Hippocampal damage equally impairs memory for single items and memory for conjunctions

In a prior study of continuous recognition performance, data were reported in support of the hypothesis that the hippocampus is not needed to remember the individual components of a stimulus but is important for remembering associations between its components (Kroll et al. 1996 . J Mem Lang 35:176–196). Patients with left hippocampal damage were able to endorse recently encountered words and to reject novel words, as well as disyllabic words in which one of the syllables had been previously encountered. However, they failed to reject words in which both syllables had been encountered independently in different words. We present data from five experiments designed to examine this finding in more detail. In each experiment, five patients with bilateral hippocampal damage and eight controls were tested using the same protocol as Kroll et al. ( 1996 ). On each trial, a two‐component stimulus was presented. Stimuli could be entirely novel, novel with one previously encountered (repeated) component, novel but with both components repeated, or a true repetition. The first experiment was a direct replication using the same disyllabic words as Kroll et al. ( 1996 ). The second experiment used pseudo‐words, constructed of two monosyllabic words (e.g., jambark). The third experiment used the same pairs of monosyllabic words, but presented separately on the screen to encourage participants to treat each component independently. The fourth experiment used pairs of objects, and the fifth experiment used face–house pairs. In all five experiments, patients with hippocampal damage exhibited impaired recognition memory. The impairment extended across all trial types with no evidence that hippocampal damage selectively (or disproportionately) impaired the associative or conjunctive component of memory. We discuss our findings in the light of the work by Kroll et al. ( 1996 ) and other recent neuropsychological, electrophysiological, and neuroimaging studies of hippocampal function and single‐item and associative memory. Hippocampus 2003;13:281–292. © 2003 Wiley‐Liss, Inc.

[1]  L. Squire,et al.  Perceptual learning, awareness, and the hippocampus , 2001, Hippocampus.

[2]  F. Craik,et al.  The Oxford handbook of memory , 2006 .

[3]  R. Sutherland,et al.  Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia , 1989, Psychobiology.

[4]  R. O’Reilly,et al.  Computational principles of learning in the neocortex and hippocampus , 2000, Hippocampus.

[5]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

[6]  L. Squire,et al.  Contrasting Effects on Discrimination Learning after Hippocampal Lesions and Conjoint Hippocampal–Caudate Lesions in Monkeys , 2000, The Journal of Neuroscience.

[7]  J K Adamowicz,et al.  Verbalization, cognitive effort, and heart rate alteration. , 1972, Canadian journal of psychology.

[8]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

[9]  E. Tulving Memory and consciousness. , 1985 .

[10]  R. O’Reilly,et al.  Conjunctive representations in learning and memory: principles of cortical and hippocampal function. , 2001, Psychological review.

[11]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[12]  L R Squire,et al.  Impaired transverse patterning in human amnesia is a special case of impaired memory for two-choice discrimination tasks. , 1999, Behavioral neuroscience.

[13]  D. Amaral,et al.  Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation , 1996, The Journal of Neuroscience.

[14]  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.

[15]  L. Squire,et al.  Simple and associative recognition memory in the hippocampal region. , 2001, Learning & memory.

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

[17]  L. Squire,et al.  Functional Magnetic Resonance Imaging (fMRI) Activity in the Hippocampal Region during Recognition Memory , 2000, The Journal of Neuroscience.

[18]  H G Wieser,et al.  Human hippocampus associates information in memory. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  B. Weber,et al.  Human hippocampus establishes associations in memory , 1997, Hippocampus.

[20]  H. Eichenbaum,et al.  The hippocampus and memory for orderly stimulus relations. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[21]  H. Eichenbaum,et al.  Conservation of hippocampal memory function in rats and humans , 1996, Nature.

[22]  L. Squire,et al.  Recognition memory and familiarity judgments in severe amnesia: no evidence for a contribution of repetition priming. , 2000, Behavioral neuroscience.

[23]  J W Rudy,et al.  A comparison of kainic acid plus colchicine and ibotenic acid-induced hippocampal formation damage on four configural tasks in rats. , 1995, Behavioral neuroscience.

[24]  J W Rudy,et al.  Rats with damage to the hippocampal-formation are impaired on the transverse-patterning problem but not on elemental discriminations. , 1995, Behavioral neuroscience.

[25]  David Wood,et al.  Luddites must not block progress in genetics , 1999, Nature.

[26]  Mortimer Mishkin,et al.  Preserved Recognition in a Case of Developmental Amnesia: Implications for the Acaquisition of Semantic Memory? , 2001, Journal of Cognitive Neuroscience.

[27]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[29]  L R Squire,et al.  Impaired recognition memory in patients with lesions limited to the hippocampal formation. , 1997, Behavioral neuroscience.

[30]  R. O’Reilly,et al.  Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. , 2003, Psychological review.

[31]  L R Squire,et al.  Impaired recognition memory on the doors and people test after damage limited to the hippocampal region , 1999, Hippocampus.

[32]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[33]  Robert T. Knight,et al.  Cohesion Failure as a Source of Memory Illusions , 1996 .

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

[35]  R. O’Reilly,et al.  Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? , 2002, Hippocampus.

[36]  R. Erickson,et al.  Clinical memory testing: a review. , 1977, Psychological bulletin.

[37]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.

[38]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[39]  M H Buonocore,et al.  Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study , 2001, Neuroreport.

[40]  L. Squire,et al.  Characterizing amnesic patients for neurobehavioral study. , 1986, Behavioral neuroscience.

[41]  J. Nagode,et al.  Human hippocampal activation during transitive inference , 2002, Neuroreport.

[42]  H Eichenbaum,et al.  The hippocampus and transverse patterning guided by olfactory cues. , 1998, Behavioral neuroscience.

[43]  H. Eichenbaum,et al.  The Neurophysiology of Memory , 2000, Annals of the New York Academy of Sciences.