Human Hippocampal and Parahippocampal Activity during Visual Associative Recognition Memory for Spatial and Nonspatial Stimulus Configurations

Evidence from animal studies points to the importance of the parahippocampal region (PHR) [including entorhinal, perirhinal, and parahippocampal (PHC) cortices] for recognition of visual stimuli. Recent findings in animals suggest that PHR may also be involved in visual associative recognition memory for configurations of stimuli. Thus far, however, such involvement has not been demonstrated in humans. In fact, it has been argued that associative recognition in humans is critically dependent on the hippocampal formation (HF). To better understand the division of function between HF and PHR during recognition memory in humans, we measured the activity of both areas in healthy young adults during an associative recognition memory task using functional magnetic resonance imaging. To more precisely characterize the nature of the associations that might be coded by the HF and PHR during recognition, subjects were required to learn and were later tested for associations based on either the spatial arrangements of two stimuli or the identity of two stimuli (a face and a tool). An area in the PHC was found to be more active for recognized old configurations than new configurations in both the spatial and identity conditions. The HF, on the other hand, was more active for recognition of new configurations than old configurations and also more active in the spatial than the identity condition. These data highlight the involvement of PHR in the long-term coding of associative relationships between stimuli and help to clarify the nature of its functional distinction from the HF.

[1]  Alan C. Evans,et al.  Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus. , 2002, Cerebral cortex.

[2]  R. Desimone,et al.  Responses of Macaque Perirhinal Neurons during and after Visual Stimulus Association Learning , 1999, The Journal of Neuroscience.

[3]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

[4]  Malcolm W. Brown,et al.  Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory , 1999, The Journal of Neuroscience.

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

[6]  L. Saksida,et al.  ã Federation of European Neuroscience Societies Perirhinal cortex resolves feature ambiguity in complex visual discriminations , 2022 .

[7]  E. Rolls,et al.  Selective Perceptual Impairments After Perirhinal Cortex Ablation , 2001, The Journal of Neuroscience.

[8]  K Sakai,et al.  Neuronal tuning and associative mechanisms in form representation. , 1994, Learning & memory.

[9]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[10]  J. Aggleton,et al.  A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage , 2000, Neuropsychologia.

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

[12]  T. Bussey,et al.  Perceptual–mnemonic functions of the perirhinal cortex , 1999, Trends in Cognitive Sciences.

[13]  M. W. Brown,et al.  Recognition memory: neuronal substrates of the judgement of prior occurrence , 1998, Progress in Neurobiology.

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

[15]  H. Eichenbaum.  The hippocampus and declarative memory: cognitive mechanisms and neural codes , 2001, Behavioural Brain Research.

[16]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  E. Maguire,et al.  A Temporoparietal and Prefrontal Network for Retrieving the Spatial Context of Lifelike Events , 2001, NeuroImage.

[18]  H. Eichenbaum,et al.  Hippocampal Neurons Encode Information about Different Types of Memory Episodes Occurring in the Same Location , 2000, Neuron.

[19]  G. Rainer,et al.  Cognitive neuroscience: Neural mechanisms for detecting and remembering novel events , 2003, Nature Reviews Neuroscience.

[20]  M. Mishkin,et al.  One-Trial Memory for Object-Place Associations after Separate Lesions of Hippocampus and Posterior Parahippocampal Region in the Monkey , 2003, The Journal of Neuroscience.

[21]  Y. Miyashita,et al.  Backward spreading of memory-retrieval signal in the primate temporal cortex. , 2001, Science.

[22]  R. Henson,et al.  A familiarity signal in human anterior medial temporal cortex? , 2003, Hippocampus.

[23]  N Burgess,et al.  Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching , 2001, Hippocampus.

[24]  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.

[25]  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.

[26]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

[27]  Yasushi Miyashita,et al.  Forward Processing of Long-Term Associative Memory in Monkey Inferotemporal Cortex , 2003, The Journal of Neuroscience.

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

[29]  D G Gadian,et al.  Amnesia and the organization of the hippocampal system , 1998, Hippocampus.

[30]  L. Squire,et al.  Neuronal representations of stimulus associations develop in the temporal lobe during learning , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  M. Moscovitch,et al.  Distinct neural correlates of visual long-term memory for spatial location and object identity: a positron emission tomography study in humans. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[32]  L. Squire,et al.  FMRI activity in the medial temporal lobe during recognition memory as a function of study‐test interval , 2000, Hippocampus.

[33]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[34]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain , 1995, Hippocampus.

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

[36]  M. W. Brown,et al.  Neuronal signals of importance to the performance of visual recognition memory tasks: evidence from recordings of single neurones in the medial thalamus of primates. , 1993, Progress in brain research.

[37]  M. Mishkin,et al.  Object Recognition and Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala and Hippocampus , 1998, The Journal of Neuroscience.

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

[39]  L. Saksida,et al.  Impairments in visual discrimination after perirhinal cortex lesions: testing ‘declarative’ vs. ‘perceptual‐mnemonic’ views of perirhinal cortex function , 2003, The European journal of neuroscience.

[40]  M. Mishkin,et al.  Learning increases stimulus salience in anterior inferior temporal cortex of the macaque. , 2001, Journal of neurophysiology.

[41]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

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

[43]  D G Gadian,et al.  Hierarchical organization of cognitive memory. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[44]  Adam N Mamelak,et al.  Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task , 2002, Behavioural Brain Research.

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