Hippocampal Volume Reduction in Humans Predicts Impaired Allocentric Spatial Memory in Virtual-Reality Navigation.
The extent to which navigational spatial memory depends on hippocampal integrity in humans is not well documented. We investigated allocentric spatial recall using a virtual environment in a group of patients with severe hippocampal damage (SHD), a group of patients with "moderate" hippocampal damage (MHD), and a normal control group. Through four learning blocks with feedback, participants learned the target locations of four different objects in a circular arena. Distal cues were present throughout the experiment to provide orientation. A circular boundary as well as an intra-arena landmark provided spatial reference frames. During a subsequent test phase, recall of all four objects was tested with only the boundary or the landmark being present. Patients with SHD were impaired in both phases of this task. Across groups, performance on both types of spatial recall was highly correlated with memory quotient (MQ), but not with intelligence quotient (IQ), age, or sex. However, both measures of spatial recall separated experimental groups beyond what would be expected based on MQ, a widely used measure of general memory function. Boundary-based and landmark-based spatial recall were both strongly related to bilateral hippocampal volumes, but not to volumes of the thalamus, putamen, pallidum, nucleus accumbens, or caudate nucleus. The results show that boundary-based and landmark-based allocentric spatial recall are similarly impaired in patients with SHD, that both types of recall are impaired beyond that predicted by MQ, and that recall deficits are best explained by a reduction in bilateral hippocampal volumes.


CONCLUSIONS
In humans, bilateral hippocampal atrophy can lead to profound impairments in episodic memory. Across species, perhaps the most well-established contribution of the hippocampus to memory is not to episodic memory generally but to allocentric spatial memory. However, the extent to which navigational spatial memory depends on hippocampal integrity in humans is not well documented. We investigated spatial recall using a virtual environment in two groups of patients with hippocampal damage (moderate/severe) and a normal control group. The results showed that patients with severe hippocampal damage are impaired in learning and recalling allocentric spatial information. Furthermore, hippocampal volume reduction impaired allocentric navigation beyond what can be predicted by memory quotient as a widely used measure of general memory function.
Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892, guderians@mail.nih.gov f.vargha-khadem@ucl.ac.uk.
Sebastian
S
Guderian
Cognitive Neuroscience and Neuropsychiatry Section, University College London Institute of Child Health, and Great Ormond Street Hospital, London WC1N 1EH, United Kingdom.
Anna M
http://orcid.org/0000-0002-6175-8742
AM
Dzieciol
Developmental Imaging and Biophysics Section, University College London Institute of Child Health, London WC1N 1EH, United Kingdom.
David G
DG
Gadian
Cluster "Languages of Emotion," Freie Universität Berlin, Berlin 14195, Germany.
Sebastian
http://orcid.org/0000-0003-2576-5432
S
Jentschke
Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands, and.
Christian F
CF
Doeller
Institute of Cognitive Neuroscience and Institute of Neurology, University College London, London WC1N 3AR, United Kingdom.
Neil
N
Burgess
Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892.
Mortimer
http://orcid.org/0000-0002-3050-9276
M
Mishkin
Cognitive Neuroscience and Neuropsychiatry Section, University College London Institute of Child Health, and Great Ormond Street Hospital, London WC1N 1EH, United Kingdom, guderians@mail.nih.gov f.vargha-khadem@ucl.ac.uk.
Faraneh
F
Vargha-Khadem
D000293:Adolescent; D000328:Adult; D000367:Age Factors; D001930:Brain Injuries / Q000150:complications* / Q000209:etiology / Q000473:pathology*; D002545:Brain Ischemia / Q000150:complications; D002648:Child; D005260:Female; D006624:Hippocampus / Q000473:pathology*; D006801:Humans; D007360:Intelligence; D008279:Magnetic Resonance Imaging; D008297:Male; D008569:Memory Disorders / Q000209:etiology*; D011939:Mental Recall; D012044:Regression Analysis; D065854:Spatial Navigation / Q000502:physiology*; D014584:User-Computer Interface; D055815:Young Adult
amnesia; human; memory; navigation; spatial; virtual reality