Functional neuroimaging of sex differences in autobiographical memory recall

Autobiographical memory (AM) is episodic memory for personally experienced events. The brain areas underlying AM retrieval are known to include several prefrontal cortical and medial temporal lobe regions. Sex differences in AM recall have been reported in several behavioral studies, but the functional anatomical correlates underlying such differences remain unclear. This study used fMRI to compare the neural correlates of AM recall between healthy male and female participants (n = 20 per group). AM recall in response to positive, negative, and neutral cue words was compared to a semantic memory task involving the generation of examples from a category using emotionally valenced cues. Behaviorally, females recalled more negative and fewer positive AMs compared with males, while ratings of arousal, vividness, and memory age did not differ significantly between sexes. Males and females also did not differ significantly in their performance on control tasks. Neurophysiologically, females showed increased hemodynamic activity compared to males in the dorsolateral prefrontal cortex (DLPFC), dorsal anterior insula, and precuneus while recalling specific AMs (all valences combined); increased activity in the DLPFC, transverse temporal gyrus, and precuneus while recalling positive AMs; and increased activity in the anterior cingulate cortex, precuneus, amygdala, and temporopolar cortex when recalling negative AMs. When comparing positive to negative AMs directly, males and females differed in their BOLD responses in the hippocampus and DLPFC. We propose that the differential hemodynamic changes may reflect sex‐specific cognitive strategies during recall of AMs irrespective of the phenomenological properties of those memories. Hum Brain Mapp 34:3320–3332, 2013. © 2012 Wiley Periodicals, Inc.

[1]  C. Spielberger,et al.  Manual for the state-trait anxiety inventory (form Y) : "self-evaluation questionnaire" , 1983 .

[2]  G. Fernández,et al.  Gonadal hormone regulation of the emotion circuitry in humans , 2011, Neuroscience.

[3]  M. Hamilton A RATING SCALE FOR DEPRESSION , 1960, Journal of neurology, neurosurgery, and psychiatry.

[4]  Joseph M. Andreano,et al.  Progesterone at encoding predicts subsequent emotional memory. , 2011, Learning & memory.

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

[6]  John C. Gore,et al.  ROC Analysis of Statistical Methods Used in Functional MRI: Individual Subjects , 1999, NeuroImage.

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

[8]  Larry Cahill,et al.  Menstrual cycle modulation of medial temporal activity evoked by negative emotion , 2010, NeuroImage.

[9]  Martin A. Conway,et al.  A Structural Model of Autobiographical Memory , 1992 .

[10]  Robert T. Knight,et al.  Neural activity during social signal perception correlates with self-reported empathy , 2010, Brain Research.

[11]  D. Rubin,et al.  Brain Activity during Episodic Retrieval of Autobiographical and Laboratory Events: An fMRI Study using a Novel Photo Paradigm , 2004, Journal of Cognitive Neuroscience.

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

[13]  M. Buonocore,et al.  Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task , 2003, Human brain mapping.

[14]  R N Henson,et al.  Activity in prefrontal cortex, not hippocampus, varies parametrically with the increasing remoteness of memories , 2001, Neuroreport.

[15]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[16]  Rachel J. Anderson,et al.  Reduced specificity of autobiographical memory as a moderator of the relationship between daily hassles and depression , 2010 .

[17]  E. Tulving Episodic memory: from mind to brain. , 2002, Annual review of psychology.

[18]  S. Langenecker,et al.  Gender‐specific disruptions in emotion processing in younger adults with depression , 2009, Depression and anxiety.

[19]  David J. Turk,et al.  A positron emission tomography (PET) study of autobiographical memory retrieval. , 1999, Memory.

[20]  Eleanor A Maguire,et al.  Aging affects the engagement of the hippocampus during autobiographical memory retrieval. , 2003, Brain : a journal of neurology.

[21]  M. Raichle,et al.  Blood flow changes in human somatosensory cortex during anticipated stimulation , 1995, Nature.

[22]  J. Williams,et al.  Autobiographical memory in suicide attempters. , 1986, Journal of abnormal psychology.

[23]  Joseph E LeDoux Emotional networks and motor control: a fearful view. , 1996, Progress in brain research.

[24]  N. Makris,et al.  Sex Differences in Stress Response Circuitry Activation Dependent on Female Hormonal Cycle , 2010, The Journal of Neuroscience.

[25]  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.

[26]  B. Mensour,et al.  Neural circuitry underlying voluntary suppression of sadness , 2003, Biological Psychiatry.

[27]  P. Roland Cortical regulation of selective attention in man. A regional cerebral blood flow study. , 1982, Journal of neurophysiology.

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

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

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

[31]  Gereon R Fink,et al.  Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. , 2003, Brain : a journal of neurology.

[32]  C. Scheiber,et al.  Implicit emotion during recollection of past events: A nonverbal fMRI study , 2006, Brain Research.

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

[34]  T. Dalgleish,et al.  Autobiographical Memory Specificity and Emotional Disorder , 2007, Psychological bulletin.

[35]  J. Binder,et al.  Functional magnetic resonance imaging of human auditory cortex , 1994, Annals of neurology.

[36]  J. Price,et al.  Neurocircuitry of Mood Disorders , 2010, Neuropsychopharmacology.

[37]  G. Winocur,et al.  Remembering our past: functional neuroanatomy of recollection of recent and very remote personal events. , 2004, Cerebral cortex.

[38]  Sharron E. Whitecross,et al.  Neurophysiological correlates of memory for experienced and imagined events , 2003, Neuropsychologia.

[39]  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 .

[40]  J. Williams,et al.  Autobiographical memory in depression , 1988, Psychological Medicine.

[41]  Martha Frías,et al.  Are Women More Empathetic than Men? A Longitudinal Study in Adolescence , 2009, The Spanish journal of psychology.

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

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

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

[45]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[47]  M Moscovitch,et al.  Hippocampal complex and retrieval of recent and very remote autobiographical memories: Evidence from functional magnetic resonance imaging in neurologically intact people , 2001, Hippocampus.

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

[49]  Takashi Tsukiura,et al.  Neural Basis of Temporal Context Memory: A Functional MRI Study , 2001, NeuroImage.

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

[51]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.