S., Rabinak, C. A., & DiPietro, N. T. (2003). Ontogeny of eyeblink conditioned response timing in rats. Behavioral Neuroscience, 117, 283-291.
23. Frieman, J., & Goyette, C. H. (1973). Transfer of training across stimulus modality and response class. Journal of Experimental Psychology, 97, 235-241.
24. Garcia, K. S., & Mauk, M. D. (1998). Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology, 37, 471-480.
25. Garcia, K. S., Steele, P. M., & Mauk, M. D. (1999). Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. Journal of Neuroscience, 19, 10940-10947.
26. Gibson, E. J. (1969). Principles of perceptual learning and development. New York: Appleton-Century-Crofts.
27. Glickstein, M. (1997). Mossy-fibre sensory input to the cerebellum. Progress in Brain Research, 114, 251-259.
28. Gould, T. J., Sears, L. L., & Steinmetz, J. E. (1993). Possible CS and US pathways for rabbit classical eyelid conditioning: Electrophysiological evidence for projections from the pontine nuclei and inferior olive to cerebellar cortex and nuclei. Behavioral & Neural Biology, 60, 172-185.
29. Green, J. T., & Steinmetz, J. E. (2005). Purkinje cell activity in the cerebellar anterior lobe after rabbit eyeblink conditioning. Learning & Memory, 12, 260-269.
30. Harlow, H. F. (1949). The formation of learning sets. Psychological Review, 56, 51-65.
31. Harvey, J. A., Welsh, J. P., Yeo, C. H., & Romano, A. G. (1993). Recoverable and nonrecoverable deficits in conditioned responses after cerebellar cortical lesions. Journal of Neuroscience, 13, 1624-1635.
32. Hoehler, F. K., & Leonard, D. W. (1976). Double responding in classical nictitating membrane conditioning with single-CS dual-ISI training. Pavlovian Journal of Biological Science, 11, 180-190.
33. Holt, P. E., & Kehoe, E. J. (1985). Cross-modal transfer as a function of similarities between training tasks in classical conditioning of the rabbit. Animal Learning & Behavior, 13, 51-59.
34. Honey, R. C., & Hall, G. H. (1989). Acquired equivalence and distinctiveness of cues. Journal of Experimental Psychology: Animal Behavioral Processes, 15, 338-346.
35. Hull, C. L. (1939). The problem of stimulus equivalence in behavior theory. Psychological Review, 46, 9-30.
36. Ivkovich, D., Paczkowski, C. M., & Stanton, M. E. (2000). Ontogeny of delay versus trace eyeblink conditioning in the rat. Developmental Psychobiology, 36, 148-160.
37. Joscelyne, A., & Kehoe, E. J. (2007). Time and stimulus specificity in extinction of the conditioned nictitating membrane response in the rabbit (Oryctolagus cuniculus). Behavioral Neuroscience, 121, 50-62.
38. Kehoe, E. J. (1988). A layered network model of associative learning: Learning to learn and configuration. Psychological Review, 95, 411-433.
39. Kehoe, E. J. (1990). Classical conditioning: Fundamental issues for adaptive network models. In: M. Gabriel & J. Moore (Eds.), Learning and computational neuroscience: Foundations of adaptive networks. (pp. 389-420). Cambridge, MA: MIT Press.
40. Kehoe, E. J, Graham-Clarke, P., & Schreurs, B. G. (1989). Temporal patterns of the rabbit's nictitating membrane response to compound and component stimuli under mixed CS-US intervals. Behavioral Neuroscience, 103, 283-295.
41. Kehoe, E. J., & Holt, P. E. (1984). Transfer across CS-US intervals and sensory modalities in classical conditioning of the rabbit. Animal Learning & Behavior, 12, 122-128.
42. Kehoe, E. J., Horne, P. S., & Horne, A. J. (1993). Discrimination learning using different CS-US intervals in classical conditioning of the rabbit's nictitating membrane response. Psychobiology, 21, 277-285.
43. Kehoe, E. J., Horne, A. J., & Macrae, M. (1995). Learning to learn: Real-time features and a connectionist model. Adaptive Behavior, 3, 235-271.
44. Kehoe, E. J., & Joscelyne, A. (2005). Temporally specific extinction of conditioned responses in the rabbit (Oryctolagus cuniculus) nictitating membrane preparation. Behavioral Neuroscience, 119, 1011-1022.
45. Kehoe, E. J., Morrow, L. D., & Holt, P. E. (1984). General transfer across sensory modalities survives reductions in the original conditioned reflex in the rabbit. Animal Learning & Behavior, 12, 129-136.
46. Kehoe, E. J., & Napier, R. M. (1991). Temporal specificity in cross-modal transfer of the rabbit nictitating membrane response. Journal of Experimental Psychology: Animal Behavior Processes, 17, 26-35.
47. Kraebel, K. S., & Spear, N. E. (2000). Infant rats are more likely than adolescents to orient differentially to amodal (intensity-based) features of single-element and compound stimuli. Developmental Psychobiology, 36, 49-66.
48. Lavond, D. G., & Steinmetz, J. E. (1989). Acquisition of classical conditioning without cerebellar cortex. Behavioural Brain Research, 33, 113-164.
49. Lavond, D. G., Steinmetz, J. E., Yokaitis, M. H., & Thompson, R. F. (1987). Reacquisition of classical conditioning after removal of cerebellar cortex. Experimental Brain Research, 67, 569-593.
50. Lewis, J. L., LoTurco, J. J., & Solomon, P. R. (1987). Lesions of the middle cerebellar peduncle disrupt acquisition and retention of the rabbit's classically conditioned nictitating membrane response. Behavioral Neuroscience, 101, 151-157.
51. Lewkowicz, D. L., & Turkewitz, G. (1980). Cross-modal equivalence in early infancy: Auditory-visual intensity matching. Developmental Psychology, 16, 597-607.
52. Lickliter, R., & Bahrick, L. E. (2004). Perceptual development and the origins of multisensory responsiveness. In: G. A. Calvert, C. Spence, & B. E. Stein (Eds.), The handbook of multisensory processes. (pp. 643-654). Cambridge, MA: MIT Press.
53. Mauk, M. D., & Ruiz, B. P. (1992). Learning-dependent timing of Pavlovian eyelid responses: Differential conditioning using multiple interstimulus intervals. Behavioral Neuroscience, 106, 666-681.
54. McCormick, D. A., Steinmetz, J. E., & Thompson, R. F. (1985). Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Research, 359, 120-130.
55. Meck, W. H., & Church, R. M. (1982). Abstraction of temporal attributes. Journal of Experimental Psychology: Animal Behavior Processes, 8, 226-243.
56. Medina, J. F., Garcia, K. S., Nores, W. L., Taylor, N. M., & Mauk, M. D. (2000). Timing mechanisms in the cerebellum: Testing predictions of a large-scale computer simulation. Journal of Neuroscience, 20, 5516-5525.
57. Melton, R. C., Kraemer, R J., & Spear, N. E. (1991). Development of intersensory function: Age-related differences in stimulus selection of multimodal compounds in rats as revealed by Pavlovian conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 17, 448-464.
58. Metzger, F., & Kapfhammer, J. P. (2003). Protein kinase C: Its role in activity-dependent Purkinje cell dendritic development and plasticity. Cerebellum, 2, 206-214.
59. Millenson, J. R., Kehoe, E. J., & Gormezano, I. (1977). Classical conditioning of the rabbit's nictitating membrane response under fixed and mixed CS-US intervals. Learning & Motivation, 8, 351-366.
60. Miller, N. E., & Dollard, J. C. (1941). Social learning and imitation. New Haven, CT: Yale University Press.
61. Molina, J. C., Hoffman, H., Serwatka, J., & Spear, N. E. (1991). Establishing intermodal equivalence in preweanling and adult rats. Journal of Experimental Psychology: Animal Behavior Processes, 17, 433-447.
62. Moore, J. W., & Choi, J. S. (1997). Conditioned response timing and integration in the cerebellum. Learning & Memory, 3, 116-129.
63. Mortimer, J. A. (1975). Cerebellar responses to teleceptive stimuli in alert monkeys. Brain Research, 83, 369-390.
64. Nolan, B. C., & Freeman, J. H. (2006). Purkinje cell loss by OX7-saporin impairs acquisition and extinction of eyeblink conditioning. Learning & Memory, 13, 359-365.
65. Nores, W. L., Medina, J. F., Steele, P. M., & Mauk, M. D. (2000). Relative contributions of the cerebellar cortex and cerebellar nucleus to eyelid conditioning. In: D. S. Woodruff-Pak & J. E. Steinmetz (Eds.), Eyeblink classical conditioning. (Vol. 2: Animal Models, pp. 205-229). Boston: Kluwer Academic Publishers.
66. Ohyama, T., & Mauk, M. D. (2001). Latent acquisition of timed responses in cerebellar cortex. Journal of Neuroscience, 21, 682-690.
67. Paczkowski, C., Ivkovich, D., & Stanton, M. E. (1999). Ontogeny of eyeblink conditioning using a visual conditional stimulus. Developmental Psychobiology, 35, 253-263.
68. Pearce, J. M. (1987). A model for stimulus generalization in Pavlovian conditioning. Psychological Review, 94, 61-73.
69. Perrett, S. P., Ruiz, B. P., & Mauk, M. D. (1993). Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. Journal of Neuroscience, 13, 1708-1718.
70. Puro, D. G., & Woodward, D. J. (1977a). Maturation of evoked climbing fiber input to rat cerebellar Purkinje cells: I. Experimental Brain Research, 28, 85-100.
71. Puro, D. G., & Woodward, D. J. (1977b). Maturation of evoked mossy fiber input to rat cerebellar Purkinje cells: II. Experimental Brain Research, 28, 427-441.
72. Roberts, S. (1982). Cross-modal use of an internal clock. Journal of Experimental Psychology: Animal Behavior Process, 8, 2-22.
73. Schreurs, B. G., & Kehoe, E. J. (1987). Cross-modal transfer as a function of initial training level in classical conditioning with the rabbit. Animal Leaming & Behavior, 15, 47-54.
74. Smith, M. C. (1968). CS-US interval and US intensity in classical conditioning of the rabbit's nictitating membrane response. Journal of Comparative & Physiological Psychology, 66, 679-687.
75. Snider, R. S., & Stowell, A. (1944). Receiving areas of the tactile, auditory, and visual systems in the cerebellum. Journal of Neurophysiology, 7, 331-357.
76. Spear, N. E. (1984). Ecologically determined dispositions control the ontogeny of learning and Memory. In: R. Kail & N. E. Spear (Eds.), Comparative perspectives on the development of memory. (pp. 325-358). Hillsdale, NJ: Lawrence Erlbaum Associates.
77. Spear, N. E., & Kucharski, D. (1984). Ontogenetic differences in stimulus selection during conditioning. In: R. Kail & N. E. Spear (Eds.), Comparative perspectives on the development of memory. (pp. 227-252). Hillsdale, NJ: Lawrence Erlbaum Associates.
78. Spear, N. E., & Molina, J. C. (1987). The role of sensory modality in the ontogeny of stimulus selection. In: N. Krasnegor, E. M. Blass, M. A. Hofer, & W. P. Smotherman (Eds.), Perinatal development: A psychobiological perspective. (pp 83-110). Orlando, FL: Academic Press.
79. Stanton, M. E., Fox, G. D., & Carter, C. S. (1998). Ontogeny of the conditioned eyeblink response in rats: Acquisition or expression? Neuropharmacology, 37, 623-632.
80. Stanton, M. E., & Freeman, J. H. (1994). Eyeblink conditioning in the developing rat: An animal model of learning in developmental neurotoxicology. Environmental Health Perspectives, 102, 131-139.
81. Stanton, M. E., & Freeman, J. H. (2000). Developmental studies of eyeblink conditioning in the rat. In: D. S. Woodruff-Pak & J. E. Steinmetz (Eds.), Eyeblink classical conditioning. (Vol. 2: Animal Models, pp. 17-49). Boston: Kluwer Academic Publishers.
82. Stanton, M. E., Freeman, J. H., & Skelton, R. W. (1992). Eyeblink conditioning in the developing rat. Behavioral Neuroscience, 106, 657-665.
83. Steinmetz, J. E., Logan, C. G., Rosen, D. J., Thompson, J. K., Lavond, D. G., & Thompson, R. F. (1987). Initial localization of the acoustic conditioned stimulus projection system to the cerebellum essential for classical eyelid conditioning. Proceedings of the National Academy of Sciences of the United States of America, 84, 3531-3535.
84. Thomas, D. R., Miller, J. T., & Svinicki, J. G. (1971). Nonspecific transfer effects of discrimination training in the rat. Journal of Comparative & Physiological Psychology, 74, 96-101.
85. Tracy, J., Britton, G. B., & Steinmetz, J. E. (2001). Comparison of single unit responses to tone, light, and compound conditioned stimuli during rabbit classical eyeblink conditioning. Neurobiology of Learning & Memory, 76, 253-267.
86. Tran, T. D., Stanton, M. E., & Goodlett, C. R. (2007). Bingelike ethanol exposure during the early postnatal period impairs eyeblink conditioning at short and long CS-US intervals in rats. Developmental Psychobiology, 49, 589-605.
87. Turkewitz, G., & Mellon, R. C. (1989). Dynamic organization of intersensory function. Canadian Journal of Psychology, 43, 286-301.
88. Yeo, C. H., & Hardiman, M. J. (1992). Cerebellar cortex and eyeblink conditioning: A reexamination. Experimental Brain Research, 88, 623-638.