The cerebellum and olfaction in the aging brain: a functional magnetic resonance imaging study

The present study investigated activation of distinct cerebellar regions as a result of olfactory stimulation in healthy young and elderly adults using functional magnetic resonance imaging (fMRI). Ten young and 10 elderly adults were imaged using a 1.5-TMR scanner. The odorant amyl acetate was delivered in 12-s on, 40-s off cycles. Throughout the scan participants responded with a button press at first detection of each stimulus interval followed by a second button press upon odorant extinction. Images were processed with AFNI software. Elderly participants showed significantly decreased cerebellar activation in both the superior semilunar lobule (Crus I) and the inferior semilunar lobule (Crus II), two of three previously identified regions of interest for odor processing, compared to young adults. Interestingly, both groups showed similar levels of activation in the third region of interest, the posterior quadrangular lobule (VI), although the elderly showed more variability than the young did. Previous research identifying this area to be involved in attention may reflect the possibility that elderly adults engaged in olfactory tasks may show more variability than young participants in the degree of attentional demands needed for these tasks as a result of decreased olfactory abilities.

[1]  Alan C. Evans,et al.  Flavor processing: more than the sum of its parts , 1997, Neuroreport.

[2]  E. Courchesne,et al.  A new role for the cerebellum in cognitive operations. , 1992, Behavioral neuroscience.

[3]  J. Schmahmann,et al.  The cerebellar cognitive affective syndrome. , 1998, Brain : a journal of neurology.

[4]  Paul R. Solomon,et al.  Lesions of the middle cerebellar peduncle disrupt acquisition and retention of the rabbit's classically conditioned nictitating membrane response. , 1987, Behavioral neuroscience.

[5]  C. Murphy,et al.  Nutrition and chemosensory perception in the elderly. , 1993, Critical reviews in food science and nutrition.

[6]  J. Desmond,et al.  Neuroimaging studies of the cerebellum: language, learning and memory , 1998, Trends in Cognitive Sciences.

[7]  D. Yousem,et al.  The effect of age on odor-stimulated functional MR imaging. , 1999, AJNR. American journal of neuroradiology.

[8]  M. Laska,et al.  Perception of trigeminal chemosensory qualities in the elderly. , 2001, Chemical senses.

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

[10]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.

[11]  C. Murphy,et al.  Age-related effects on the threshold, psychophysical function, and pleasantness of menthol. , 1983, Journal of gerontology.

[12]  W. T. Thach What is the role of the cerebellum in motor learning and cognition? , 1998, Trends in Cognitive Sciences.

[13]  S. Markison,et al.  Psychophysical Assessment of Chemosensory Disorders in Clinical Populations , 1994 .

[14]  C. Fennema-Notestine,et al.  Effects of age on tissues and regions of the cerebrum and cerebellum , 2001, Neurobiology of Aging.

[15]  Gary H. Glover,et al.  Odorant-Induced and Sniff-Induced Activation in the Cerebellum of the Human , 1998, The Journal of Neuroscience.

[16]  W S Cain,et al.  Clinical evaluation of olfaction. , 1983, American journal of otolaryngology.

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

[18]  J. Covington,et al.  Olfactory event-related potentials and aging: normative data. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[20]  David G. Lavond,et al.  Trace conditioning: Abolished by cerebellar nuclear lesions but not lateral cerebellar cortex aspirations , 1985, Brain Research.

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

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

[23]  S S Schiffman,et al.  Perception of taste and smell in elderly persons. , 1993, Critical reviews in food science and nutrition.

[24]  J M Bower,et al.  Control of sensory data acquisition. , 1997, International review of neurobiology.

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

[26]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[27]  T. Ebner,et al.  Functional magnetic resonance imaging of cerebellar activation during the learning of a visuomotor dissociation task , 1996, Human brain mapping.

[28]  Anna Bacon Moore,et al.  A Demonstration of Classical Conditioning of the Human Eyeblink to an Olfactory Stimulus , 1999, Physiology & Behavior.

[29]  T. Thesen,et al.  Age-related changes in olfactory processing detected with olfactory event-related brain potentials using velopharyngeal closure and natural breathing. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

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

[32]  S. Schiffman,et al.  Food recognition by the elderly. , 1977, Journal of gerontology.

[33]  R. Doty,et al.  Smell identification ability: changes with age. , 1984, Science.

[34]  M J Brammer,et al.  Functional MR imaging during odor stimulation: preliminary data. , 1997, Radiology.

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

[36]  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.

[37]  M. D’Esposito,et al.  The Effect of Normal Aging on the Coupling of Neural Activity to the Bold Hemodynamic Response , 1999, NeuroImage.

[38]  J Xiong,et al.  Lateral cerebellar hemispheres actively support sensory acquisition and discrimination rather than motor control. , 1997, Learning & memory.

[39]  Charles D. Smith,et al.  Neural substrates of facial emotion processing using fMRI. , 2001, Brain research. Cognitive brain research.

[40]  E. Courchesne,et al.  Prediction and preparation, fundamental functions of the cerebellum. , 1997, Learning & memory.

[41]  Gerd Kobal,et al.  Pain-related electrical potentials of the human nasal mucosa elicited by chemical stimulation , 1985, Pain.

[42]  C. Jack,et al.  Rate of medial temporal lobe atrophy in typical aging and Alzheimer's disease , 1998, Neurology.

[43]  J. Bower,et al.  Cerebellum Implicated in Sensory Acquisition and Discrimination Rather Than Motor Control , 1996, Science.

[44]  E. Courchesne,et al.  Attentional Activation of the Cerebellum Independent of Motor Involvement , 1997, Science.

[45]  A. Fawcett,et al.  Cerebellar Tests Differentiate Between Groups of Poor Readers With and Without IQ Discrepancy , 2001, Journal of learning disabilities.

[46]  J L Andersson,et al.  Brain regions associated with episodic retrieval in normal aging and Alzheimer’s disease , 1999, Neurology.

[47]  William S. Cain,et al.  Odor identification: The blind are better , 1986, Physiology & Behavior.

[48]  T Lindvall,et al.  Perceived intensity of odor as a function of time of adaptation. , 1967, Scandinavian journal of psychology.

[49]  Alan C. Evans,et al.  MRI Atlas of the Human Cerebellum , 2000 .

[50]  S. Nordin,et al.  Odor identification as an early marker for Alzheimer's disease: impact of lexical functioning and detection sensitivity. , 1995, Journal of clinical and experimental neuropsychology.

[51]  Ivanka Savic,et al.  Processing of odorous signals in humans , 2001, Brain Research Bulletin.

[52]  K. Kaissling,et al.  Elementary Receptor Potentials of Insect Olfactory Cells , 1994 .

[53]  L. Bellak,et al.  Geriatric psychiatry : a handbook for psychiatrists and primary care physicians , 1976 .