Top

Published in:

01-02-2010 | Research Article

Neuroanatomical correlates of olfactory performance

Authors: Johannes Frasnelli, Johan N. Lundström, Julie A. Boyle, Jelena Djordjevic, Robert J. Zatorre, Marilyn Jones-Gotman

Published in: Experimental Brain Research | Issue 1/2010

Abstract

We investigated associations between olfactory function and gray matter thickness in 46 healthy young subjects by means of an automated technique for measuring cortical thickness. We used an extended version of the Sniffin’ Sticks test to assess olfactory function, including odor threshold, concentration discrimination, quality discrimination, and odor identification. We observed a correlation between olfactory performance and cortical thickness of structures involved in earlier and later stages of chemosensory processing such as right medial orbitofrontal cortex, right insula, and adjacent cortex. Furthermore, we found significant bilateral correlations of olfactory performance with cortical thickness of areas around the central sulcus bilaterally, structures responsible for voluntary respiration and sniffing. In addition to expected general sex effects on cortical thickness, we observed areas, such as the entorhinal cortex, occipital cortex, intraparietal sulcus and insula (all in the right hemisphere), where the correlation between higher order olfactory functions and cortical thickness differed between women and men. These data demonstrate, for some neuroanatomical structures, a link between cortical thickness and olfactory function, in that thicker cortex is usually associated with better performance, but not always. This association between anatomy and olfactory performance suggests a possible biological explanation for the high degree of individual differences and sex effects observed in higher order olfactory tasks.

Ad-Dab’bagh Y, Singh V, Robbins S, Lerch J, Lyttelton O, Fombonne E, Evans AC (2005) Native-space cortical thickness measurement and the absence of correlation to cerebral volume. In: Zilles K (ed) 11th annual meeting of the organization for human brain mapping (OHBM), Toronto

Ad-Dab’bagh Y, Einarson D, Lyttelton O, Muehlboeck J-S, Mok K, Ivanov O, Vincent RD, Lepage C, Lerch J, Fombonne E, Evans AC (2006) The CIVET image-processing environment: a fully automated comprehensive pipeline for anatomical neuroimaging research. In: Corbetta M (ed) 12th annual meeting of the organization for human brain mapping, Florence (Italy)

Adler D, Gonzalez-Bermejo J, Duguet A, Demoule A, Le Pimpec-Barthes F, Hurbault A, Morelot-Panzini C, Similowski T (2009) Diaphragm pacing restores olfaction in tetraplegia. Eur Respir J 34(2):365–370CrossRefPubMed

Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11:805–821CrossRefPubMed

Bengtsson S, Berglund H, Gulyas B, Cohen E, Savic I (2001) Brain activation during odor perception in males and females. Neuroreport 12:2027–2033CrossRefPubMed

Bermudez P, Lerch JP, Evans AC, Zatorre RJ (2008) Neuroanatomical correlates of musicianship as revealed by cortical thickness and voxel-based morphometry. Cereb Cortex 19(7):1583–1596CrossRefPubMed

Boyle JA, Frasnelli J, Gerber J, Heinke M, Hummel T (2007) Cross-modal integration of intranasal stimuli: a functional magnetic resonance imaging study. Neuroscience 149:223–231CrossRefPubMed

Buschhuter D, Smitka M, Puschmann S, Gerber JC, Witt M, Abolmaali ND, Hummel T (2008) Correlation between olfactory bulb volume and olfactory function. Neuroimage 42:498–502CrossRefPubMed

Cain WS, Stevens JC, Nickou CM, Giles A, Johnston I, Garcia-Medina MR (1995) Life-span development of odor identification, learning, and olfactory sensitivity. Perception 24:1457–1472CrossRefPubMed

Cao J (1999) The size of the connected components of excursion sets of χ ² , t and F fields. Adv Appl Probab 31:579–595CrossRef

Cerf-Ducastel B, Murphy C (2003) FMRI brain activation in response to odors is reduced in primary olfactory areas of elderly subjects. Brain Res 986:39–53CrossRefPubMed

Choi YY, Shamosh NA, Cho SH, De Young CG, Lee MJ, Lee JM, Kim SI, Cho ZH, Kim K, Gray JR, Lee KH (2008) Multiple bases of human intelligence revealed by cortical thickness and neural activation. J Neurosci 28:10323–10329CrossRefPubMed

Chung MK, Taylor J (2004) Diffusion smoothing on brain surface via finite element method. Proc IEEE Int Symp Biomed Imaging 1:432–435

Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D inter-subject registration of MR volumetric data in standardized Talairach Space. J Comput Assist Tomogr 18:192–205CrossRefPubMed

Dade LA, Zatorre RJ, Jones-Gotman M (2002) Olfactory learning: convergent findings from lesion and brain imaging studies in humans. Brain 125:86–101CrossRefPubMed

Djordjevic J, Zatorre RJ, Petrides M, Boyle JA, Jones-Gotman M (2005) Functional neuroimaging of odor imagery. Neuroimage 24:791–801CrossRefPubMed

Doty RL, Shaman P, Dann M (1984) Development of the University of Pennsylvania smell identification test: a standardized microencapsulated test of olfactory function. Physiol Behav 32:489–502CrossRefPubMed

Doty RL, Applebaum SL, Zusho H, Settle RG (1985) A cross-cultural study on sex differences in odor identification ability. Neuropsychologia 23:667–672CrossRefPubMed

Evans KC, Shea SA, Saykin AJ (1999) Functional MRI localisation of central nervous system regions associated with volitional inspiration in humans. J Physiol 520(Pt 2):383–392CrossRefPubMed

Friston KJ, Worsley KJ, Frackowiak RSJ, Mazziotta JC, Evans AC (1994) Assessing the significance of focal activations using their spatial extent. Hum Brain Mapp 1:214–220CrossRef

Garcia-Falgueras A, Junque C, Gimenez M, Caldu X, Segovia S, Guillamon A (2006) Sex differences in the human olfactory system. Brain Res 1116:103–111CrossRefPubMed

Gottfried JA, Dolan RJ (2003) The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 39:375–386CrossRefPubMed

Gottfried JA, Zald DH (2005) On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res Rev 50:287–304PubMed

Grabner G, Janke AL, Budge MM, Smith D, Pruessner J, Collins DL (2006) Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults. Med Image Comput Comput Assist Interv Int Conf Med Image Comput Comput Assist Interv 9:58–66

Hillert L, Musabasic V, Berglund H, Ciumas C, Savic I (2007) Odor processing in multiple chemical sensitivity. Hum Brain Mapp 28:172–182CrossRefPubMed

Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (1997) “Sniffin’ sticks”: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 22:39–52CrossRefPubMed

Hummel T, Damm M, Vent J, Schmidt M, Theissen P, Larsson M, Klussmann JP (2003) Depth of olfactory sulcus and olfactory function. Brain Res 975:85–89CrossRefPubMed

Hummel T, Kobal G, Gudziol H, Mackay-Sim A (2007) Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3, 000 subjects. Eur Arch Otorhinolaryngol 264:237–243CrossRefPubMed

Hyde KL, Lerch JP, Zatorre RJ, Griffiths TD, Evans AC, Peretz I (2007) Cortical thickness in congenital amusia: when less is better than more. J Neurosci 27:13028–13032CrossRefPubMed

Im K, Lee JM, Lee J, Shin YW, Kim IY, Kwon JS, Kim SI (2006) Gender difference analysis of cortical thickness in healthy young adults with surface-based methods. Neuroimage 31:31–38CrossRefPubMed

Jiang J, Zhu W, Shi F, Liu Y, Li J, Qin W, Li K, Yu C, Jiang T (2009) Thick visual cortex in the early blind. J Neurosci 29:2205–2211CrossRefPubMed

Johnson BN, Mainland JD, Sobel N (2003) Rapid olfactory processing implicates subcortical control of an olfactomotor system. J Neurophysiol 90:1084–1094CrossRefPubMed

Jones-Gotman M, Zatorre RJ (1988) Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia 26:387–400CrossRefPubMed

Kim JS, Singh V, Lee JK, Lerch J, Ad-Dab’bagh Y, MacDonald D, Lee JM, Kim SI, Evans AC (2005) Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification. Neuroimage 27:210–221CrossRefPubMed

Koritnik B, Azam S, Andrew CM, Leigh PN, Williams SC (2008) Imaging the brain during sniffing: a pilot fMRI study. Pulm Pharmacol Ther 22(2):97–101CrossRefPubMed

Larsson M (1997) Semantic factors in episodic recognition of common odors in early and late adulthood: a review. Chem Senses 22:623–633CrossRefPubMed

Larsson M, Lovden M, Nilsson LG (2003) Sex differences in recollective experience for olfactory and verbal information. Acta Psychol 112:89–103CrossRef

Laska M, Genzel D, Wieser A (2005) The number of functional olfactory receptor genes and the relative size of olfactory brain structures are poor predictors of olfactory discrimination performance with enantiomers. Chem Senses 30:171–175CrossRefPubMed

Lerch JP, Evans AC (2005) Cortical thickness analysis examined through power analysis and a population simulation. Neuroimage 24:163–173CrossRefPubMed

Livermore A, Hummel T (2004) The influence of training on chemosensory event-related potentials and interactions between the olfactory and trigeminal systems. Chem Senses 29:41–51CrossRefPubMed

Luders E, Narr KL, Thompson PM, Rex DE, Woods RP, Deluca H, Jancke L, Toga AW (2006) Gender effects on cortical thickness and the influence of scaling. Hum Brain Mapp 27:314–324CrossRefPubMed

Lundstrom JN, Boyle JA, Jones-Gotman M (2008) Body position-dependent shift in odor percept present only for perithreshold odors. Chem Senses 33:23–33CrossRefPubMed

MacDonald D, Kabani N, Avis D, Evans AC (2000) Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. Neuroimage 12:340–356CrossRefPubMed

Mainland J, Sobel N (2006) The sniff is part of the olfactory percept. Chem Senses 31:181–196CrossRefPubMed

Mainland JD, Bremner EA, Young N, Johnson BN, Khan RM, Bensafi M, Sobel N (2002) Olfactory plasticity: one nostril knows what the other learns. Nature 419:802CrossRefPubMed

Miyanari A, Kaneoke Y, Ihara A, Watanabe S, Osaki Y, Kubo T, Kato A, Yoshimine T, Sagara Y, Kakigi R (2006) Neuromagnetic changes of brain rhythm evoked by intravenous olfactory stimulation in humans. Brain Topogr 18:189–199CrossRefPubMed

Miyanari A, Kaneoke Y, Noguchi Y, Honda M, Sadato N, Sagara Y, Kakigi R (2007) Human brain activation in response to olfactory stimulation by intravenous administration of odorants. Neurosci Lett 423:6–11CrossRefPubMed

Moran DT, Jafek BW, Eller PM, Rowley JC (1992) Ultrastructural histopathology of human olfactory dysfunction. Microsc Res Tech 23:103–110CrossRefPubMed

Narr KL, Woods RP, Thompson PM, Szeszko P, Robinson D, Dimtcheva T, Gurbani M, Toga AW, Bilder RM (2007) Relationships between IQ and regional cortical gray matter thickness in healthy adults. Cereb Cortex 17:2163–2171CrossRefPubMed

Pardini M, Huey ED, Cavanagh AL, Grafman J (2009) Olfactory function in corticobasal syndrome and frontotemporal dementia. Arch Neurol 66:92–96CrossRefPubMed

Plailly J, Radnovich AJ, Sabri M, Royet JP, Kareken DA (2007) Involvement of the left anterior insula and frontopolar gyrus in odor discrimination. Hum Brain Mapp 28:363–372CrossRefPubMed

Rombaux P, Mouraux A, Bertrand B, Nicolas G, Duprez T, Hummel T (2006) Olfactory function and olfactory bulb volume in patients with postinfectious olfactory loss. Laryngoscope 116:436–439CrossRefPubMed

Savic I, Gulyas B (2000) PET shows that odors are processed both ipsilaterally and contralaterally to the stimulated nostril. Neuroreport 11:2861–2866CrossRefPubMed

Savic I, Gulyas B, Larsson M, Roland P (2000) Olfactory functions are mediated by parallel and hierarchical processing. Neuron 26:735–745CrossRefPubMed

Savic I, Gulyas B, Berglund H (2002) Odorant differentiated pattern of cerebral activation: comparison of acetone and vanillin. Hum Brain Mapp 17:17–27CrossRefPubMed

Simonyan K, Saad ZS, Loucks TM, Poletto CJ, Ludlow CL (2007) Functional neuroanatomy of human voluntary cough and sniff production. Neuroimage 37:401–409CrossRefPubMed

Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97CrossRefPubMed

Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, Sullivan EV, Gabrieli JD (1998) Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392:282–286CrossRefPubMed

Sobel N, Prabhakaran V, Zhao Z, Desmond JE, Glover GH, Sullivan EV, Gabrieli JD (2000) Time course of odorant-induced activation in the human primary olfactory cortex. J Neurophysiol 83:537–551PubMed

Sowell ER, Peterson BS, Kan E, Woods RP, Yoshii J, Bansal R, Xu D, Zhu H, Thompson PM, Toga AW (2007) Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. Cereb Cortex 17:1550–1560CrossRefPubMed

Tohka J, Zijdenbos A, Evans A (2004) Fast and robust parameter estimation for statistical partial volume models in brain MRI. Neuroimage 23:84–97CrossRefPubMed

Walhovd KB, Fjell AM, Dale AM, Fischl B, Quinn BT, Makris N, Salat D, Reinvang I (2006) Regional cortical thickness matters in recall after months more than minutes. Neuroimage 31:1343–1351CrossRefPubMed

Wang J, Eslinger PJ, Smith MB, Yang QX (2005) Functional magnetic resonance imaging study of human olfaction and normal aging. J Gerontol A Biol Sci Med Sci 60:510–514PubMed

Wicker B, Keysers C, Plailly J, Royet JP, Gallese V, Rizzolatti G (2003) Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron 40:655–664CrossRefPubMed

Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC (1996) A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4:58–73CrossRef

Zatorre RJ, Jones-Gotman M (2000) Functional imaging of the chemical senses. In: Toga AW, Mazziotta JC (eds) Brain mapping: the applications. Academic Press, San Diego, pp 403–424CrossRef

Zatorre RJ, Jones-Gotman M, Evans AC, Meyer E (1992) Functional localization and lateralization of human olfactory cortex. Nature 360:339–340CrossRefPubMed

Zelano C, Bensafi M, Porter J, Mainland J, Johnson B, Bremner E, Telles C, Khan R, Sobel N (2005) Attentional modulation in human primary olfactory cortex. Nat Neurosci 8:114–120CrossRefPubMed

Zijdenbos A, Forghani R, Evans AC (1998) Automatic quantification of ms lesions in 3D MRI brain data sets: validation of INSECT. In: Wells WM, Colchester V, Delp S (eds) Medical image computing and computer-assisted interventation (MICCAI98). Springer, Heidelberg, pp 439–448CrossRef

Zijdenbos AP, Forghani R, AC E (2002) Automatic pipeline analysis of 3-D MRI data for clinical trials: application to multiple sclerosis. IEEE Trans Med Imaging 21(10):1280–1291CrossRefPubMed

Title: Neuroanatomical correlates of olfactory performance
Authors: Johannes Frasnelli
Johan N. Lundström
Julie A. Boyle
Jelena Djordjevic
Robert J. Zatorre
Marilyn Jones-Gotman
Publication date: 01-02-2010
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 1/2010
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-009-1999-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Neuroanatomical correlates of olfactory performance

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2010

Presaccadic attention interferes with feature detection

Two mechanisms underlying inhibition of return

Control of dynamic stability during adaptation to gait termination on a slippery surface

Why do humans make antisaccade errors?

Reach-to-grasp movement as a minimization process

Head stability during quiet sitting in children with cerebral palsy: effect of vision and trunk support