The effects of ibotenic acid lesions of the nucleus accumbens on spatial learning and extinction in the rat

Rats with ibotenic acid lesions of the nucleus accumbens (N. Acc) were studied in two spatial learning paradigms: a T-maze and a Morris water maze. Learning of a spatial discrimination task and its reversal in the T-maze were disrupted by the N. Acc lesions. As both original and reversal learning were impaired, there was no evidence of a specific lesion effect on reversal learning. The lesioned rats did not perseverate excessively in their choice of the previously reinforced arm. There was evidence of behavioural inflexibility during extinction when the lesioned rats failed to slow the pace at which they ran the maze in the absence of reward. Spontaneous alternation was not significantly affected by the lesion. Acquisition of the second spatial task, locating the hidden platform in the Morris water maze, was also impaired. The lesioned rats did eventually learn the task and successfully reached the platform with similar latencies and heading errors to controls. Thus, the N. Acc lesion impaired but did not abolish spatial learning in the T-maze and the water maze. The deficits observed in this study may reflect a role for the N. Acc in the reorganisation of behaviour in response to external change.

[1]  G. Mogenson,et al.  A study of the contribution of hippocampal-accumbens-subpallidal projections to locomotor activity. , 1984, Behavioral and neural biology.

[2]  U. Ungerstedt Stereotaxic mapping of the monoamine pathways in the rat brain. , 1971, Acta physiologica Scandinavica. Supplementum.

[3]  A. Kelley,et al.  The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: An anterograde and retrograde-horseradish peroxidase study , 1982, Neuroscience.

[4]  Bryan Kolb,et al.  Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat , 1982, Neuroscience Letters.

[5]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[6]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  I. Whishaw,et al.  Decortication abolishes place but not cue learning in rats , 1984, Behavioural Brain Research.

[8]  I. Whishaw,et al.  Disruption of central cholinergic systems in the rat by basal forebrain lesions or atropine: Effects on feeding, sensorimotor behaviour, locomotor activity and spatial navigation , 1985, Behavioural Brain Research.

[9]  C. Carter,et al.  Effect of 6‐Hydroxydopamine Lesions of the Medial Prefrontal Cortex on Neurotransmitter Systems in Subcortical Sites in the Rat , 1980, Journal of neurochemistry.

[10]  T. Robbins,et al.  Selective disruption of displacement behaviour by lesions of the mesolimbic dopamine system , 1980, Nature.

[11]  L. Heimer,et al.  Ventral striatum and ventral pallidum Components of the motor system? , 1982, Trends in Neurosciences.

[12]  M. Le Moal,et al.  Behavioral study after local injection of 6-hydroxydopamine into the nucleus accumbens in the rat , 1985, Brain Research.

[13]  B. Kolb,et al.  Comparisons of behavioral effects of hippocampal and prefrontal cortex lesions in the rat. , 1974, Journal of comparative and physiological psychology.

[14]  Ian Q. Whishaw,et al.  Impairments in the acquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats , 1987, Behavioural Brain Research.

[15]  P. Kelly,et al.  Effects of amphetamine and apomorphine on locomotor activity after 6-OHDA and electrolytic lesions of the nucleus accumbens septi , 1983, Pharmacology Biochemistry and Behavior.

[16]  C. Carter,et al.  Behavioural and biochemical effects of dopamine and noradrenaline depletion within the medial prefrontal cortex of the rat , 1980, Brain Research.

[17]  M. Mesulam,et al.  Temporal cortical projections to the olfactory tubercle in the rhesus monkey , 1976, Brain Research.

[18]  E. D. Kemble,et al.  Vicarious trial and error following amygdaloid lesions in rats. , 1970, Neuropsychologia.

[19]  H. E. Rosvold,et al.  Behavioral effects of selective ablation of the caudate nucleus. , 1967, Journal of comparative and physiological psychology.

[20]  E. W. Powell,et al.  Connections of the nucleus accumbens , 1976, Brain Research.

[21]  I. Whishaw,et al.  Dopamine depletion, stimulation or blockade in the rat disrupts spatial navigation and locomotion dependent upon beacon or distal cues , 1985, Behavioural Brain Research.

[22]  R. Sutherland,et al.  A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. , 1983, Behavioral neuroscience.

[23]  W. Nauta,et al.  Efferent connections of the ventral pallidum: Evidence of a dual striato pallidofugal pathway , 1985, The Journal of comparative neurology.

[24]  M. Le Moal,et al.  Alternation behavior, spatial discrimination, and reversal disturbances following 6-hydroxydopamine lesions in the nucleus accumbens of the rat. , 1985, Behavioral and neural biology.

[25]  R. Sutherland,et al.  Dissociation of the contributions of the prefrontal cortex and dorsomedial thalamic nucleus to spatially guided behavior in the rat , 1982, Behavioural Brain Research.

[26]  T. Robbins,et al.  Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi and olfactory tubercle on feeding, locomotor activity, and amphetamine anorexia in the rat. , 1978, Journal of comparative and physiological psychology.

[27]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain II. Amygdala, suprarhinal cortex and entorhinal cortex , 1978, The Journal of comparative neurology.

[28]  F Mauguiere,et al.  The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis. , 1980, Brain : a journal of neurology.

[29]  G. P. Smith,et al.  Decreased locomotor and investigatory exploration after denervation of catecholamine terminal fields in the forebrain of rats. , 1979, Journal of comparative and physiological psychology.

[30]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[31]  R. Morris Spatial Localization Does Not Require the Presence of Local Cues , 1981 .

[32]  F. Fonnum,et al.  The effects of surgical and chemical lesions on neurotransmitter candidates in the nucleus accumbens of the rat , 1979, Neuroscience.

[33]  T. Robbins,et al.  Comparative effects of infusions of 6-hydroxydopamine into nucleus accumbens and anterolateral hypothalamus induced by 6-hydroxydopamine on the response to dopamine agonists, body weight, locomotor activity and measures of exploration in the rat , 1985, Neuropharmacology.

[34]  B. Kolb,et al.  Double dissociation of spatial impairments and perseveration following selective prefrontal lesions in rats. , 1974, Journal of comparative and physiological psychology.

[35]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain IV. Topography of the dopamine projection to the basal forebrain and neostriatum , 1978, The Journal of comparative neurology.

[36]  S. Iversen,et al.  Learning impairments following selective kainic acid-induced lesions within the neostriatum of rats , 1981, Behavioural Brain Research.

[37]  G. Mogenson,et al.  Electrophysiological responses of neurones in the nucleus accumbens to hippocampal stimulation and the attenuation of the excitatory responses by the mesolimbic dopaminergic system , 1984, Brain Research.

[38]  W. Nauta,et al.  The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods , 1982, Neuroscience.

[39]  N. McNaughton,et al.  Comparison between the behavioural effects of septal and hippocampal lesions: A review , 1983, Neuroscience & Biobehavioral Reviews.

[40]  C. Y. Yim,et al.  Response of nucleus accumbens neurons to amygdala stimulation and its modification by dopamine , 1982, Brain Research.

[41]  R. Morris,et al.  The effects of central catecholamine depletions on spatial learning in rats , 1983, Behavioural Brain Research.

[42]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[43]  E. D. Kemble,et al.  Runway performance of rats following amygdaloid lesions. , 1970, Physiology & behavior.

[44]  Gerard P. Smith,et al.  Relationships between selective denervation of dopamine terminal fields in the anterior forebrain and behavioral responses to amphetamine and apomorphine , 1980, Brain Research.

[45]  J. V. van Rossum,et al.  Effects of chemical stimulation of the mesolimbic dopamine system upon locomotor activity. , 1976, European journal of pharmacology.

[46]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[47]  L. Pellegrino,et al.  stereotaxic atlas of the rat brain , 1967 .

[48]  W. Nauta,et al.  Crossroads of Limbic and Striatal Circuitry: Hypothalamo-Nigral Connections , 1978 .

[49]  G. V. Van Hoesen,et al.  Widespread corticostriate projections from temporal cortex of the rhesus monkey , 1981, The Journal of comparative neurology.

[50]  I. Whishaw Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool. , 1985, Behavioral neuroscience.

[51]  G. Mogenson,et al.  Neuropharmacological evidence to suggest that the nucleus accumbens and subpallidal region contribute to exploratory locomotion. , 1984, Behavioral and neural biology.

[52]  W. Nauta,et al.  Efferent connections of the substantia nigra and ventral tegmental area in the rat , 1979, Brain Research.

[53]  J. Harvey,et al.  Lesions in the nuclei accumbens septi of the rat: behavioral and neurochemical effects. , 1970, Journal of comparative and physiological psychology.

[54]  J. Rossum,et al.  Stimulation of locomotor activity following injection of dopamine into the nucleus accumbens , 1973, The Journal of pharmacy and pharmacology.