fMRI evidence of word frequency and strength effects in recognition memory.

We used event-related fMRI to investigate the neural correlates of encoding strength and word frequency effects in recognition memory. At test, participants made Old/New decisions to intermixed low (LF) and high frequency (HF) words that had been presented once or twice at study and to new, unstudied words. The Old/New effect for all hits vs. correctly rejected unstudied words was associated with differential activity in multiple cortical regions, including the anterior medial temporal lobe (MTL), hippocampus, left lateral parietal cortex and anterior left inferior prefrontal cortex (LIPC). Items repeated at study had superior hit rates (HR) compared to items presented once and were associated with reduced activity in the right anterior MTL. By contrast, other regions that had shown conventional Old/New effects did not demonstrate modulation according to memory strength. A mirror effect for word frequency was demonstrated, with the LF word HR advantage associated with increased activity in the left lateral temporal cortex. However, none of the regions that had demonstrated Old/New item retrieval effects showed modulation according to word frequency. These findings are interpreted as supporting single-process memory models proposing a unitary strength-like memory signal and models attributing the LF word HR advantage to the greater lexico-semantic context-noise associated with HF words due to their being experienced in many pre-experimental contexts.

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

[2]  S Dennis,et al.  Dual processes in recognition: Does a focus on measurement operations provide a sufficient foundation? , 2000, Psychonomic bulletin & review.

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

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

[5]  Florin Dolcos,et al.  Attention-related activity during episodic memory retrieval: a cross-function fMRI study , 2003, Neuropsychologia.

[6]  James L. McClelland,et al.  Familiarity breeds differentiation: a subjective-likelihood approach to the effects of experience in recognition memory. , 1998, Psychological review.

[7]  W. Hockley,et al.  Recollection and familiarity through the looking glass: when old does not mirror new. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[8]  M. Humphreys,et al.  A context noise model of episodic word recognition. , 2001, Psychological review.

[9]  Jin Fan,et al.  Functional magnetic resonance imaging of source versus item memory , 2003, Neuroreport.

[10]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.

[11]  Suzanne Corkin,et al.  Semantic knowledge in patient H.M. and other patients with bilateral medial and lateral temporal lobe lesions , 2002, Hippocampus.

[12]  L. Jacoby,et al.  Two effects of repetition: Support for a dual-process model of know judgments and exclusion errors , 1998 .

[13]  D. Shanks,et al.  Neuropsychological Dissociations between Priming and Recognition: a Single-system Connectionist Account , 2003 .

[14]  Kenneth J. Malmberg,et al.  Modeling the effects of repetitions, similarity, and normative word frequency on old-new recognition and judgments of frequency. , 2004, Journal of experimental psychology. Learning, memory, and cognition.

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

[16]  Endel Tulving,et al.  Prefrontal cortex and episodic memory retrieval mode. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[17]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[18]  John T Wixted,et al.  In defense of the signal detection interpretation of remember/know judgments , 2004, Psychonomic bulletin & review.

[19]  M. Unser,et al.  Interpolation Revisited , 2000, IEEE Trans. Medical Imaging.

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

[21]  M. Unser,et al.  Interpolation revisited [medical images application] , 2000, IEEE Transactions on Medical Imaging.

[22]  W Todd Maddox,et al.  On the processes underlying stimulus-familiarity effects in recognition of words and nonwords. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

[23]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[24]  Murray Glanzer,et al.  Six regularities of source recognition. , 2004, Journal of experimental psychology. Learning, memory, and cognition.

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

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

[27]  Kerry Lee,et al.  Recognition memory for studied words is determined by cortical activation differences at encoding but not during retrieval , 2004, NeuroImage.

[28]  Randy L. Buckner,et al.  Functional–Anatomic Correlates of Sustained and Transient Processing Components Engaged during Controlled Retrieval , 2003, The Journal of Neuroscience.

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

[30]  R. Shiffrin,et al.  A model for recognition memory: REM—retrieving effectively from memory , 1997, Psychonomic bulletin & review.

[31]  T. Landauer.  Memory without organization: Properties of a model with random storage and undirected retrieval , 1975, Cognitive Psychology.

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

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

[34]  W T Maddox,et al.  Direct and indirect stimulus-frequency effects in recognition. , 1997, Journal of experimental psychology. Learning, memory, and cognition.

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

[36]  J. Wixted,et al.  On the difference between strength-based and frequency-based mirror effects in recognition memory. , 1998, Journal of experimental psychology. Learning, memory, and cognition.

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

[38]  S. Blumstein,et al.  An Event-Related fMRI Investigation of Implicit Semantic Priming , 2003, Journal of Cognitive Neuroscience.

[39]  M. Glanzer,et al.  The regularities of recognition memory. , 1993, Psychological review.

[40]  M. Humphreys,et al.  What you get out of memory depends on the question you ask. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

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

[42]  Karl J. Friston,et al.  Modelling Geometric Deformations in Epi Time Series , 2022 .

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

[44]  L. Squire,et al.  The anatomy of semantic knowledge: medial vs. lateral temporal lobe. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Guillén Fernández,et al.  Process dissociation between contextual retrieval and item recognition , 2004, Neuroreport.

[46]  Kenneth J. Malmberg,et al.  The effect of normative context variability on recognition memory. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

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

[48]  T. O. Nelson,et al.  The word frequency effect for recognition memory and the elevated-attention hypothesis , 2003, Memory & cognition.

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

[50]  L. Squire,et al.  Intact Conceptual Priming in the Absence of Declarative Memory , 2004, Psychological science.

[51]  G. Bydder,et al.  Magnetic Resonance Scanning and Epilepsy , 1994, NATO ASI Series.

[52]  L. Reder,et al.  A mechanistic account of the mirror effect for word frequency: a computational model of remember-know judgments in a continuous recognition paradigm. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[53]  Jeroen G. W. Raaijmakers,et al.  Spacing and repetition effects in human memory: application of the SAM model , 2003, Cogn. Sci..

[54]  Simon Finnigan,et al.  fMRI evidence of word frequency and strength effects during episodic memory encoding. , 2005, Brain research. Cognitive brain research.

[55]  Katie L. McMahon,et al.  Brain activity during automatic semantic priming revealed by event-related functional magnetic resonance imaging , 2003, NeuroImage.

[56]  W. Donaldson,et al.  The role of decision processes in remembering and knowing , 1996, Memory & cognition.

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

[58]  W J Levelt,et al.  Spoken word production: A theory of lexical access , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[59]  S. Sikström.  The variance theory of the mirror effect in recognition memory , 2001, Psychonomic bulletin & review.

[60]  J. Dunn.  Remember-know: a matter of confidence. , 2004, Psychological review.

[61]  Vinod Menon,et al.  Relating semantic and episodic memory systems. , 2002, Brain research. Cognitive brain research.

[62]  Alan C. Evans,et al.  An MRI-Based Probabilistic Atlas of Neuroanatomy , 1994 .

[63]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

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

[65]  L. Reder,et al.  A dual-process account of the list-length and strength-based mirror effects in recognition , 2003 .

[66]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.