A Rapid, Hippocampus-Dependent, Item-Memory Signal that Initiates Context Memory in Humans

Summary The hippocampus, a structure located in the temporal lobes of the brain, is critical for the ability to recollect contextual details of past episodes. It is still debated whether the hippocampus also enables recognition memory for previously encountered context-free items. Brain imaging [1, 2] and neuropsychological patient studies [3, 4] have both individually provided conflicting answers to this question. We overcame the individual limitations of imaging and behavioral patient studies by combining them and observed a novel relationship between item memory and the hippocampus. We show that interindividual variability of hippocampal volumes in a large patient population with graded levels of hippocampal volume loss and controls correlates with context, but not item-memory performance. Nevertheless, concurrent measures of brain activity using magnetoencephalography reveal an early (350 ms) but sustained hippocampus-dependent signal that evolves from an item signal into a context memory signal. This is temporally distinct from an item-memory signal that is not hippocampus dependent. Thus, we provide evidence for a hippocampus-dependent item-memory process that initiates context retrieval without making a substantial contribution to item recognition performance. Our results reconcile contradictory evidence concerning hippocampal involvement in item memory and show that hippocampus-dependent mnemonic processes are more rapid than previously believed.

[1]  Mortimer Mishkin,et al.  Deferred Imitation of Action Sequences in Developmental Amnesia , 2005, Journal of Cognitive Neuroscience.

[2]  R. Clark,et al.  Recognition memory and the medial temporal lobe: a new perspective , 2007, Nature Reviews Neuroscience.

[3]  John T Wixted,et al.  A demonstration that the hippocampus supports both recollection and familiarity , 2009, Proceedings of the National Academy of Sciences.

[4]  Karen R. Brandt,et al.  Impairment of recollection but not familiarity in a case of developmental amnesia , 2009, Neurocase.

[5]  M. Mishkin,et al.  Developmental amnesia associated with early hypoxic-ischaemic injury. , 2000, Brain : a journal of neurology.

[6]  M Mishkin,et al.  Brain activity evidence for recognition without recollection after early hippocampal damage , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Rugg,et al.  Event-related potentials and recognition memory , 2007, Trends in Cognitive Sciences.

[8]  S. Köhler,et al.  Double dissociation of selective recollection and familiarity impairments following two different surgical treatments for temporal-lobe epilepsy , 2010, Neuropsychologia.

[9]  Zhuang Song,et al.  Impaired capacity for familiarity after hippocampal damage , 2011, Proceedings of the National Academy of Sciences.

[10]  R. Henson,et al.  Memory signals are temporally dissociated within and across human hippocampus and perirhinal cortex , 2012, Nature Neuroscience.

[11]  L. Squire,et al.  Recognition memory and the hippocampus: A test of the hippocampal contribution to recollection and familiarity. , 2010, Learning & memory.

[12]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[13]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[14]  A. Yonelinas Receiver-operating characteristics in recognition memory: evidence for a dual-process model. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[15]  Myra A. Fernandes,et al.  Neural correlates of recollection and familiarity: A review of neuroimaging and patient data , 2007, Neuropsychologia.

[16]  Larry R. Squire,et al.  In Search of Recollection and Familiarity Signals in the Hippocampus , 2010, Journal of Cognitive Neuroscience.

[17]  L. Squire,et al.  The cognitive neuroscience of human memory since H.M. , 2011, Annual review of neuroscience.

[18]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[20]  A. Yonelinas The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[21]  Peter E. Wais,et al.  The Hippocampus Supports both the Recollection and the Familiarity Components of Recognition Memory , 2006, Neuron.

[22]  Robert T. Knight,et al.  Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity , 2002, Nature Neuroscience.

[23]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[24]  Neil Burgess,et al.  Attractor Dynamics in the Hippocampal Representation of the Local Environment , 2005, Science.

[25]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[26]  John T Wixted,et al.  The Hippocampus Supports Both Recollection and Familiarity When Memories Are Strong , 2011, The Journal of Neuroscience.

[27]  Richard N. A. Henson,et al.  Electrophysiological correlates of masked face priming , 2008, NeuroImage.

[28]  Michael D. Rugg,et al.  Item memory, context memory and the hippocampus: fMRI evidence , 2012, Neuropsychologia.