Parallel Information Processing in the Dorsal Striatum: Relation to Hippocampal Function

We investigated the effects of localized medial and lateral CPu lesions and fornix/fimbria lesions on responses to a local cue and to behavior based on cognitive–spatial information in the water maze. Rats were trained concurrently on the cue (visible platform) and spatial (submerged platform) components of the task, followed by a test in which responses to the two types of information were dissociated by a measure of competing response tendencies. Bilateral lesions of lateral CPu did not affect acquisition of either cue or spatial responding but produced a preference for the spatial response on the competition test. Bilateral lesions of the medial CPu retarded but did not prevent learning both components and produced a preference for the cue response on the competition test. The latter effect was accompanied by increased thigmotaxis (swimming in the periphery of the pool), primarily during the early acquisition trials, which was attributed to an impaired ability to respond to learned spatial information. Fornix/fimbria lesions prevented spatial but not cue learning and produced a preference for the cue response on the competition test. Asymmetric lesions (unilateral hippocampus and contralateral medial CPu) produced mild retardation of acquisition of both the cue and spatial tasks and a preference for the cue response on the competition test. These findings dissociate the functions of the lateral and medial CPu and suggest that the hippocampus and medial CPu may be parts of a system that promotes responding based on learned cognitive–spatial information, particularly in competitive cue–place response situations.

[1]  J. Stevens,et al.  Animal Intelligence , 1883, Nature.

[2]  E. Thorndike.  A PROOF OF THE LAW OF EFFECT. , 1933, Science.

[3]  L. S. Kogan.  Review of Principles of Behavior. , 1943 .

[4]  B. Skinner,et al.  Principles of Behavior , 1944 .

[5]  E. Tolman.  Cognitive maps in rats and men. , 1948, Psychological review.

[6]  W. Mikulas.  Effects of lights at the choice point on spatial alternation and position learning by normal rats and rats with bilateral lesions of the caudate nucleus , 1966 .

[7]  B. Milner,et al.  Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.☆ , 1968 .

[8]  J. A. Horel,et al.  Partial Klüver-Bucy syndrome produced by cortical disconnection. , 1969, Brain research.

[9]  V. B. Domesick.  Projections from the cingulate cortex in the rat. , 1969, Brain research.

[10]  J. A. Horel,et al.  Recovery from a partial Klüver-Bucy syndrome in the monkey produced by disconnection. , 1972, Journal of comparative and physiological psychology.

[11]  G. Winocur.  Functional dissociation within the caudate nucleus of rats. , 1974, Journal of comparative and physiological psychology.

[12]  P J Donovick,et al.  A metachromatic stain for neural tissue. , 1974, Stain technology.

[13]  R. Hirsh.  The hippocampus and contextual retrieval of information from memory: a theory. , 1974, Behavioral biology.

[14]  D. Olton.  The function of septo-hippocampal connections in spatially organized behaviour. , 1977, Ciba Foundation symposium.

[15]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[16]  M. Santini.  Golgi Centennial Symposium: perspectives in neurobiology , 1978, Medical History.

[17]  I. Divac,et al.  Behavioral and anatomical consequences of small intrastriatal injections of kainic acid in the rat , 1978, Brain Research.

[18]  G. Winocur.  The hippocampus and cue utilization , 1980 .

[19]  L. Swanson,et al.  A direct projection from Ammon's horn to prefrontal cortex in the rat , 1981, Brain Research.

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

[21]  A. Siegel,et al.  A projection from the entorhinal cortex to the nucleus accumbens in the rat , 1981, Brain Research.

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

[23]  S. Iversen,et al.  Sensorimotor impairments following localized kainic acid and 6-hydroxydopamine lesions of the neostriatum , 1982, Brain Research.

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

[25]  S. Iversen,et al.  Neurotoxic lesions of ventrolateral but not anteromedial neostriatum in rats impair differential reinforcement of low rates (DRL) performance , 1982, Behavioural Brain Research.

[26]  M. Witter,et al.  Entorhinal efferents reach the caudato-putamen , 1983, Neuroscience Letters.

[27]  R. Sutherland,et al.  A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat , 1983, Behavioural Brain Research.

[28]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[29]  C. Gerfen.  The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems , 1984, Nature.

[30]  G. Hall,et al.  Response-reinforcer associations after caudate-putamen lesions in the rat: spatial discrimination and overshadowing-potentiation effects in instrumental learning. , 1985, Behavioral Neuroscience.

[31]  Response-reinforcer associations after caudate-putamen lesions in the rat: spatial discrimination and overshadowing-potentiation effects in instrumental learning. , 1985 .

[32]  L. Swanson,et al.  Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[34]  M. Witter,et al.  Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin , 1987, Neuroscience.

[35]  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.

[36]  C Ls Olson,et al.  Statistics: Making Sense of Data , 1987 .

[37]  D. Gaffan,et al.  Amygdalectomy and disconnection in visual learning for auditory secondary reinforcement by monkeys , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  G. Hall,et al.  Learning in rats with caudate-putamen lesions: unimpaired classical conditioning and beneficial effects of redundant stimulus cues on instrumental and spatial learning deficits. , 1988, Behavioral neuroscience.

[39]  D. Gaffan,et al.  Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  Learning in rats with caudate-putamen lesions: unimpaired classical conditioning and beneficial effects of redundant stimulus cues on instrumental and spatial learning deficits. , 1988, Behavioral neuroscience.

[41]  R. Sutherland,et al.  Contributions of cingulate cortex to two forms of spatial learning and memory , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  T. Robbins,et al.  Elementary processes of response selection mediated by distinct regions of the striatum , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  M. Packard,et al.  Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  N. White,et al.  Dissociation of visual and olfactory conditioning in the neostriatum of rats , 1989, Behavioural Brain Research.

[45]  R. Sutherland,et al.  The role of the fornix/fimbria and some related subcortical structures in place learning and memory , 1989, Behavioural Brain Research.

[46]  T. Jay,et al.  Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat , 1989, Brain Research.

[47]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[48]  B. Volpe,et al.  Allocentric spatial and tactile memory impairments in rats with dorsal caudate lesions are affected by preoperative behavioral training. , 1989, Behavioral neuroscience.

[49]  D. Gaffan,et al.  Visual-visual associative learning and reward-association learning in monkeys: the role of the amygdala , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[51]  N. White.  A functional hypothesis concerning the striatal matrix and patches: mediation of S-R memory and reward. , 1989, Life sciences.

[52]  A. Graybiel.  Neurotransmitters and neuromodulators in the basal ganglia , 1990, Trends in Neurosciences.

[53]  M. Pisa,et al.  Regionally selective roles of the rat's striatum in modality-specific discrimination learning and forelimb reaching , 1990, Behavioural Brain Research.

[54]  H. Groenewegen,et al.  The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. , 1990, Progress in brain research.

[55]  M. Glickstein,et al.  Afferent and Efferent Connections of Temporal Association Cortex in the Rat: A Horseradish Peroxidase Study , 1991, The European journal of neuroscience.

[56]  T. Robbins,et al.  Dissociable roles of the ventral, medial and lateral striatum on the acquisition and performance of a complex visual stimulus-response habit , 1991, Behavioural Brain Research.

[57]  M. Packard,et al.  Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists. , 1991, Behavioral neuroscience.

[58]  T. Robbins,et al.  The basolateral amygdala-ventral striatal system and conditioned place preference: Further evidence of limbic-striatal interactions underlying reward-related processes , 1991, Neuroscience.

[59]  T. Jay,et al.  Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris‐leucoagglutinin , 1991, The Journal of comparative neurology.

[60]  N. White,et al.  Localized intracaudate dopamine D2 receptor activation during the post-training period improves memory for visual or olfactory conditioned emotional responses in rats. , 1991, Behavioral and neural biology.

[61]  R. Skelton,et al.  Bilateral knife cuts to the perforant path disrupt spatial learning in the Morris water maze , 1992, Hippocampus.

[62]  D. S. Zahm,et al.  The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro‐gold , 1993, The Journal of comparative neurology.

[63]  R. J. McDonald,et al.  A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. , 1993, Behavioral neuroscience.

[64]  R. Sutherland,et al.  Posterior Cingulate Cortex and Spatial Memory: A Microlimnology Analysis , 1993 .

[65]  W. Hauber,et al.  Differential effects of lesions of the dorsomedial and dorsolateral caudate-putamen on reaction time performance in rats , 1994, Behavioural Brain Research.

[66]  James C. Houk,et al.  Elements of the Intrinsic Organization and Information Processing in the Neostriatum , 1994 .

[67]  R. J. McDonald,et al.  Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. , 1994, Behavioral and neural biology.

[68]  R. J. McDonald,et al.  Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. , 1994, Cerebral cortex.

[69]  M. Witter,et al.  The Rat Nervous System , 1995 .

[70]  R. J. McDonald,et al.  Hippocampal and nonhippocampal contributions to place learning in rats. , 1995, Behavioral neuroscience.

[71]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain , 1995, Hippocampus.

[72]  E. Audinat,et al.  Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents , 1995, The Journal of comparative neurology.

[73]  M. Gallagher,et al.  Entorhinal-perirhinal lesions impair performance of rats on two versions of place learning in the Morris water maze. , 1995, Behavioral neuroscience.

[74]  S. Dunnett,et al.  The Placement of a Striatal Ibotenic Acid Lesion Affects Skilled Forelimb Use and the Direction of Drug-Induced Rotation , 1996, Brain Research Bulletin.

[75]  D. Bilkey,et al.  Direct connection between perirhinal cortex and hippocampus is a major constituent of the lateral perforant path , 1998, Hippocampus.

[76]  J. D. McGaugh,et al.  Inactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning , 1996, Neurobiology of Learning and Memory.

[77]  H. L. Petri,et al.  Dissociation of Hippocampal and Striatal Contributions to Spatial Navigation in the Water Maze , 1996, Neurobiology of Learning and Memory.

[78]  M. Mazurek,et al.  Behavioral Characterization of Quinolinate-Induced Lesions of the Medial Striatum: Relevance for Huntington's Disease , 1996, Experimental Neurology.

[79]  D. Gaffan,et al.  Interaction of Perirhinal Cortex with the Fornix–Fimbria: Memory for Objects and “Object-in-Place” Memory , 1996, The Journal of Neuroscience.

[80]  N. White.  Mnemonic functions of the basal ganglia , 1997, Current Opinion in Neurobiology.

[81]  P. Holland,et al.  The Role of an Amygdalo-Nigrostriatal Pathway in Associative Learning , 1997, The Journal of Neuroscience.

[82]  J. Seamans,et al.  Selective Roles for Hippocampal, Prefrontal Cortical, and Ventral Striatal Circuits in Radial-Arm Maze Tasks With or Without a Delay , 1997, The Journal of Neuroscience.

[83]  Garrett E. Alexander.  Basal ganglia , 1998 .

[84]  R. J. McDonald,et al.  Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: relation to thigmotaxis , 1999, Behavioural Brain Research.