Lesions of the retrosplenial cortex produce deficits in reversal learning of the rabbit nictitating membrane response: implications for potential interactions between hippocampal and cerebellar brain systems.

The effect of bilateral lesions of the retrosplenial cortex on discrimination reversal learning of the rabbit nictitating membrane response was examined. Results showed that animals with such lesions were not impaired in their ability to acquire a cross-modality discrimination, but were severely impaired in their ability to reverse the discrimination once it was learned. All animals failed at the reversal phase of the task because they displayed high levels of conditioned responding to both the CS+ and the CS-. Thus bilateral damage to the retrosplenial cortex results in deficits in reversal learning that are highly similar to those observed after bilateral hippocampectomy. These findings are interpreted within a conceptual framework that characterizes multisynaptic projections from the hippocampus to the retrosplenial cortex, and ultimately to the cerebellum, as responsible for the behavioral expression of learning-related changes in hippocampal pyramidal cell activity.

[1]  I. Gormezano,et al.  Nictitating Membrane: Classical Conditioning and Extinction in the Albino Rabbit , 1962, Science.

[2]  R. F. Thompson,et al.  Effect of the interstimulus (CS-UCS) interval on hippocampal unit activity during classical conditioning of the nictitating membrane response of the rabbit (Oryctolagus cuniculus). , 1980, Journal of comparative and physiological psychology.

[3]  Richard F. Thompson,et al.  Hippocampal cellular plasticity during extinction of classically conditioned nictitating membrane behavior , 1982, Behavioural Brain Research.

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

[5]  G. Lynch,et al.  Memory systems of the brain : animal and human cognitive processes , 1985 .

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

[7]  K. E. Sørensen Ipsilateral projection from the subiculum to the retrosplenial cortex in the guinea pig , 1980, The Journal of comparative neurology.

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

[9]  N. Tsukahara,et al.  Pontine relay from cerebral cortex to cerebellar cortex and nucleus interpositus. , 1968, Brain research.

[10]  W. B. Orr,et al.  Hippocampectomy disrupts acquisition and retention of learned conditional responding. , 1984, Behavioral neuroscience.

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

[12]  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.

[13]  A. R. Lurii︠a︡,et al.  The neuropsychology of memory , 1977 .

[14]  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.

[15]  J. W. Moore,et al.  Red nucleus lesions disrupt the classically conditioned nictitating membrane response in rabbits , 1983, Behavioural Brain Research.

[16]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

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

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

[19]  Richard F. Thompson,et al.  Reciprocal anatomical connections between anterior thalamus and cingulate—retrosplenial cortex in the rabbit , 1980, Brain Research.

[20]  JOHN W. Moore,et al.  The nictitating membrane response: An electrophysiological study of the abducens nerve and nucleus and the accessory abducens nucleus in rabbit , 1983, Brain Research.

[21]  J. E. Rose,et al.  Structure and relations of limbic cortex and anterior thalamic nuclei in rabbit and cat , 1948, The Journal of comparative neurology.

[22]  D. Powell,et al.  Divergencies in Pavlovian conditioned heart rate and eyeblink responses produced by hippocampectomy in the rabbit (Oryctolagus cuniculus). , 1980, Behavioral and neural biology.

[23]  R. F. Thompson,et al.  Cerebellum: essential involvement in the classically conditioned eyelid response. , 1984, Science.

[24]  Cegavske Cf,et al.  Mechanisms of efferent neuronal control of the reflex nicitating membrane response in rabbit (Oryctolagus cuniculus) , 1976 .

[25]  G. Holstege,et al.  Anatomical observation on the afferent projections to the retractor bulbi motoneuronal cell group and other pathways possibly related to the blink reflex in the cat , 1986, Brain Research.

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

[27]  V. Chan‐Palay,et al.  Afferents to the cerebellar lateral nucleus. Evidence from retrograde transport of horseradish peroxidase after pressure injections through micropipettes , 1976, The Journal of comparative neurology.

[28]  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.

[29]  G. A. Clark,et al.  Effects of lesions of cerebellar nuclei on conditioned behavioral and hippocampal neuronal responses , 1984, Brain Research.