Neural substrates of cross-modal olfactory recognition memory: An fMRI study

Ten young adults (aged 20 to 25 years) participated in a functional Magnetic Resonance Imaging (fMRI) study to investigate neural substrates of cross-modal olfactory recognition memory. Before entering the scanner, participants were presented with 16 familiar odors selected from the COLT (Murphy, C., Nordin, S., Acosta, L., 1997. Odor learning, recall, and recognition memory in young and elderly adults. Neuropsychology 11, 126-137) and were then scanned for 3 runs according to a paradigm derived from Stark and Squire (Stark, C.E., Squire, L.R., 2000. Functional magnetic resonance imaging (fMRI) activity in the hippocampal region during recognition memory. J. Neurosci. 20, 7776-7781). During each run, participants were shown names of odors presented (targets) or not presented (foils) at encoding. Participants distinguished targets from foils via button press. Each run alternated 4 'ON' periods containing 7 targets and 2 foils (36 s) and 4 'OFF' periods with 7 foils and 2 targets (36 s). Data were processed with AFNI (Cox, R.W., 1996. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162-173) and compared ON and OFF periods, extracting activation in regions that responded during the cross-modal olfactory recognition memory task. Group analysis showed that regions activated during the first run included right hippocampus, piriform/amygdalar area, superior temporal gyrus, anterior cingulate gyrus, inferior frontal/orbitofrontal gyrus, superior/medial frontal gyrus, and bilateral parahippocampal gyrus, inferior parietal lobule, supramarginal gyrus, cerebellum, lingual/fusiform area and middle/posterior cingulate gyrus. Region of interest analysis showed that degree of activation significantly decreased from run 1 to run 3 in the right hippocampus, fusiform gyrus, lingual gyrus, parahippocampal gyrus and middle frontal gyrus but not in other regions, suggesting that these regions sustain a specific function in olfactory recognition memory that attenuates as foils become more familiar with repeated presentation.

[1]  W. C. Halstead.  Brain and intelligence , 1947 .

[2]  Lars Nyberg,et al.  Hemispheric asymmetries of memory: the HERA model revisited , 2003, Trends in Cognitive Sciences.

[3]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[4]  L. Squire,et al.  Functional Magnetic Resonance Imaging (fMRI) Activity in the Hippocampal Region during Recognition Memory , 2000, The Journal of Neuroscience.

[5]  R. Klein,et al.  Prevalence of olfactory impairment in older adults. , 2002, JAMA.

[6]  S. Nordin,et al.  Impaired sensory and cognitive olfactory function in questionable Alzheimer's disease. , 1996 .

[7]  Bruce R. Rosen,et al.  Activation and Habituation in Olfaction—An fMRI Study , 2001, NeuroImage.

[8]  J. Talairach,et al.  Referentially oriented cerebral MRI anatomy : an atlas of stereotaxic anatomical correlations for gray and white matter , 1993 .

[9]  B. Cerf-Ducastel,et al.  fMRI activation in response to odorants orally delivered in aqueous solutions. , 2001, Chemical senses.

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

[11]  J. D. E. Gabrieli,et al.  Sniffing and smelling: separate subsystems in the human olfactory cortex , 1998, Nature.

[12]  Karl J. Friston,et al.  Activation of Human Hippocampal Formation During Memory for Faces: A Pet Study , 1995, Cortex.

[13]  Gilles Sicard,et al.  Functional Anatomy of Perceptual and Semantic Processing for Odors , 1999, Journal of Cognitive Neuroscience.

[14]  Barbara Cerf-Ducastel,et al.  ERP, fMRI and functional connectivity studies of brain response to odor in normal aging and Alzheimer's disease. , 2005, Chemical senses.

[15]  R. Dolan,et al.  The Nose Smells What the Eye Sees Crossmodal Visual Facilitation of Human Olfactory Perception , 2003, Neuron.

[16]  S. Nordin,et al.  Odor learning, recall, and recognition memory in young and elderly adults. , 1997, Neuropsychology.

[17]  J. Pardo,et al.  Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[18]  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.

[19]  Alan C. Evans,et al.  Functional localization and lateralization of human olfactory cortex , 1992, Nature.

[20]  Hans J. Markowitsch,et al.  Which brain regions are critically involved in the retrieval of old episodic memory? , 1995, Brain Research Reviews.

[21]  Dick J. Veltman,et al.  Parahippocampal Activation during Successful Recognition of Words: A Self-Paced Event-Related fMRI Study , 2001, NeuroImage.

[22]  Robert J Zatorre,et al.  Olfactory learning: convergent findings from lesion and brain imaging studies in humans. , 2002, Brain : a journal of neurology.

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

[24]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[25]  E Tulving,et al.  Functional role of the prefrontal cortex in retrieval of memories: a PET study , 1995, Neuroreport.

[26]  Anthony R. McIntosh,et al.  Age-Related Differences in Neural Activity during Memory Encoding and Retrieval: A Positron Emission Tomography Study , 1997, The Journal of Neuroscience.

[27]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[28]  D. Yousem,et al.  Gender effects on odor-stimulated functional magnetic resonance imaging , 1999, Brain Research.

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

[30]  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.

[31]  Alan C. Evans,et al.  Human Brain Function during Odor Encoding and Recognition: A PET Activation Study a , 1998, Annals of the New York Academy of Sciences.

[32]  G Kobal,et al.  Olfactory functional imaging and physiology. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[33]  Joseph L. Price,et al.  Beyond the primary olfactory cortex: olfactory-related areas in the neocortex, thalamus and hypothalamus , 1985 .

[34]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[35]  B. Gulyás,et al.  Olfactory Functions Are Mediated by Parallel and Hierarchical Processing , 2000, Neuron.

[36]  Stephan Arndt,et al.  The cerebellum plays a role in conscious episodic memory retrieval , 1999, Human brain mapping.

[37]  W. Cain,et al.  Sensory and semantic factors in recognition memory for odors and graphic stimuli: elderly versus young persons. , 1991, The American journal of psychology.

[38]  B. Cerf-Ducastel,et al.  FMRI brain activation in response to odors is reduced in primary olfactory areas of elderly subjects , 2003, Brain Research.

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

[40]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A. Jensen,et al.  The Stroop color-word test: a review. , 1966, Acta psychologica.

[42]  A. Anderson,et al.  Emotional memory: What does the amygdala do? , 1997, Current Biology.

[43]  J. Gabrieli.  Functional Neuroimaging of Episodic Memory , 2001 .

[44]  R. Henson,et al.  The neural basis of episodic memory: evidence from functional neuroimaging. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[45]  Howard Eichenbauma.  Using Olfaction to Study Memory , 1998 .

[46]  J. O'Doherty,et al.  Appetitive and Aversive Olfactory Learning in Humans Studied Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[47]  T. Davidson,et al.  Rapid clinical evaluation of anosmia. The alcohol sniff test. , 1997, Archives of otolaryngology--head & neck surgery.

[48]  E. Tulving,et al.  Frontal lobe damage produces episodic memory impairment , 1995, Journal of the International Neuropsychological Society.

[49]  R. Dolan,et al.  Dissociating prefrontal and hippocampal function in episodic memory encoding , 1997, Nature.

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

[51]  David P. Salmon,et al.  Olfactory thresholds are associated with degree of dementia in Alzheimer's disease , 1990, Neurobiology of Aging.

[52]  Integrating Clinical Assessment with Cognitive Neuroscience: Construct Validation of the California Verbal Learning Test. , 1988 .

[53]  Christine Fennema-Notestine,et al.  Left hippocampal volume loss in Alzheimer's disease is reflected in performance on odor identification: a structural MRI study. , 2003, Journal of the International Neuropsychological Society : JINS.

[54]  Sally Ferdon,et al.  The cerebellum and olfaction in the aging brain: a functional magnetic resonance imaging study , 2003, NeuroImage.

[55]  Daniel Tranel,et al.  A specific role for the human amygdala in olfactory memory. , 2003, Learning & memory.

[56]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[57]  Howard Eichenbaum,et al.  The hippocampus and memory for "what," "where," and "when". , 2004, Learning & memory.

[58]  E T Rolls,et al.  Sensory‐specific satiety‐related olfactory activation of the human orbitofrontal cortex , 2000, Neuroreport.

[59]  J. Price,et al.  Central olfactory connections in the macaque monkey , 1994, The Journal of comparative neurology.

[60]  Lars Nyberg,et al.  Mapping episodic memory , 1998, Behavioural Brain Research.

[61]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[62]  R. Cabeza,et al.  Handbook of functional neuroimaging of cognition , 2001 .