Distinct brain networks in recognition memory share a defined region in the precuneus

Current models of recognition memory performance postulate that there are two fundamentally distinct retrieval processes, i.e. recollection and familiarity. This view has been challenged and little is known from human research about the functional connectivity of the brain areas involved in these processes. In our study we used a Remember‐Know procedure to assess the functional connectivity of brain regions under recognition memory in 30 healthy adults. Using functional magnetic resonance imaging, we analysed the blood oxygen level‐dependent responses during correct Remember, correct Know, correct Rejection and missed responses of the subjects during recognition of non‐emotional nouns. One activation cluster was found in the left precuneus associated with both recollection and familiarity answers. To acquire information about the way in which activity in one brain region modulates activity in another brain region in response to the active task, we performed a psychophysiological interaction analysis with the left precuneus as a seed region. This analysis revealed functionally distinct networks of brain areas underlying recollection and familiarity. Furthermore, we discuss the differential involvement of the hippocampus in a recollection network as compared with a familiarity network. In summary, our results further strengthen the assumptions of a dual‐process view of recognition memory [e.g. H. Eichenbaum et al. (2007) Annual Review of Neuroscience, 30, 123–152; A.P. Yonelinas (2001) Philosophical Transactions of the Royal Society London B Biological Sciences, 356, 1363–1374] and add empirical findings about the functional interconnectivity of brain regions supporting either recollection or familiarity.

[1]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[2]  P. Fransson Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[3]  Benjamin J. Shannon,et al.  Coherent spontaneous activity identifies a hippocampal-parietal memory network. , 2006, Journal of neurophysiology.

[4]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[5]  J. H. Steiger Tests for comparing elements of a correlation matrix. , 1980 .

[6]  B. Gulyás,et al.  Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. , 1995, Cerebral cortex.

[7]  Alan Richardson-Klavehn,et al.  Recognition memory and decision processes: A meta-analysis of remember, know, and guess responses , 2002, Memory.

[8]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[9]  Andrew P. Yonelinas,et al.  Perirhinal Cortex Supports Encoding and Familiarity-Based Recognition of Novel Associations , 2008, Neuron.

[10]  Kaia L. Vilberg,et al.  Memory retrieval and the parietal cortex: A review of evidence from a dual-process perspective , 2008, Neuropsychologia.

[11]  Barbara J Knowlton,et al.  The effect of testing procedure on remember-know judgments , 2002, Psychonomic bulletin & review.

[12]  J. Fuster,et al.  Visuo-tactile cross-modal associations in cortical somatosensory cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Binder,et al.  A Parametric Manipulation of Factors Affecting Task-induced Deactivation in Functional Neuroimaging , 2003, Journal of Cognitive Neuroscience.

[14]  M. W. Brown,et al.  Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe , 1998, Neuropharmacology.

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

[16]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[17]  L. Jacoby A process dissociation framework: Separating automatic from intentional uses of memory , 1991 .

[18]  L. Nyberg,et al.  Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration? , 2005, Consciousness and Cognition.

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

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

[21]  I. Daum,et al.  Associations evoked during memory encoding recruit the context‐network , 2009, Hippocampus.

[22]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[23]  T. Shallice,et al.  Confidence in Recognition Memory for Words: Dissociating Right Prefrontal Roles in Episodic Retrieval , 2000, Journal of Cognitive Neuroscience.

[24]  John P. Aggleton,et al.  Interleaving brain systems for episodic and recognition memory , 2006, Trends in Cognitive Sciences.

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

[26]  Edward Bullmore,et al.  The neural correlates of intentional and incidental self processing , 2002, Neuropsychologia.

[27]  H. Heinze,et al.  Recapitulating emotional context: activity of amygdala, hippocampus and fusiform cortex during recollection and familiarity , 2005, The European journal of neuroscience.

[28]  R. Cabeza,et al.  Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[30]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[31]  Peter Fransson,et al.  The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis , 2008, NeuroImage.

[32]  Colleen M. Parks,et al.  Moving beyond pure signal-detection models: comment on Wixted (2007). , 2007, Psychological review.

[33]  J. Wixted Dual-process theory and signal-detection theory of recognition memory. , 2007, Psychological review.

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

[35]  M. Rugg,et al.  Separating the Brain Regions Involved in Recollection and Familiarity in Recognition Memory , 2005, The Journal of Neuroscience.

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

[37]  Mark E Wheeler,et al.  Functional-anatomic correlates of remembering and knowing , 2004, NeuroImage.

[38]  S. Petersen,et al.  Functional Anatomic Studies of Memory Retrieval for Auditory Words and Visual Pictures , 1996, The Journal of Neuroscience.

[39]  Richard S. J. Frackowiak,et al.  The Mind's Eye—Precuneus Activation in Memory-Related Imagery , 1995, NeuroImage.

[40]  R. Marsh,et al.  Remember-know judgments can depend on how memory is tested , 1999, Psychonomic bulletin & review.

[41]  Julie A Fiez,et al.  Functional dissociations within the inferior parietal cortex in verbal working memory , 2004, NeuroImage.

[42]  Michael D. Rugg,et al.  Dissociation of the neural correlates of recognition memory according to familiarity, recollection, and amount of recollected information , 2007, Neuropsychologia.

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

[44]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[45]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[46]  L. Davachi,et al.  Behavioral/systems/cognitive Functional–neuroanatomic Correlates of Recollection: Implications for Models of Recognition Memory , 2022 .

[47]  G. Mandler Recognizing: The judgment of previous occurrence. , 1980 .

[48]  John T Wixted,et al.  Activity in the Medial Temporal Lobe Predicts Memory Strength, Whereas Activity in the Prefrontal Cortex Predicts Recollection , 2008, The Journal of Neuroscience.

[49]  Michael D. Rugg,et al.  Content-specificity of the neural correlates of recollection , 2005, Neuropsychologia.

[50]  Karl Magnus Petersson,et al.  The role of precuneus and left inferior frontal cortex during source memory episodic retrieval , 2005, NeuroImage.

[51]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

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

[53]  A. Ishai,et al.  Recollection- and Familiarity-Based Decisions Reflect Memory Strength , 2008, Frontiers in systems neuroscience.

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

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

[56]  A. Yonelinas Components of episodic memory: the contribution of recollection and familiarity. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[57]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[58]  R. Cabeza,et al.  Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. , 2006, Journal of neurophysiology.

[59]  Richard S. J. Frackowiak,et al.  Brain regions associated with acquisition and retrieval of verbal episodic memory , 1994, Nature.

[60]  Norbert Victor,et al.  Verfahrensbibliothek Versuchsplanung und -auswertung. , 1996 .

[61]  L. Cohen,et al.  The role of the supplementary motor area (SMA) in word production , 2006, Brain Research.

[62]  Kenichi Ohki,et al.  Dissociated pathways for successful memory retrieval from the human parietal cortex: anatomical and functional connectivity analyses. , 2008, Cerebral cortex.

[63]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

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

[65]  Andrew P. Yonelinas,et al.  Sparing of the familiarity component of recognition memory in a patient with hippocampal pathology , 2005, Neuropsychologia.

[66]  Jesper Andersson,et al.  Isolating the retrieval of imagined pictures during episodic memory: activation of the left precuneus and left prefrontal cortex , 2003, NeuroImage.

[67]  R. Knight,et al.  The functional neuroanatomy of working memory: Contributions of human brain lesion studies , 2006, Neuroscience.

[68]  A R McIntosh,et al.  Functional interactions between the medial temporal lobes and posterior neocortex related to episodic memory retrieval. , 1998, Cerebral cortex.

[69]  C. Caltagirone,et al.  Recollection and familiarity in hippocampal amnesia , 2008, Hippocampus.

[70]  Sabrina M. Tom,et al.  Dissociable correlates of recollection and familiarity within the medial temporal lobes , 2004, Neuropsychologia.

[71]  I. Tendolkar,et al.  The rhinal cortex: ‘gatekeeper’ of the declarative memory system , 2006, Trends in Cognitive Sciences.

[72]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[73]  J. Voogd,et al.  The Human Central Nervous System , 1978, Springer Berlin Heidelberg.

[74]  D. Montaldi,et al.  The neural system that mediates familiarity memory , 2006, Hippocampus.

[75]  Andrew P. Yonelinas,et al.  Separating conscious and unconscious influences of memory: measuring recollection , 1993 .

[76]  Craig J. Brozinsky,et al.  Functional connectivity with the hippocampus during successful memory formation , 2005, Hippocampus.

[77]  Koji Jimura,et al.  Activation shift from medial to lateral temporal cortex associated with recency judgements following impoverished encoding. , 2006, Cerebral cortex.

[78]  Yael Shrager,et al.  Activity in Both Hippocampus and Perirhinal Cortex Predicts the Memory Strength of Subsequently Remembered Information , 2008, Neuron.

[79]  F L Bookstein,et al.  Differential functional connectivity of prefrontal and medial temporal cortices during episodic memory retrieval , 1997, Human brain mapping.

[80]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.