False Recall Is Reduced by Damage to the Ventromedial Prefrontal Cortex: Implications for Understanding the Neural Correlates of Schematic Memory

Schematic memory, or contextual knowledge derived from experience (Bartlett, 1932), benefits memory function by enhancing retention and speeding learning of related information (Bransford and Johnson, 1972; Tse et al., 2007). However, schematic memory can also promote memory errors, producing false memories. One demonstration is the “false memory effect” of the Deese–Roediger–McDermott (DRM) paradigm (Roediger and McDermott, 1995): studying words that fit a common schema (e.g., cold, blizzard, winter) often produces memory for a nonstudied word (e.g., snow). We propose that frontal lobe regions that contribute to complex decision-making processes by weighting various alternatives, such as ventromedial prefrontal cortex (vmPFC), may also contribute to memory processes by weighting the influence of schematic knowledge. We investigated the role of human vmPFC in false memory by combining a neuropsychological approach with the DRM task. Patients with vmPFC lesions (n = 7) and healthy comparison participants (n = 14) studied word lists that excluded a common associate (the critical item). Recall and recognition tests revealed expected high levels of false recall and recognition of critical items by healthy participants. In contrast, vmPFC patients showed consistently reduced false recall, with significantly fewer intrusions of critical items. False recognition was also marginally reduced among vmPFC patients. Our findings suggest that vmPFC increases the influence of schematically congruent memories, a contribution that may be related to the role of the vmPFC in decision making. These novel neuropsychological results highlight a role for the vmPFC as part of a memory network including the medial temporal lobes and hippocampus (Andrews-Hanna et al., 2010).

[1]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

[2]  Henry L. Roediger,et al.  Age differences in veridical and false recall are not inevitable: The role of frontal lobe function , 2004, Psychonomic bulletin & review.

[3]  Antonio Damasio,et al.  The somatic marker hypothesis: A neural theory of economic decision , 2005, Games Econ. Behav..

[4]  Cheryl L. Dahle,et al.  Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. , 2005, Cerebral cortex.

[5]  R. J. Frank,et al.  Three-dimensional in vivo mapping of brain lesions in humans. , 1992, Archives of neurology.

[6]  R. Henson,et al.  How schema and novelty augment memory formation , 2012, Trends in Neurosciences.

[7]  Guillén Fernández,et al.  Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans , 2010, Proceedings of the National Academy of Sciences.

[8]  K. Saleem,et al.  Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey , 2008, The Journal of comparative neurology.

[9]  H L Roediger,et al.  Modality effects in false recall and false recognition. , 2001, Journal of experimental psychology. Learning, memory, and cognition.

[10]  Lynn Hasher,et al.  Is memory schematic , 1983 .

[11]  J. Deese Influence of Inter-Item Associative Strength upon Immediate Free Recall , 1959 .

[12]  Dorothy Tse,et al.  Schema-Dependent Gene Activation and Memory Encoding in Neocortex , 2011, Science.

[13]  Dagmar Zeithamova,et al.  Hippocampal and Ventral Medial Prefrontal Activation during Retrieval-Mediated Learning Supports Novel Inference , 2012, Neuron.

[14]  J. D. McGaugh,et al.  False memories in highly superior autobiographical memory individuals , 2013, Proceedings of the National Academy of Sciences.

[15]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[16]  R. Adolphs,et al.  Damage to the prefrontal cortex increases utilitarian moral judgements , 2007, Nature.

[17]  Daniel L. Schacter,et al.  False recognition in younger and older adults: Exploring the characteristics of illusory memories , 1997, Memory & cognition.

[18]  Sean A. Spence,et al.  Descartes' Error: Emotion, Reason and the Human Brain , 1995 .

[19]  D. Stuss,et al.  Organizational strategies with unilateral or bilateral frontal lobe injury in word learning tasks. , 1994 .

[20]  H L Roediger,et al.  Norms for word lists that create false memories , 1999, Memory & cognition.

[21]  Margaret L. Schlichting,et al.  The hippocampus and inferential reasoning: building memories to navigate future decisions , 2012, Front. Hum. Neurosci..

[22]  D. Schacter,et al.  The Neuropsychology of Memory Illusions: False Recall and Recognition in Amnesic Patients , 1996 .

[23]  John S. Allen,et al.  Normal neuroanatomical variation due to age: The major lobes and a parcellation of the temporal region , 2005, Neurobiology of Aging.

[24]  K. McDermott,et al.  Creating false memories: Remembering words not presented in lists. , 1995 .

[25]  T Shallice,et al.  Preserved recall versus impaired recognition. A case study. , 1990, Brain : a journal of neurology.

[26]  R. Henson,et al.  Differential roles for medial prefrontal and medial temporal cortices in schema-dependent encoding: From congruent to incongruent , 2013, Neuropsychologia.

[27]  R. Grissom,et al.  Effect Sizes for Research : Univariate and Multivariate Applications, Second Edition , 2005 .

[28]  L. Squire,et al.  Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. , 1980, Science.

[29]  Nikolaus Weiskopf,et al.  Detecting Representations of Recent and Remote Autobiographical Memories in vmPFC and Hippocampus , 2012, The Journal of Neuroscience.

[30]  D. Hassabis,et al.  Tracking the Emergence of Conceptual Knowledge during Human Decision Making , 2009, Neuron.

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

[32]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[33]  David A. Balota,et al.  Memory changes in healthy older adults. , 2000 .

[34]  A P Shimamura,et al.  Cognitive impairment following frontal lobe damage and its relevance to human amnesia. , 1989, Behavioral neuroscience.

[35]  W. Scoville,et al.  Loss of Recent Memory After Bilateral Hippocampal Lesions , 2000 .

[36]  A. Damasio,et al.  Deciding Advantageously Before Knowing the Advantageous Strategy , 1997, Science.

[37]  Morris Moscovitch,et al.  Mechanisms of spontaneous confabulations: a strategic retrieval account. , 2006, Brain : a journal of neurology.

[38]  Marcia K. Johnson,et al.  False recollection induced by photographs: a comparison of older and younger adults. , 1997, Psychology and aging.

[39]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

[40]  K. McDermott,et al.  Factors that determine false recall: A multiple regression analysis , 2001, Psychonomic bulletin & review.

[41]  Marcia K. Johnson,et al.  Contextual prerequisites for understanding: Some investigations of comprehension and recall , 1972 .

[42]  Bruce L McNaughton,et al.  Apparent Encoding of Sequential Context in Rat Medial Prefrontal Cortex Is Accounted for by Behavioral Variability , 2006, The Journal of Neuroscience.

[43]  Catherine A. Cole,et al.  The Orbitofrontal Cortex, Real‐World Decision Making, and Normal Aging , 2007, Annals of the New York Academy of Sciences.

[44]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[45]  R. J. Frank,et al.  Brainvox: An Interactive, Multimodal Visualization and Analysis System for Neuroanatomical Imaging , 1997, NeuroImage.