The Role of VMPC in Metamemorial Judgments of Content Retrievability

Making judgments about the retrievability of information is a critical part of the metamemory processes engaged during remembering. A recent study of patients with frontal lesions suggests that ventral medial prefrontal cortex (VMPC) plays a critical role in such judgments [Schnyer, D. M., Verfaellie, M., Alexander, M. P., Lafleche, G., Nicholls, L., & Kaszniak, A. W. A role for right medial prefrontal cortex in accurate feeling of knowing judgments: Evidence from patients with lesions to frontal cortex. Neuropsychologia, 42, 957966, 2004]. The observed impairment was thought to reflect an inability to determine the accessibility of memory contents. To further examine the neuroanatomical basis of content accessibility assessment, we used fMRI in an episodic feeling-of-knowing (FOK) paradigm. Participants were asked to make trial-by-trial predictions about the retrievability of the final word that completed studied sentences and then to select the correct completion from among alternatives. Results indicated that the VMPC is engaged during accurate FOK judgments and its activation is modulated by retrieval rating. Structural equations modeling supported the notion that VMPC, as part of a broader left hemisphere network involved in memory retrieval, monitors the output of the retrieval process. More generally, VMPC may participate in metacognitive processes that allow for the comparison of available data against an internal model.

[1]  T. O. Nelson Metamemory: A Theoretical Framework and New Findings , 1990 .

[2]  D. Schacter,et al.  Can medial temporal lobe regions distinguish true from false? An event-related functional MRI study of veridical and illusory recognition memory , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Steven H. Stein,et al.  The Human Frontal Lobes: Functions and Disorders , 2000 .

[4]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[5]  D Yves von Cramon,et al.  Decision-making and the frontal lobes , 2006, Current opinion in neurology.

[6]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[7]  M. Mishkin,et al.  The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. , 2001, Brain : a journal of neurology.

[8]  Armin Schnider,et al.  Spontaneous confabulators fail to suppress currently irrelevant memory traces , 1999, Nature Neuroscience.

[9]  A. Koriat How do we know that we know? The accessibility model of the feeling of knowing. , 1993 .

[10]  Christian Büchel,et al.  Neural correlates of memory confidence , 2006, NeuroImage.

[11]  L R Squire,et al.  Memory and metamemory: a study of the feeling-of-knowing phenomenon in amnesic patients. , 1986, Journal of experimental psychology. Learning, memory, and cognition.

[12]  S. Becker,et al.  A Computational Model of Prefrontal Control in Free Recall: Strategic Memory Use in the California Verbal Learning Task , 2003, Journal of Cognitive Neuroscience.

[13]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[14]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[15]  Jason P. Mitchell,et al.  Feeling-of-knowing in episodic memory: an event-related fMRI study , 2003, NeuroImage.

[16]  I. Fischler,et al.  Completion norms for 329 sentence contexts , 1980, Memory & cognition.

[17]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[18]  Stephen D. Christman,et al.  A Neuropsychological Dimension for Anchoring Effects , 2005 .

[19]  M. Isingrini,et al.  Aging, episodic memory feeling-of-knowing, and frontal functioning. , 2000, Neuropsychology.

[20]  Morris Moscovitch,et al.  The frontal cortex and working with memory , 2002 .

[21]  Gregory Schraw,et al.  Measures of feeling-of-knowing accuracy: A new look at an old problem , 1995 .

[22]  Arthur P. Shimamura,et al.  Memory and metamemory: Comparisons between patients with frontal lobe lesions and amnesic patients , 1989, Psychobiology.

[23]  D. Pandya,et al.  Association pathways of the prefrontal cortex and functional observations , 2002 .

[24]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

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

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

[27]  Marcia K. Johnson,et al.  The role of prefrontal cortex during tests of episodic memory , 1998, Trends in Cognitive Sciences.

[28]  L. Reder Strategy selection in question answering , 1987, Cognitive Psychology.

[29]  Larry Cahill,et al.  Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage , 2003, NeuroImage.

[30]  R. Turner,et al.  Detecting Latency Differences in Event-Related BOLD Responses: Application to Words versus Nonwords and Initial versus Repeated Face Presentations , 2002, NeuroImage.

[31]  M. Alexander,et al.  A role for right medial prefrontal cortex in accurate feeling-of-knowing judgments: evidence from patients with lesions to frontal cortex , 2004, Neuropsychologia.

[32]  B. Mesquita,et al.  The experience of emotion. , 2007, Annual review of psychology.

[33]  Rugg,et al.  Recollection and familiarity in recognition memory: an event-related fMRI study , 1999 .

[34]  Daniel L. Schacter,et al.  Understanding metamemory: Neural correlates of the cognitive process and subjective level of confidence in recognition memory , 2006, NeuroImage.

[35]  H. Spiers,et al.  Prefrontal and medial temporal lobe interactions in long-term memory , 2003, Nature Reviews Neuroscience.

[36]  F. Gonzalez-Lima,et al.  Structural equation modeling and its application to network analysis in functional brain imaging , 1994 .

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

[38]  J Metcalfe Novelty monitoring, metacognition, and control in a composite holographic associative recall model: implications for Korsakoff amnesia. , 1993, Psychological review.

[39]  Randy L Buckner,et al.  Functional–Anatomic Correlates of Control Processes in Memory , 2003, The Journal of Neuroscience.

[40]  M. Woldorff,et al.  Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. , 2004, Cerebral cortex.

[41]  A Koriat,et al.  The combined contributions of the cue-familiarity and accessibility heuristics to feelings of knowing. , 2001, Journal of experimental psychology. Learning, memory, and cognition.

[42]  Cheryl L. Grady,et al.  Neuroimaging and activation of the frontal lobes. , 1999 .

[43]  Anthony D Wagner,et al.  Executive Control during Episodic Retrieval Multiple Prefrontal Processes Subserve Source Memory , 2002, Neuron.

[44]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[45]  Michel Isingrini,et al.  Diminished episodic memory awareness in older adults: Evidence from feeling-of-knowing and recollection , 2007, Consciousness and Cognition.

[46]  P. Bentler,et al.  Comparative fit indexes in structural models. , 1990, Psychological bulletin.

[47]  A R McIntosh,et al.  Neural correlates of the episodic encoding of pictures and words. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  H. Akaike,et al.  Information Theory and an Extension of the Maximum Likelihood Principle , 1973 .

[49]  L. Reder,et al.  What determines initial feeling of knowing? Familiarity with question terms, not with the answer , 1992 .

[50]  John D E Gabrieli,et al.  Neural correlates of actual and predicted memory formation , 2005, Nature Neuroscience.

[51]  Asher Koriat,et al.  The Feeling of Knowing: Some Metatheoretical Implications for Consciousness and Control , 2000, Consciousness and Cognition.

[52]  T Shallice,et al.  'Theory of mind' and the prefrontal cortex. , 2001, Brain : a journal of neurology.

[53]  Kenichi Ohki,et al.  Neural Correlates for Feeling-of-Knowing An fMRI Parametric Analysis , 2002, Neuron.

[54]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[55]  J. Herskowitz,et al.  Proceedings of the National Academy of Sciences, USA , 1996, Current Biology.

[56]  Karl J. Friston,et al.  Delineating Necessary and Sufficient Neural Systems with Functional Imaging Studies of Neuropsychological Patients , 1999, Journal of Cognitive Neuroscience.

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

[58]  Karl J. Friston,et al.  Dynamic Diaschisis: Anatomically Remote and Context-Sensitive Human Brain Lesions , 2001, Journal of Cognitive Neuroscience.

[59]  M. Browne,et al.  Alternative Ways of Assessing Model Fit , 1992 .