The functional neuroanatomy of odor evoked autobiographical memories cued by odors and words

Behavioral evidence indicates that odor evoked autobiographical memories (OEAMs) are older, more emotional, less thought of and induce stronger time traveling characteristics than autobiographical memories (AMs) evoked by other modalities. The main aim of this study was to explore the neural correlates of AMs evoked by odors as a function of retrieval cue. Participants were screened for specific OEAMs and later presented with the odor cue and its verbal referent in an fMRI paradigm. Because the same OEAM was retrieved across both cue formats (odor and word), potential cue dependent brain activations were investigated. The overall results showed that odor and word cued OEAMs activated regions typically associated with recollection of autobiographical information. Although no odors were presented, a verbal cuing of the OEAMs activated areas associated with olfactory perception (e.g., piriform cortex). However, relative to word cuing, an odor cuing of OEAMs resulted in more activity in MTL regions such as the parahippocampus, and areas involved in visual vividness (e.g., occipital gyrus and precuneus). Furthermore, odor cues activated areas related to emotional processing, such as limbic and tempopolar regions significantly more. In contrast, word cues relative to odor cues recruited a more widespread and bilateral prefrontal activity. Hippocampus activity did not vary as function of the remoteness of the memory, but recollection of OEAMs from the 1(st) vs the 2(nd) decade of life showed specific activation in the right OFC, whereas the 2(nd) reflected a higher activation in the left inferior frontal gyrus.

[1]  T. Parrish,et al.  Right Orbitofrontal Cortex Mediates Conscious Olfactory Perception , 2010, Psychological science.

[2]  B. Gulyás,et al.  Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. , 1995, Cerebral cortex.

[3]  Hadas Lapid,et al.  The Privileged Brain Representation of First Olfactory Associations , 2009, Current Biology.

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

[5]  Eric Halgren,et al.  Ecphory of autobiographical memories: An fMRI study of recent and remote memory retrieval , 2006, NeuroImage.

[6]  Maria Larsson,et al.  Smell your way back to childhood: Autobiographical odor memory , 2006, Psychonomic bulletin & review.

[7]  Jared F. Danker,et al.  The ghosts of brain states past: remembering reactivates the brain regions engaged during encoding. , 2010, Psychological bulletin.

[8]  Mark Jenkinson,et al.  Optimization of static field homogeneity in human brain using diamagnetic passive shims , 2002, Magnetic resonance in medicine.

[9]  Lars-Göran Nilsson,et al.  Reactivation of Motor Brain Areas during Explicit Memory for Actions , 2001, NeuroImage.

[10]  R. Herz,et al.  Verbal coding in olfactory versus nonolfactory cognition , 2000, Memory & cognition.

[11]  Michael D Rugg,et al.  Remembrance of Odors Past Human Olfactory Cortex in Cross-Modal Recognition Memory , 2004, Neuron.

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

[13]  R. Herz,et al.  The effect of verbal context on olfactory perception. , 2003, Journal of experimental psychology. General.

[14]  M. Mesulam,et al.  Neural inputs into the temporopolar cortex of the rhesus monkey , 1987, The Journal of comparative neurology.

[15]  Karl J. Friston,et al.  Spatial Normalization using Basis Functions , 2003 .

[16]  Daniel L. Schacter,et al.  Routes to the past: Neural substrates of direct and generative autobiographical memory retrieval , 2012, NeuroImage.

[17]  F Rösler,et al.  Dynamics of activation in long-term memory: the retrieval of verbal, pictorial, spatial, and color information. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[18]  M. Petrides,et al.  Functional neuroimaging of odor imagery , 2005, NeuroImage.

[19]  John E Desmond,et al.  Evidence for cortical encoding specificity in episodic memory: memory-induced re-activation of picture processing areas , 2002, Neuropsychologia.

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

[21]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

[22]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[23]  D. Addis,et al.  Differential neural activity during search of specific and general autobiographical memories elicited by musical cues , 2011, Neuropsychologia.

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

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

[26]  R. Herz.  Are Odors the Best Cues to Memory? A Cross‐Modal Comparison of Associative Memory Stimuli a , 1998, Annals of the New York Academy of Sciences.

[27]  Maria Larsson,et al.  Autobiographical Odor Memory , 2009, Annals of the New York Academy of Sciences.

[28]  J. Gottfried.  Central mechanisms of odour object perception , 2010, Nature Reviews Neuroscience.

[29]  D. Rubin,et al.  The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving. , 2008, Cerebral cortex.

[30]  G. Cupchik,et al.  The emotional distinctiveness of odor-evoked memories. , 1995, Chemical senses.

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

[33]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  W. D. Penny,et al.  Random-Effects Analysis , 2002 .

[35]  R. Buckner,et al.  The cognitive neuroscience og remembering , 2001, Nature Reviews Neuroscience.

[36]  Friedemann Pulvermüller,et al.  Reading cinnamon activates olfactory brain regions , 2006, NeuroImage.

[37]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[38]  L. Klimek,et al.  Multicenter investigation of 1,036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds , 2000, European Archives of Oto-Rhino-Laryngology.

[39]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[40]  A. Gilbert,et al.  Olfactory and visual mental imagery. , 1998 .

[41]  L. Nadel,et al.  Autobiographical Memory Retrieval and Hippocampal Activation as a Function of Repetition and the Passage of Time , 2007, Neural plasticity.

[42]  L Nyberg,et al.  Conjunction analysis of cortical activations common to encoding and retrieval , 2000, Microscopy research and technique.

[43]  E. Tulving,et al.  Reactivation of encoding-related brain activity during memory retrieval. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  G. Shulman,et al.  Evidence for separate perceptual reactivation and search processes during remembering. , 2006, Cerebral cortex.

[45]  Maria Larsson,et al.  Olfaction and emotion: The case of autobiographical memory , 2007, Memory & cognition.

[46]  J. Downes,et al.  Odour-evoked autobiographical memories: psychological investigations of proustian phenomena. , 2000, Chemical senses.

[47]  D C Rubin,et al.  Olfactory cuing of autobiographical memory. , 1984, The American journal of psychology.

[48]  Richard J. S. Wise,et al.  The Contribution of the Parietal Lobes to Speaking and Writing , 2009, Cerebral cortex.

[49]  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.

[50]  James Eliassen,et al.  Neuroimaging evidence for the emotional potency of odor-evoked memory , 2004, Neuropsychologia.

[51]  J. Gottfried,et al.  Smell: central nervous processing. , 2006, Advances in oto-rhino-laryngology.

[52]  G. Winocur,et al.  Systems consolidation and hippocampus: two views , 2007 .

[53]  Kevin S. LaBar,et al.  Co-activation of the amygdala, hippocampus and inferior frontal gyrus during autobiographical memory retrieval , 2005, Neuropsychologia.

[54]  T. Hummel,et al.  'Sniffin' sticks': olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. , 1997, Chemical senses.

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

[56]  Noam Sobel,et al.  Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception. , 2007, Journal of neurophysiology.

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

[58]  J. Schooler,et al.  A naturalistic study of autobiographical memories evoked by olfactory and visual cues: testing the Proustian hypothesis. , 2002, The American journal of psychology.

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