Interaction between the Human Hippocampus and the Caudate Nucleus during Route Recognition

Navigation through familiar environments can rely upon distinct neural representations that are related to different memory systems with either the hippocampus or the caudate nucleus at their core. However, it is a fundamental question whether and how these systems interact during route recognition. To address this issue, we combined a functional neuroimaging approach with a naturally occurring, well-controlled human model of caudate nucleus dysfunction (i.e., preclinical and early-stage Huntington's disease). Our results reveal a noncompetitive interaction so that the hippocampus compensates for gradual caudate nucleus dysfunction with a gradual activity increase, maintaining normal behavior. Furthermore, we revealed an interaction between medial temporal and caudate activity in healthy subjects, which was adaptively modified in Huntington patients to allow compensatory hippocampal processing. Thus, the two memory systems contribute in a noncompetitive, cooperative manner to route recognition, which enables the hippocampus to compensate seamlessly for the functional degradation of the caudate nucleus.

[1]  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.

[2]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[3]  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.

[4]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[5]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

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

[7]  R. J. McDonald,et al.  Multiple Parallel Memory Systems in the Brain of the Rat , 2002, Neurobiology of Learning and Memory.

[8]  L. Nadel,et al.  Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex , 1998, Neuropsychologia.

[9]  M. Gluck,et al.  Interactive memory systems in the human brain , 2001, Nature.

[10]  John J. B. Allen,et al.  Memory Deficits Characterized by Patterns of Lesions to the Hippocampus and Parahippocampal Cortex , 2000, Annals of the New York Academy of Sciences.

[11]  B. Harper.  Huntington Disease , 2005, Journal of the Royal Society of Medicine.

[12]  J. D. McGaugh,et al.  Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. , 1992, Behavioral neuroscience.

[13]  David Wechsler,et al.  Wechsler Memory scale. , 2005 .

[14]  Peter S. Harper,et al.  Huntington's disease , 1991 .

[15]  J M Ramos,et al.  Long‐term spatial memory in rats with hippocampal lesions , 2000, The European journal of neuroscience.

[16]  A. Dagher,et al.  The role of the striatum and hippocampus in planning: a PET activation study in Parkinson's disease. , 2001, Brain : a journal of neurology.

[17]  Jane S. Paulsen,et al.  Unified Huntington's disease rating scale: Reliability and consistency , 1996, Movement disorders : official journal of the Movement Disorder Society.

[18]  Nancy D. Chiaravalloti,et al.  The Wechsler Memory Scale, Third Edition: A New Perspective , 2003 .

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

[20]  E. Maguire,et al.  The Well-Worn Route and the Path Less Traveled Distinct Neural Bases of Route Following and Wayfinding in Humans , 2003, Neuron.

[21]  H Eichenbaum,et al.  Functional organization of the hippocampal memory system. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[22]  P. S. Achilles.  THE PSYCHOLOGICAL CORPORATION. , 1923, Science.

[23]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

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

[25]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[26]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[27]  R. Turner,et al.  Characterizing Dynamic Brain Responses with fMRI: A Multivariate Approach , 1995, NeuroImage.

[28]  D. Wechsler.  Wechsler Adult Intelligence Scale , 2021, Encyclopedia of Evolutionary Psychological Science.

[29]  J. Gabrieli.  Cognitive neuroscience of human memory. , 1998, Annual review of psychology.

[30]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[31]  Jane S. Paulsen,et al.  Unified Huntington's disease rating scale: Reliability and consistency , 1996, Movement disorders : official journal of the Movement Disorder Society.

[32]  Hippocampal and nonhippocampal contributions to place learning in rats. , 1995 .

[33]  R. Poldrack,et al.  Competition among multiple memory systems: converging evidence from animal and human brain studies , 2003, Neuropsychologia.

[34]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[35]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[36]  M. Potegal.  The caudate nucleus egocentric localization system. , 1972, Acta neurobiologiae experimentalis.

[37]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[38]  Edie M. Rasmussen,et al.  Parallel Information Processing. , 1992 .

[39]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[40]  A. Cools,et al.  Memory and learning strategies in patients with Parkinson's disease , 1994, Neuropsychologia.

[41]  N. White,et al.  Parallel Information Processing in the Dorsal Striatum: Relation to Hippocampal Function , 1999, The Journal of Neuroscience.

[42]  G Pearlson,et al.  Bicaudate ratio as a measure of caudate volume on MR images. , 1991, AJNR. American journal of neuroradiology.

[43]  M. Petrides,et al.  Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice , 2003, The Journal of Neuroscience.