Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life

Damage to the hippocampus typically produces temporally graded retrograde amnesia, whereby memories acquired recently are impaired more than memories acquired remotely. This phenomenon has been demonstrated repeatedly in a variety of species and tasks, and it has figured prominently in theoretical treatments of memory and hippocampal function. A striking exception to the finding of temporally graded retrograde amnesia comes from studies with rodents using spatial tasks like the water maze. In these studies, recent and remote memory were similarly impaired following hippocampal lesions. In contrast to work with rodents, studies of patients with medial temporal lobe lesions, including complete hippocampal lesions, indicate that remote spatial memory can be intact. One difference between studies in humans and studies in rodents is that spatial memory in animal studies is acquired during a limited period of time when the animals are adults. In contrast, the spatial memory studied in humans was acquired beginning at an early age and learning continued for a considerable period of time. We initiated training in a standard water maze immediately after rats had been weaned at 21 days of age and continued training until the rats were young adults (90 days old). Large hippocampal lesions were made 100 days after the completion of training. After recovery from surgery, control rats exhibited good retention on the first retention probe trial, but rats with hippocampal lesions performed at chance. Thus, even after extended training beginning early in life, and with a prolonged training–surgery interval, hippocampal lesions impair performance in the water maze task. Possible reasons for these findings are discussed in the context of the specific performance requirements of the water maze task. Published 2005 Wiley‐Liss, Inc.

[1]  Morris Moscovitch,et al.  Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions , 2000, Nature Neuroscience.

[2]  Morris Moscovitch,et al.  Visual imagery deficits, impaired strategic retrieval, or memory loss: disentangling the nature of an amnesic person’s autobiographical memory deficit , 2004, Neuropsychologia.

[3]  E. Schuman,et al.  Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory , 2004, Nature.

[4]  Larry R Squire,et al.  Failure to acquire new semantic knowledge in patients with large medial temporal lobe lesions , 2005, Hippocampus.

[5]  Barbara J Knowlton,et al.  The hippocampus, consolidation and on-line memory , 1998, Current Opinion in Neurobiology.

[6]  Larry R. Squire,et al.  Memory for places learned long ago is intact after hippocampal damage , 1999, Nature.

[7]  J. Ramos Retrograde amnesia for spatial information: a dissociation between intra and extramaze cues following hippocampus lesions in rats , 1998, The European journal of neuroscience.

[8]  J. Bolhuis,et al.  Retrograde Amnesia and Memory Reactivation in Rats with Ibotenate Lesions to the Hippocampus or Subiculum , 1994, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[9]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[10]  M. Moser,et al.  Impaired Recognition of the Goal Location during Spatial Navigation in Rats with Hippocampal Lesions , 2001, The Journal of Neuroscience.

[11]  L. Squire,et al.  Retrograde amnesia and memory consolidation: a neurobiological perspective , 1995, Current Opinion in Neurobiology.

[12]  G. Winocur Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions , 1990, Behavioural Brain Research.

[13]  L R Squire,et al.  Retrograde amnesia † , 2001, Hippocampus.

[14]  Yutaka Kirino,et al.  Time-Dependent Reorganization of the Brain Components Underlying Memory Retention in Trace Eyeblink Conditioning , 2003, The Journal of Neuroscience.

[15]  S. J. Martin,et al.  Reversible neural inactivation reveals hippocampal participation in several memory processes , 1999, Nature Neuroscience.

[16]  Joseph R. Manns,et al.  Recognition Memory and the Human Hippocampus , 2003, Neuron.

[17]  Larry R Squire,et al.  Anterograde Amnesia and Temporally Graded Retrograde Amnesia for a Nonspatial Memory Task after Lesions of Hippocampus and Subiculum , 2002, The Journal of Neuroscience.

[18]  M. Fanselow,et al.  Temporally Graded Retrograde Amnesia of Contextual Fear after Hippocampal Damage in Rats: Within-Subjects Examination , 1999, The Journal of Neuroscience.

[19]  S H Salter,et al.  The Atlantis platform: a new design and further developments of Buresova's on-demand platform for the water maze. , 1994, Learning & memory.

[20]  Larry R Squire,et al.  Hippocampus and remote spatial memory in rats , 2005, Hippocampus.

[21]  D. Béracochéa,et al.  Extended temporal gradient for the retrograde and anterograde amnesia produced by ibotenate entorhinal cortex lesions in mice , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  E. Tulving,et al.  Long-lasting perceptual priming and semantic learning in amnesia: a case experiment. , 1991, Journal of experimental psychology. Learning, memory, and cognition.

[23]  R. Sutherland,et al.  Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks , 2001, Hippocampus.

[24]  J J Kim,et al.  Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. , 1995, Behavioral neuroscience.

[25]  Robert E. Clark,et al.  Medial Temporal Lobe Function and Memory. , 2004 .

[26]  M Moscovitch,et al.  Anterograde and retrograde amnesia in rats with large hippocampal lesions , 2001, Hippocampus.

[27]  Karen Zito,et al.  The Flip Side of Synapse Elimination , 2003, Neuron.

[28]  Robert S Astur,et al.  Retrograde amnesia and selective damage to the hippocampal formation: memory for places and object discriminations , 1999, Behavioural Brain Research.

[29]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[30]  Yutaka Kirino,et al.  Time-limited role of the hippocampus in the memory for trace eyeblink conditioning in mice , 2002, Brain Research.

[31]  Robert E. Clark,et al.  Impaired Recognition Memory in Rats after Damage to the Hippocampus , 2000, The Journal of Neuroscience.

[32]  D J Brooks,et al.  Temporally‐specific retrograde amnesia in two cases of discrete bilateral hippocampal pathology , 1999, Hippocampus.

[33]  B. Bontempi,et al.  Sites of Neocortical Reorganization Critical for Remote Spatial Memory , 2004, Science.