Hippocampectomy disrupts trace eye-blink conditioning in rabbits.

The role of the hippocampus (HFC) in trace eye-blink conditioning was evaluated using a 100-ms tone conditioned stimulus (CS), a 300- or 500-ms trace interval, and a 150-ms air puff unconditioned stimulus (UCS). Rabbits received complete hippocampectomy (dorsal & ventral), sham lesions, or neocortical lesions. Hippocampectomy produced differential effects in relation to the trace interval used. With a 300-ms trace interval, HPC-lesioned Ss showed profound resistance to extinction after acquisition. With a 500-ms trace interval, HPC-lesioned Ss did not learn the task (only 22% conditioned responses (CRs) after 25 sessions, whereas controls showed >80% after 10 sessions), and on the few trials in which a CR occurred, most were "nonadaptive" short-latency CRs (i.e., they started during or just after the CS and always terminated prior to UCS onset). The authors conclude that the HPC encodes a temporal relationship between CS and UCS, and when the trace interval is long enough (e.g., 500 ms), that the HPC is necessary for associative learning of the conditioned eye-blink response.

[1]  M. Segal.  Flow of conditioned responses in limbic telencephalic system of the rat. , 1973, Journal of neurophysiology.

[2]  D. Alkon,et al.  AHP reductions in rabbit hippocampal neurons during conditioning correlate with acquisition of the learned response , 1988, Brain Research.

[3]  J. Theios,et al.  Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). , 1972, Journal of comparative and physiological psychology.

[4]  JOHN W. Moore,et al.  A brain stem region essential for the classically conditioned but not unconditioned nictitating membrane response , 1982, Physiology & Behavior.

[5]  M. Glickstein,et al.  Classical conditioning of the nictitating membrane response of the rabbit , 2004, Experimental Brain Research.

[6]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[7]  M. Glickstein,et al.  Classical conditioning of the nictitating membrane response of the rabbit , 2004, Experimental Brain Research.

[8]  Richard F. Thompson,et al.  Neuronal plasticity recorded from cat hippocampus during classical conditioning , 1979, Brain Research.

[9]  O. Vinogradova.  Functional Organization of the Limbic System in the Process of Registration of Information: Facts and Hypotheses , 1975 .

[10]  R. Church,et al.  Hippocampus, time, and memory. , 1984, Behavioral neuroscience.

[11]  M. M. Patterson,et al.  Retention and acquisition of classical trace conditioned responses by rabbits with hippocampal lesions. , 1986, Behavioral neuroscience.

[12]  Richard F. Thompson,et al.  Retention of classically conditioned eyelid responses following acute decerebration , 1987, Brain Research.

[13]  J. Disterhoft,et al.  Learning-induced afterhyperpolarization reductions in hippocampus are specific for cell type and potassium conductance , 1990, Experimental Brain Research.

[14]  J. Rawlins,et al.  Associations across time: The hippocampus as a temporary memory store , 1985, Behavioral and Brain Sciences.

[15]  T W Berger,et al.  Identification of pyramidal cells as the critical elements in hippocampal neuronal plasticity during learning. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[16]  G Lynch,et al.  Classical conditioning of the rabbit eyelid response increases glutamate receptor binding in hippocampal synaptic membranes. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[17]  P. Solomon.  Temporal versus spatial information processing theories of hippocampal function. , 1979, Psychological bulletin.

[18]  R. F. Thompson,et al.  Neuronal substrate of classical conditioning in the hippocampus , 1976, Science.

[19]  D. Alkon,et al.  Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Richard F. Thompson,et al.  Pharmacological analysis of the magnocellular red nucleus during classical conditioning of the rabbit nictitating membrane response , 1988, Brain Research.

[21]  P. Solomon.  A time and a place for everything? Temporal processing views of hippocampal function with special reference to attention , 1980 .

[22]  D. Alkon,et al.  Hippocampal lesions impair memory of short-delay conditioned eye blink in rabbits. , 1989, Behavioral neuroscience.

[23]  J. Falk.  Physiology and Behavior. , 1973 .

[24]  C. Yeo,et al.  Hippocampal lesions and trace conditioning in the rabbit , 1987, Behavioural Brain Research.

[25]  P. Solomon,et al.  Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation. , 1975, Journal of comparative and physiological psychology.

[26]  W. B. Orr,et al.  Hippocampectomy selectively disrupts discrimination reversal conditioning of the rabbit nictitating membrane response , 1983, Behavioural Brain Research.

[27]  D L Alkon,et al.  Classical conditioning induces long-term translocation of protein kinase C in rabbit hippocampal CA1 cells. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Theodore W. Berger,et al.  Hippocampal unit-behavior correlations during classical conditioning , 1980, Brain Research.

[29]  M. M. Patterson,et al.  Differential effects of hippocampectomy on classically conditioned rabbit nictitating membrane response related to interstimulus interval. , 1985, Behavioral neuroscience.

[30]  R. F. Thompson,et al.  Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  T W Berger,et al.  Hippocampectomy disrupts the topography of conditioned nictitating membrane responses during reversal learning. , 1985, Behavioral neuroscience.

[32]  D L Alkon,et al.  Enhancement of synaptic potentials in rabbit CA1 pyramidal neurons following classical conditioning. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Disterhoft,et al.  Nictating membrane conditioning to tone in the immobilized albino rabbit , 1977, Brain Research.

[34]  R. F. Thompson,et al.  Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. , 1983, Journal of neurophysiology.

[35]  Richard F. Thompson,et al.  The effect of temporal single alternation on learned increases in hippocampal unit activity in classical conditioning of the rabbit nictitating membrane response , 1979 .

[36]  R. F. Thompson,et al.  Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. , 1986, Behavioral neuroscience.

[37]  L. Squire,et al.  Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  J. B. Sidowski,et al.  Experimental methods and instrumentation in psychology , 1966 .

[39]  D L Alkon,et al.  Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus. , 1989, Science.

[40]  D. Kimble,et al.  Hippocampectomy and response perseveration in the rat. , 1965, Journal of comparative and physiological psychology.

[41]  D. Alkon,et al.  Classical conditioning reduces amplitude and duration of calcium-dependent afterhyperpolarization in rabbit hippocampal pyramidal cells. , 1989, Journal of neurophysiology.

[42]  Richard F. Thompson,et al.  Neuronal plasticity in the limbic system during classical conditioning of the rabbit nictitating membrane response. I. The hippocampus , 1978, Brain Research.

[43]  M. M. Patterson,et al.  Fimbrial lesions and sensory preconditioning. , 1984, Behavioral neuroscience.