A disconnection analysis of hippocampal function

A disconnection analysis determined the extent to which the fornix, hippocampus and entorhinal cortex are components of the same functional system in tasks that require working memory. Preoperatively, rats were trained to perform accurately on a radial arm maze. Then various combinations of unilateral and bilateral lesions were placed in the fornix and entorhinal cortex, either with or without a transection of the hippocampal commissures. When the lesions left intact at least one pathway through the hippocampus interconnecting the fornix and entorhinal cortex, rats performed normally. Either an uncrossed pathway (following a unilateral lesion of the fornix, transection of the hippocampal commissures, and an ipsilateral lesion of the entorhinal cortex) or a crossed pathway (following a unilateral lesion of the fornix and a contralateral lesion of the entorhinal cortex, leaving the hippocampal commissures intact) was sufficient. When the lesions produced a complete bilateral disconnection of the fornix and entorhinal cortex, rats performed poorly. The results indicate that the hippocampal system provides a functional connection between the subcortical structures associated with the fornix and the neocortical structures associated with the entorhinal cortex, and that without this connection normal processing of working memory can not occur.

[1]  Technique for producing directionally specific brain lesions with radio frequency current , 1975, Physiology & Behavior.

[2]  D. Olton,et al.  Cognitive mapping and hippocampal system function , 1981, Neuropsychologia.

[3]  N. Geschwind Disconnexion syndromes in animals and man. II. , 1965, Brain : a journal of neurology.

[4]  J. A. Horel,et al.  Visual discrimination impaired by cutting temporal lobe connections. , 1976, Science.

[5]  L. Swanson The anatomical organization of septo-hippocampal projections. , 1977, Ciba Foundation symposium.

[6]  G. Lynch,et al.  Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. , 1972, Brain research.

[7]  O. Steward,et al.  Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: open field activity and cue utilization following bilateral entorhinal cortex lesions , 1977, Brain Research Bulletin.

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

[9]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

[10]  D. Olton,et al.  Neuroanatomical bases of spatial memory , 1980, Brain Research.

[11]  D. Olton Mazes, maps, and memory. , 1979, The American psychologist.

[12]  T. Blackstad Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination , 1956, The Journal of comparative neurology.

[13]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[14]  J. Winson,et al.  Neuronal transmission through hippocampal pathways dependent on behavior. , 1978, Journal of neurophysiology.

[15]  G. Handelmann,et al.  Hippocampal function: Working memory or cognitive mapping? , 1980 .

[16]  N. Geschwind Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[17]  F. Gage,et al.  Hippocampal connections and spatial discrimination , 1978, Brain Research.

[18]  O. Steward,et al.  Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat , 1976, The Journal of comparative neurology.

[19]  A. Hjorth-Simonsen,et al.  Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation , 1972, The Journal of comparative neurology.

[20]  G. Handelmann,et al.  A re-examination of the role of hippocampus in working memory , 1979 .

[21]  W. K. Honig Spatial aspects of working memory , 1979 .

[22]  C. Shute,et al.  The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. , 1967, Brain : a journal of neurology.

[23]  K. Akert,et al.  Hippocampal seizure states in guinea pig. , 1955, Electroencephalography and clinical neurophysiology.

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

[25]  L. Jarrard Anatomical and behavioral analysis of hippocampal cell fields in rats. , 1976, Journal of comparative and physiological psychology.

[26]  D. Olton Discrimination reversal performance after hippocampal lesions: an enduring failure of reinforcement and non-reinforcement to direct behavior. , 1972, Physiology & behavior.

[27]  J. A. Horel,et al.  Somatosensory deficit produced by parietal-temporal cortical disconnection in the monkey. , 1971, Experimental neurology.

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

[29]  L. Jarrard Selective hippocampal lesions and behavior , 1980 .

[30]  O. Steward,et al.  Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: Recovery of alternation performance following unilateral entorhinal cortex lesions , 1977, Brain Research Bulletin.

[31]  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.

[32]  P. Andersen Organization of Hippocampal Neurons and Their Interconnections , 1975 .

[33]  D. Olton,et al.  Spatial memory deficit following fimbria-fornix lesions: Independent of time for stimulus processing , 1979, Physiology & Behavior.

[34]  G. Lynch,et al.  The Hippocampus as a Model for Studying Anatomical Plasticity in the Adult Brain , 1975 .

[35]  D. Olton,et al.  Hippocampal function and behavior: Spatial discrimination and response inhibition , 1978, Physiology & Behavior.

[36]  David S. Olton,et al.  Spatial memory following damage to hippocampal CA3 pyramidal cells with kainic acid: impairment and recovery with preoperative training , 1981, Brain Research.

[37]  L. Jarrard,et al.  Selective hippocampal lesions: differential effects on performance by rats of a spatial task with preoperative versus postoperative training. , 1978, Journal of comparative and physiological psychology.

[38]  S. Nakajima Hippocampal Protein Synthesis and Spike Discharges in Relation to Memory , 1975 .

[39]  R. Chronister,et al.  Fiberarchitecture of the Hippocampal Formation: Anatomy, Projections, and Structural Significance , 1975 .

[40]  P Andersen,et al.  Entorhinal activation of dentate granule cells. , 1966, Acta physiologica Scandinavica.

[41]  O. Steward,et al.  Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat , 1976, The Journal of comparative neurology.

[42]  F. Gage,et al.  Damage to hippocampus and hippocampal connections: effects on DRL and spontaneous alternation. , 1977, Journal of comparative and physiological psychology.

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

[44]  D. Olton,et al.  Spatial memory and hippocampal function , 1979, Neuropsychologia.