Content-specificity of the neural correlates of recollection

It is widely assumed that episodic retrieval (recollection) involves reinstatement of cortical activity engaged during the processing of an episode when it was initially experienced. It follows from this assumption that the cortical correlates of recollection should differ with the content of what is recollected, and that retrieval of different content should be associated with activity in functionally distinct cortical regions. The present experiment investigated these predictions. Subjects (N=17) studied a mixed list of words and pictures and were then presented with a test list comprised of words only. Test items were studied words, the names of studied pictures, and unstudied (new) words. Functional magnetic resonance images were acquired while the subjects made Remember/Know/New judgments to these test words. Independent of study material, studied items endorsed as Remembered elicited greater activity than correctly classified unstudied items in several regions, including left frontal, left lateral parietal, and posterior cingulate cortex. In addition, Remembered items elicited greater activity in the right hippocampus and parahippocampal gyrus than items accorded Know judgments, replicating previous findings. Analysis of content-specific effects demonstrated a regional double-dissociation within left fusiform cortex; recollected words elicited greater activity than recollected pictures in lateral fusiform, whereas the reverse effect was evident in an anterior fusiform region. The lateral and anterior fusiform areas correspond closely to areas held to be functionally specialized for the processing of visual words and pictures, respectively. Thus, the current findings support the cortical reinstatement hypothesis of episodic retrieval.

[1]  Michael D Rugg,et al.  Electrophysiological dissociation of retrieval orientation and retrieval effort , 2002, Psychonomic bulletin & review.

[2]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

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

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

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

[6]  R. Buckner,et al.  Functional Dissociation among Components of Remembering: Control, Perceived Oldness, and Content , 2003, The Journal of Neuroscience.

[7]  L. Shastri Episodic memory and cortico–hippocampal interactions , 2002, Trends in Cognitive Sciences.

[8]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Applications , 2002, NeuroImage.

[9]  Michael D Rugg,et al.  Remembrance of Odors Past Human Olfactory Cortex in Cross-Modal Recognition Memory , 2004, Neuron.

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

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

[12]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

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

[14]  M. Hasselmo,et al.  The hippocampus as an associator of discontiguous events , 1998, Trends in Neurosciences.

[15]  John E Desmond,et al.  Evidence for cortical encoding specificity in episodic memory: memory-induced re-activation of picture processing areas , 2002, Neuropsychologia.

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

[17]  Pierre Maquet,et al.  Brain activity underlying encoding and retrieval of source memory. , 2002, Cerebral cortex.

[18]  L Nyberg,et al.  Conjunction analysis of cortical activations common to encoding and retrieval , 2000, Microscopy research and technique.

[19]  E. Tulving,et al.  Reactivation of encoding-related brain activity during memory retrieval. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[20]  P Alvarez,et al.  Memory consolidation and the medial temporal lobe: a simple network model. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[21]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

[22]  Suparna Rajaram,et al.  Remembering and knowing: Two means of access to the personal past , 1993, Memory & cognition.

[23]  R. Buckner,et al.  Neural Correlates of Episodic Retrieval Success , 2000, NeuroImage.

[24]  E. Rolls,et al.  Hippocampo‐cortical and cortico‐cortical backprojections , 2000, Hippocampus.

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

[26]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[27]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Lars-Göran Nilsson,et al.  Reactivation of Motor Brain Areas during Explicit Memory for Actions , 2001, NeuroImage.

[29]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[30]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[32]  Leif R. Hedman,et al.  The picture superiority effect in a cross-modality recognition task , 1995, Memory & cognition.

[33]  M D Rugg Convergent approaches to electrophysiological and hemodynamic investigations of memory , 1998, Human brain mapping.

[34]  D C Rubin,et al.  Visual memory-deficit amnesia: a distinct amnesic presentation and etiology. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  T. Bussey,et al.  The cognitive neuroscience of memory : encoding and retrieval , 2002 .

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

[37]  Rugg,et al.  Episodic memory retrieval: an (event-related) functional neuroimaging perspective , 2002 .

[38]  R. Henson,et al.  Neural correlates of retrieval processing in the prefrontal cortex during recognition and exclusion tasks , 2003, Neuropsychologia.

[39]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Rugg,et al.  Human recognition memory: a cognitive neuroscience perspective , 2003, Trends in Cognitive Sciences.

[41]  C. Stark,et al.  Making Memories without Trying: Medial Temporal Lobe Activity Associated with Incidental Memory Formation during Recognition , 2003, The Journal of Neuroscience.

[42]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

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

[44]  Anthony D Wagner,et al.  Memory orientation and success: separable neurocognitive components underlying episodic recognition , 2003, Neuropsychologia.

[45]  S. Dehaene,et al.  Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. , 2002, Brain : a journal of neurology.

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