Sex Differences in the Neural Correlates of Specific and General Autobiographical Memory

Autobiographical memory (AM) underlies the formation and temporal continuity over time of personal identity. The few studies on sex-related differences in AM suggest that men and women adopt different cognitive or emotional strategies when retrieving AMs. However, none of the previous works has taken into account the distinction between episodic autobiographical memory (EAM), consisting in the retrieval of specific events by means of mental time travel, and semantic autobiographical memory (SAM), which stores general personal events. Thus, it remains unclear whether differences in these strategies depend on the nature of the memory content to be retrieved. In the present study we employed functional MRI to examine brain activity underlying potential sex differences in EAM and SAM retrieval focusing on the differences in strategies related to the emotional aspects of memories while controlling for basic cognitive strategies. On the behavioral level, there was no significant sex difference in memory performances or subjective feature ratings of either type of AM. Activations common to men and women during AM retrieval were observed in a typical bilateral network comprising medial and lateral temporal regions, precuneus, occipital cortex as well as prefrontal cortex. Contrast analyses revealed that there was no difference between men and women in the EAM condition. In the SAM condition, women showed an increased activity, compared to men, in the dorsal anterior cingulate cortex, inferior parietal and precentral gyrus. Overall, these findings suggest that differential neural activations reflect sex-specific strategies related to emotional aspects of AMs, particularly regarding SAM. We propose that this pattern of activation during SAM retrieval reflects the cognitive cost linked to emotion regulation strategies recruited by women compared to men. These sex-related differences have interesting implications for understanding psychiatric disorders with differential sex prevalence and in which one of key features is overgenerality in AM.

[1]  C. Woolley,et al.  Sex Differences in Molecular Signaling at Inhibitory Synapses in the Hippocampus , 2015, The Journal of Neuroscience.

[2]  E. Balteau,et al.  Brains creating stories of selves: the neural basis of autobiographical reasoning. , 2014, Social cognitive and affective neuroscience.

[3]  C. Oppenheim,et al.  Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex , 2013, PloS one.

[4]  Jerzy Bodurka,et al.  Functional neuroimaging of sex differences in autobiographical memory recall , 2013, Human brain mapping.

[5]  P. Piolino,et al.  The self-reference effect on episodic memory recollection in young and older adults and Alzheimer's disease. , 2013, Current Alzheimer research.

[6]  J. Hudson,et al.  Gender differences in autobiographical memory: Developmental and methodological considerations , 2013 .

[7]  M. Desrocher,et al.  The effects of gender on the retrieval of episodic and semantic components of autobiographical memory , 2013, Memory.

[8]  Pascale Piolino,et al.  Neural substrates of the self‐memory system: New insights from a meta‐analysis , 2013, Human brain mapping.

[9]  D. Addis,et al.  Autobiographical memory and sense of self. , 2013, Psychological bulletin.

[10]  C. Malherbe,et al.  Don’t be Too Strict with Yourself! Rigid Negative Self-Representation in Healthy Subjects Mimics the Neurocognitive Profile of Depression for Autobiographical Memory , 2013, Front. Behav. Neurosci..

[11]  S. Klein,et al.  Facets of Self in Schizophrenia , 2013 .

[12]  Louis Renoult,et al.  Personal semantics: at the crossroads of semantic and episodic memory , 2012, Trends in Cognitive Sciences.

[13]  M. Yücel,et al.  Sex differences in the neural correlates of emotion: Evidence from neuroimaging , 2011, Biological Psychology.

[14]  Julian F Thayer,et al.  Sex differences in the neural correlates of autonomic arousal: a pilot PET study. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  Roberto Cabeza,et al.  Gender differences in autobiographical memory for everyday events: Retrieval elicited by SenseCam images versus verbal cues , 2011, Memory.

[16]  M. Corbetta,et al.  Episodic Memory Retrieval, Parietal Cortex, and the Default Mode Network: Functional and Topographic Analyses , 2011, The Journal of Neuroscience.

[17]  Georg Northoff,et al.  Brain imaging of the self – Conceptual, anatomical and methodological issues , 2011, Consciousness and Cognition.

[18]  Pascale Piolino,et al.  Mental time travel into the past and the future in healthy aged adults: An fMRI study , 2011, Brain and Cognition.

[19]  Daniel S. Margulies,et al.  Delineating self-referential processing from episodic memory retrieval: Common and dissociable networks , 2010, NeuroImage.

[20]  T. Singer,et al.  The role of anterior insular cortex in social emotions , 2010, Brain Structure and Function.

[21]  S. Klein,et al.  The self: as a construct in psychology and neuropsychological evidence for its multiplicity. , 2010, Wiley interdisciplinary reviews. Cognitive science.

[22]  S. Belleville,et al.  Reduced specificity of autobiographical memory and aging: Do the executive and feature binding functions of working memory have a role? , 2010, Neuropsychologia.

[23]  Markus Heinrichs,et al.  The neural correlates of sex differences in emotional reactivity and emotion regulation , 2009, Human brain mapping.

[24]  Martin A. Conway,et al.  Autobiographical memory and amnesia: Using conceptual knowledge to ground the self , 2009, Neurocase.

[25]  Pascale Piolino,et al.  Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings , 2009, Neuropsychologia.

[26]  E. Hollander,et al.  Brief Report: Parental Age and the Sex Ratio in Autism , 2009, Journal of autism and developmental disorders.

[27]  Joseph M. Andreano,et al.  Sex influences on the neurobiology of learning and memory. , 2009, Learning & memory.

[28]  J. Gabrieli,et al.  Gender Differences in Emotion Regulation: An fMRI Study of Cognitive Reappraisal , 2008, Group processes & intergroup relations : GPIR.

[29]  J. Gross,et al.  The Neural Bases of Emotion Regulation: Reappraisal and Suppression of Negative Emotion , 2008, Biological Psychiatry.

[30]  Roberto Cabeza,et al.  Parietal Lobe and Episodic Memory: Bilateral Damage Causes Impaired Free Recall of Autobiographical Memory , 2007, The Journal of Neuroscience.

[31]  J. Singer,et al.  Older, wiser, and happier? Comparing older adults’ and college students’ self-defining memories , 2007, Memory.

[32]  Pascale Piolino,et al.  Hippocampal activation for autobiographical memories over the entire lifetime in healthy aged subjects: an fMRI study. , 2007, Cerebral cortex.

[33]  F. Eustache,et al.  Self multidimensionnel, mémoire autobiographique et vieillissement , 2007 .

[34]  I. Olson,et al.  The Enigmatic temporal pole: a review of findings on social and emotional processing. , 2007, Brain : a journal of neurology.

[35]  Sally A. Moore,et al.  Overgeneral autobiographical memory and traumatic events: an evaluative review. , 2007, Psychological bulletin.

[36]  R. Cabeza,et al.  Functional neuroimaging of autobiographical memory , 2007, Trends in Cognitive Sciences.

[37]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[38]  Michael P. Kaschak,et al.  Body posture facilitates retrieval of autobiographical memories , 2007, Cognition.

[39]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[40]  Francis Eustache,et al.  The relationship between working memory and episodic memory disorders in transient global amnesia , 2006, Neuropsychologia.

[41]  K. Hugdahl,et al.  Sex differences in visuo-spatial processing: An fMRI study of mental rotation , 2006, Neuropsychologia.

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

[43]  B. Desgranges,et al.  Autobiographical memory, autonoetic consciousness, and self-perspective in aging. , 2006, Psychology and aging.

[44]  P. Fossati,et al.  Episodic autobiographical memory in depression: Specificity, autonoetic consciousness, and self-perspective , 2006, Consciousness and Cognition.

[45]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[46]  Rossana de Beni,et al.  Left mediotemporal structures mediate the retrieval of episodic autobiographical mental images , 2006, NeuroImage.

[47]  Michael C. Wendl,et al.  Argonaute—a database for gene regulation by mammalian microRNAs , 2005, BMC Bioinformatics.

[48]  M. Van der Linden,et al.  Affective valence and the self-reference effect: influence of retrieval conditions. , 2005, British journal of psychology.

[49]  Martin A. Conway,et al.  Memory and the self , 2005 .

[50]  Gereon R. Fink,et al.  Recollections of one’s own past: the effects of aging and gender on the neural mechanisms of episodic autobiographical memory , 2005, Anatomy and Embryology.

[51]  R. Pohl,et al.  Autobiographical memory and social skills of men and women , 2005 .

[52]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[53]  Gereon R Fink,et al.  Gender differences in the functional neuroanatomy of emotional episodic autobiographical memory , 2005, Human brain mapping.

[54]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

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

[56]  Morris Moscovitch,et al.  Characterizing spatial and temporal features of autobiographical memory retrieval networks: a partial least squares approach , 2004, NeuroImage.

[57]  Brian Levine,et al.  The Functional Neuroanatomy of Episodic and Semantic Autobiographical Remembering: A Prospective Functional MRI Study , 2004, Journal of Cognitive Neuroscience.

[58]  Martin A. Conway,et al.  The Self and Autobiographical Memory: Correspondence and Coherence , 2004 .

[59]  Jennifer M. Talarico,et al.  Emotional intensity predicts autobiographical memory experience , 2004, Memory & cognition.

[60]  Jean-Claude Baron,et al.  Re-experiencing old memories via hippocampus: a PET study of autobiographical memory , 2004, NeuroImage.

[61]  J. Singer,et al.  Four dimensions of self-defining memories (specificity, meaning, content, and affect) and their relationships to self-restraint, distress, and repressive defensiveness. , 2004, Journal of personality.

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

[63]  F. Bermpohl,et al.  Cortical midline structures and the self , 2004, Trends in Cognitive Sciences.

[64]  Jonas Persson,et al.  Common prefrontal activations during working memory, episodic memory, and semantic memory , 2003, Neuropsychologia.

[65]  David B. Pillemer,et al.  Gender differences in autobiographical memory styles of older adults , 2003, Memory.

[66]  F. Craik,et al.  In search of the emotional self: an fMRI study using positive and negative emotional words. , 2003, The American journal of psychiatry.

[67]  Pascale Piolino,et al.  Autobiographical memory and autonoetic consciousness: triple dissociation in neurodegenerative diseases. , 2003, Brain : a journal of neurology.

[68]  Hanna Damasio,et al.  Effects of gender on blood flow correlates of naming concrete entities , 2003, NeuroImage.

[69]  R. Kahn,et al.  Sex differences in the risk of schizophrenia: evidence from meta-analysis. , 2003, Archives of general psychiatry.

[70]  T. Wüstenberg,et al.  Women and men exhibit different cortical activation patterns during mental rotation tasks , 2002, Neuropsychologia.

[71]  G. Winocur,et al.  Aging and autobiographical memory: dissociating episodic from semantic retrieval. , 2002, Psychology and aging.

[72]  Pascale Piolino,et al.  Episodic and semantic remote autobiographical memory in ageing , 2002, Memory.

[73]  S. Wester,et al.  Sex Differences in Emotion , 2002 .

[74]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[75]  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.

[76]  E A Maguire,et al.  Neuroimaging studies of autobiographical event memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[77]  M. Buonocore,et al.  Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval , 2001, Neuroscience.

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

[79]  M. J. Emerson,et al.  The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis , 2000, Cognitive Psychology.

[80]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[81]  M. Conway,et al.  The construction of autobiographical memories in the self-memory system. , 2000, Psychological review.

[82]  S. Gallagher Philosophical conceptions of the self: implications for cognitive science , 2000, Trends in Cognitive Sciences.

[83]  R. Maddock The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain , 1999, Trends in Neurosciences.

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

[85]  P. Davis Gender differences in autobiographical memory for childhood emotional experiences. , 1999, Journal of personality and social psychology.

[86]  G. Winocur,et al.  In Search of the Self: A Positron Emission Tomography Study , 1999 .

[87]  S Dehaene,et al.  A neuronal model of a global workspace in effortful cognitive tasks. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[88]  Alex Martin,et al.  Neural correlates of semantic and episodic memory retrieval , 1998, Neuropsychologia.

[89]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[90]  A. Kring,et al.  Sex differences in emotion: expression, experience, and physiology. , 1998, Journal of personality and social psychology.

[91]  A. Herlitz,et al.  Gender differences in episodic memory , 1997, Memory & cognition.

[92]  N. Breslau,et al.  Sex differences in posttraumatic stress disorder. , 1997, Archives of general psychiatry.

[93]  G. Fink,et al.  Cerebral Representation of One’s Own Past: Neural Networks Involved in Autobiographical Memory , 1996, The Journal of Neuroscience.

[94]  Peter Salovey,et al.  Mood Regulation and Memory: Repairing Sad Moods with Happy Memories , 1996 .

[95]  Charles Freer,et al.  Functional Neuroimaging , 1995 .

[96]  Martin A. Conway,et al.  The self and recollective experience. , 1995 .

[97]  M. J. Sharps,et al.  Gender and Task in the Determination of Spatial Cognitive Performance , 1993 .

[98]  G. Cupchik,et al.  An experimental characterization of odor-evoked memories in humans , 1992 .

[99]  E. Diener,et al.  Gender differences in negative affect and well-being: the case for emotional intensity. , 1991, Journal of personality and social psychology.

[100]  A. Pines,et al.  Sex differences in gender-related childhood memories , 1991 .

[101]  Charles P. Thompson,et al.  Social memory in everyday life: Recall of self-events and other-events. , 1991 .

[102]  Z. Kunda,et al.  Motivated recruitment of autobiographical memories. , 1990, Journal of personality and social psychology.

[103]  A D Baddeley,et al.  The autobiographical memory interview: a new assessment of autobiographical and personal semantic memory in amnesic patients. , 1989, Journal of clinical and experimental neuropsychology.

[104]  J. Ritchie,et al.  Gender differences in friendship patterns , 1988 .

[105]  S. Nolen-Hoeksema,et al.  Sex differences in unipolar depression: evidence and theory. , 1987, Psychological bulletin.

[106]  U. Neisser,et al.  Point of view in personal memories , 1983, Cognitive Psychology.

[107]  E. C. Ritchie,et al.  Gender Differences , 1981, Language in Society.

[108]  S. Vandenberg,et al.  Mental Rotations, a Group Test of Three-Dimensional Spatial Visualization , 1978, Perceptual and motor skills.

[109]  J. Block,et al.  Conceptions of sex role. Some cross-cultural and longitudinal perspectives. , 1973, The American psychologist.

[110]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[111]  R. Reitan Validity of the Trail Making Test as an Indicator of Organic Brain Damage , 1958 .

[112]  Glenda Andrews,et al.  Sex and sex-role differences in specific cognitive abilities , 2016 .

[113]  Self-Concept Variables Sex Differences in , 2016 .

[114]  Alisha C. Holland,et al.  The Neural Correlates of Cognitive Reappraisal during Emotional Autobiographical Memory Recall , 2013, Journal of Cognitive Neuroscience.

[115]  K. Taber,et al.  Anterior cingulate cortex: unique role in cognition and emotion. , 2011, The Journal of neuropsychiatry and clinical neurosciences.

[116]  Chen,et al.  A functional magnetic resonance imaging study , 2011 .

[117]  J. Cottraux,et al.  Protocoles et échelles d'évaluation en psychiatrie et psychologie , 2010 .

[118]  P. Ruby,et al.  What is self-specific? Theoretical investigation and critical review of neuroimaging results. , 2009, Psychological review.

[119]  F. Eustache,et al.  [Multidimensional Self, autobiographical memory and aging]. , 2007, Psychologie & neuropsychiatrie du vieillissement.

[120]  Morris Moscovitch,et al.  Recollective qualities modulate hippocampal activation during autobiographical memory retrieval , 2004, Hippocampus.

[121]  J. Gross,et al.  PERSONALITY PROCESSES AND INDIVIDUAL DIFFERENCES Emotion Regulation and Memory: The Cognitive Costs of Keeping One's Cool , 2004 .

[122]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[123]  F. Crivello,et al.  Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of t , 2001 .

[124]  D. Wechsler,et al.  Echelle d'intelligence de Wechsler pour adultes , 2000 .

[125]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[126]  E. Diener,et al.  Sex differences in the recall of affective experiences. , 1998, Journal of personality and social psychology.

[127]  B. Fredrickson,et al.  Response styles and the duration of episodes of depressed mood. , 1993, Journal of abnormal psychology.

[128]  A. Beck,et al.  Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation , 1988 .

[129]  H. Buschke,et al.  Genuine memory deficits in dementia , 1987 .

[130]  Gemma C. L. Bornick Eating disorders. , 1987, Southern medical journal.

[131]  M. Weissman,et al.  Sex differences and the epidemiology of depression. , 1977, Archives of general psychiatry.

[132]  D. Schacter,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Aging, Blockinself-referencing, Blockinand Blockinmedial Blockinprefrontal Cortex , 2022 .