Rapidly acquired multisensory association in the olfactory cortex

Brain and Behavior

Volumn 5, Issue 11, 2015, Pages

  Karunanayaka, Prasanna R ^a   Wilson, Donald A ^b,c   Vasavada, Megha ^a   Wang, Jianli ^a   Martinez, Brittany ^a   Tobia, Michael J ^a   Kong, Lan ^a   Eslinger, Paul ^a   Yang, Qing X ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Associative learning; fMRI; ICA; Odor intensity; Unified SEM

Indexed keywords

ADULT; ARTICLE; ASSOCIATION; BOLD SIGNAL; BREATHING PATTERN; CLINICAL ARTICLE; COGNITIVE FUNCTION TEST; CORTICAL AMYGDALA; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMIC PARAMETERS; HUMAN; MALE; NEUROIMAGING; ODOR; ODOR RECOGNITION TEST; OLFACTOMETER; OLFACTORY CORTEX; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; SENSORY CORTEX; SMELLING; SPATIOTEMPORAL ANALYSIS; STATE DEPENDENT LEARNING; STRUCTURAL EQUATION MODELING; VISUAL STIMULATION; BRAIN MAPPING; CONDITIONED REFLEX; CYTOLOGY; HIPPOCAMPUS; LEARNING; MEMORY; NUCLEAR MAGNETIC RESONANCE IMAGING; OLFACTORY RECEPTOR NEURON; PHOTOSTIMULATION; PHYSIOLOGY;

FRAGRANCE;

ADULT; ASSOCIATION LEARNING; BRAIN MAPPING; CONDITIONING, CLASSICAL; CUES; FEMALE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; ODORANTS; OLFACTORY CORTEX; OLFACTORY RECEPTOR NEURONS; PHOTIC STIMULATION; SMELL;

EID: 84954366750     PISSN: None     EISSN: 21623279     Source Type: Journal    
DOI: 10.1002/brb3.390     Document Type: Article

References (68)

1. Allen, W. 1936. Studies on the level of anesthesia for the olfactory and trigeminal respiratory reflexes in dogs and rabbits. Am. J. Physiol. 115:579-587.
2. Anderson, A. K., and N. Sobel . 2003. Dissociating intensity from valence as sensory inputs to emotion. Neuron 39:581-583.
3. Bartels, A., and S. Zeki . 2004. The chronoarchitecture of the human brain-natural viewing conditions reveal a time-based anatomy of the brain. Neuroimage 22:419-433.
4. Bollen, K. A. 1989. Structural equations with latent variables. John Wiley & Sons, New York.
5. Bollen, K. A., and J. S. Long . 1993. Testing structural equation models. Sage, Thousand Oaks, CA.
6. Calhoun, V. D., J. J. Pekar, and G. D. Pearlson . 2004. Alcohol intoxication effects on simulated driving: exploring alcohol-dose effects on brain activation using functional MRI. Neuropsychopharmacology 29:2097-2017.
7. Cerf-Ducastel, B., and C. Murphy . 2006. Neural substrates of cross-modal olfactory recognition memory: an fMRI study. Neuroimage 31:386-396.
8. Collins, D. L., A. P. Zijdenbos, V. Kollokian, J. G. Sled, N. J. Kabani, C. J. Holmes, et al. 1998. Design and construction of a realistic digital brain phantom. IEEE Trans. Med. Imaging 17:463-468.
9. Doty, R. L., P. Shaman, S. L. Applebaum, R. Giberson, L. Siksorski, and L. Rosenberg . 1984. Smell identification ability: changes with age. Science 226:1441-1443.
10. Duann, J. R., T. P. Jung, W. J. Kuo, T. C. Yeh, S. Makeig, J. C. Hsieh, et al. 2002. Single-trial variability in event-related BOLD signals. Neuroimage 15:823-835.
11. Eichele, T., S. Debener, V. D. Calhoun, K. Specht, A. K. Engel, K. Hugdahl, et al. 2008. Prediction of human errors by maladaptive changes in event-related brain networks. Proc. Natl. Acad. Sci. USA 105:6173-6178.
12. Field, T., M. Diego, M. Hernandez-Reif, W. Cisneros, L. Feijo, Y. Vera, et al. 2005. Lavender fragrance cleansing gel effects on relaxation. Int. J. Neurosci. 115:207-222.
13. Friston, K. J. 2011. Functional and effective connectivity: a review. Brain Connect. 1:13-36.
14. Gates, K. M., P. C. Molenaar, et al. 2011. Extended unified SEM approach for modeling event-related fMRI data. NeuroImage 54:1151-1158.
15. Gates, K. M., and P. C. Molenaar . 2012. Group search algorithm recovers effective connectivity maps for individuals in homogeneous and heterogeneous samples. NeuroImage 63:310-319.
16. Ghazanfar, A. A., and C. E. Schroeder . 2006. Is neocortex essentially multisensory? Trends Cogn. Sci. 10:278-285.
17. Gottfried, J. A. 2010. Central mechanisms of odour object perception. Nat. Rev. Neurosci. 11:628-641.
18. Gottfried, J. A., and R. J. Dolan . 2003. The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 39:375-386.
19. Gottfried, J. A., J. O'Doherty, and R. J. Dolan . 2003. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301:1104-1107.
20. Gottfried, J. A., A. P. Smith, M. D. Rugg, and R. J. Dolan . 2004. Remembrance of odors past: human olfactory cortex in cross-modal recognition memory. Neuron 42:687-695.
21. Goutte, C., F. A. Nielsen, and L. K. Hansen . 2000. Modeling the haemodynamic response in fMRI using smooth FIR filters. IEEE Trans. Med. Imaging 19:1188-1201.
22. Guzman-Ramos, K., and F. Bermudez-Rattoni . 2012. Interplay of amygdala and insular cortex during and after associative taste aversion memory formation. Rev. Neurosci. 23:463-471.
23. Henke, K. 2010. A model for memory systems based on processing modes rather than consciousness. Nat. Rev. Neurosci. 11:523-532.
24. Himberg, J., A. Hyvarinen, and F. Esposito . 2004. Validating the independent components of neuroimaging time series via clustering and visualization. Neuroimage 22:1214-1222.
25. Hyvarinen, A. 1999. Fast and robust fixed-point algorithms for independent component analysis. IEEE Trans. Neural Netw. 10:626-634.
26. Joreskog, K. G., and D. Sorbom . 1996. LISREL 8. User's reference guide. Scientific Software International, Chicago.
27. Karunanayaka, P. R., S. K. Holland, V. J. Schmithorst, A. Solodkin, E. E. Chen, J. P. Szaflarski, et al. 2007. Age-related connectivity changes in fMRI data from children listening to stories. Neuroimage 34:349-360.
28. Karunanayaka, P., V. J. Schmithorst, J. Vannest, J. P. Szaflarski, E. Plante, and S. K. Holland . 2010. A group independent component analysis of covert verb generation in children: a functional magnetic resonance imaging study. Neuroimage 51:472-487.
29. Karunanayaka, P., P. J. Eslinger, J. L. Wang, C. W. Weitekamp, S. Molitoris, K. M. Gates, et al. 2014. Networks involved in olfaction and their dynamics using independent component analysis and unified structural equation modeling. Hum. Brain Mapp. 35:2055-2072.
30. Kim, J., W. Zhu, et al. 2007. Unified structural equation modeling approach for the analysis of multisubject, multivariate functional MRI data. Hum. Brain Mapp. 28:85-93.
31. Koenig, O., G. Bourron, and J. P. Royet . 2000. Evidence for separate perceptive and semantic memories for odours: a priming experiment. Chem. Senses 25:703-708.
32. Li, W., E. Luxenberg, T. Parrish, and J. A. Gottfried . 2006. Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbitofrontal cortices. Neuron 52:1097-1108.
33. Lindquist, M. A., J. Meng Loh, L. Y. Atlas, and T. D. Wager . 2009. Modeling the hemodynamic response function in fMRI: efficiency, bias and mis-modeling. Neuroimage 45:S187-S198.
34. Maier, J. X., M. Wachowiak, and D. B. Katz . 2012. Chemosensory convergence on primary olfactory cortex. J. Neurosci. 32:17037-17047.
35. Mesulam, M. M., and E. J. Mutshon . 1985. The insula of Reil in man and monkey. Architectonics, connectivity and function. Plenum Press, New York.
36. Ollinger, J. M., M. Corbetta, and G. L. Shulman . 2001. Separating processes within a trial in event-related functional MRI. Neuroimage 13:218-229.
37. Olofsson, J. K., R. S. Hurley, N. E. Bowman, X. Bao, M. M. Mesulam, and J. A. Gottfried . 2014. A designated odor-language integration system in the human brain. J. Neurosci. 34:14864-14873.
38. Olsson, M. J., and M. Friden . 2001. Evidence of odor priming: edibility judgements are primed differently between the hemispheres. Chem. Senses 26:117-123.
39. Olsson, M. J., M. Faxbrink, and F. U. Johnson . 2002. Repetion priming in odor memory. Pp 246-260 in C. Rouby, B. Schaal, D. Dubois, R. Gervais, A. Holly, eds. Olfaction, taste and cognition. Published in the United States of America by Cambridge University Press, New York.
40. Osterbauer, R. A., P. M. Matthews, M. Jenkinson, C. F. Beckmann, P. C. Hansen, and G. A. Calvert . 2005. Color of scents: chromatic stimuli modulate odor responses in the human brain. J. Neurophysiol. 93:3434-3441.
41. Patton, H. D., ed. 1960. Taste, olfaction and visceral sensation. in Medical physiology and biophysics Ch. 16. Saunders, Philadelphia.
42. Rabin, M. D., and W. S. Cain . 1984. Odor recognition: familiarity, identifiability, and encoding consistency. J. Exp. Psychol. Learn. Mem. Cogn. 10:316-325.
43. Royet, J. P., O. Koenig, M. C. Gregoire, L. Cinotti, F. Lavenne, D. Le Bars, et al. 1999. Functional anatomy of perceptual and semantic processing for odors. J. Cogn. Neurosci. 11:94-109.
44. Royet, J. P., J. Hudry, D. H. Zald, D. Godinot, M. C. Gregoire, F. Lavenne, et al. 2001. Functional neuroanatomy of different olfactory judgments. Neuroimage 13:506-519.
45. Savic, I., B. Gulyas, M. Larsson, and P. Roland . 2000. Olfactory functions are mediated by parallel and hierarchical processing. Neuron 26:735-745.
46. Schendan, H. E., M. M. Searl, R. J. Melrose, and C. E. Stern . 2003. An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 37:1013-1025.
47. Schmithorst, V. J., S. K. Holland, and E. Plante . 2006. Cognitive modules utilized for narrative comprehension in children: a functional magnetic resonance imaging study. Neuroimage 29:254-266.
48. Shankar, M., C. Simons, B. Shiv, S. McClure, C. A. Levitan, and C. Spence . 2010. An expectations-based approach to explaining the cross-modal influence of color on orthonasal olfactory identification: the influence of the degree of discrepancy. Atten. Percept. Psychophys. 72:1981-1993.
49. Small, D. M. 2012. Flavor is in the brain. Physiol. Behav. 107:540-552.
50. Smeets, M. A., and G. B. Dijksterhuis . 2014. Smelly primes - when olfactory primes do or do not work. Front. Psychol. 5:96.
51. Stevenson, R. J. 2001. Perceptual learning with odors: implications for psychological accounts of odor quality perception. Psychon. Bull. Rev. 8:708-712.
52. Stevenson, R. J., and M. Oaten . 2008. The effect of appropriate and inappropriate stimulus color on odor discrimination. Percept. Psychophys. 70:640-646.
53. Sullivan, R. M., J. L. McGaugh, and M. Leon . 1991. Norepinephrine-induced plasticity and one-trial olfactory learning in neonatal rats. Brain Res. Dev. Brain Res. 60:219-228.
54. Tabert, M. H., J. Steffener, M. W. Albers, D. W. Kern, M. Michael, H. Tang, et al. 2007. Validation and optimization of statistical approaches for modeling odorant-induced fMRI signal changes in olfactory-related brain areas. Neuroimage 34:1375-1390.
55. Tzourio-Mazoyer, N., B. Landeau, D. Papathanassiou, F. Crivello, O. Etard, N. Delcroix, et al. 2002. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273-289.
56. Vasavada, M. M., J. Wang, P. J. Eslinger, D. J. Gill, X. Sun, P. Karunanayaka, and Q. X. Yang . 2015. Olfactory cortex degeneration in Alzheimer's disease and mild cognitive impairment. J. Alzheimers Dis. 45:947-958.
57. Veldhuizen, M. G., T. G. Shepard, M. F. Wang, and L. E. Marks . 2010. Coactivation of gustatory and olfactory signals in flavor perception. Chem. Senses 35:121-133.
58. Wang, J., P. J. Eslinger, R. L. Doty, E. K. Zimmerman, R. Grunfeld, X. Sun, et al. 2010. Olfactory deficit detected by fMRI in early Alzheimer's disease. Brain Res. 1357:184-194.
59. Wang, J., X. Sun, and Q. X. Yang . 2014. Methods for olfactory fMRI studies: Implication of respiration. Hum. Brain Mapp. 35:3616-3624.
60. Wesson, D. W., and D. A. Wilson . 2010. Smelling sounds: olfactory-auditory sensory convergence in the olfactory tubercle. J. Neurosci. 30:3013-3021.
61. Wilson, D. A. 2003. Rapid, experience-induced enhancement in odorant discrimination by anterior piriform cortex neurons. J. Neurophysiol. 90:65-72.
62. Wilson, D. A., and R. J. Stevenson . 2006. Learning to smell. The Johns Hopkins University Press, Baltimore.
63. Wu, K. N., B. K. Tan, J. D. Howard, D. B. Conley, and J. A. Gottfried . 2012. Olfactory input is critical for sustaining odor quality codes in human orbitofrontal cortex. Nat. Neurosci. 15:1313-1319.
64. Yeshurun, Y., Y. Dudai, and N. Sobel . 2008. Working memory across nostrils. Behav. Neurosci. 122:1031-1037.
65. Zelano, C., M. Bensafi, J. Porter, J. Mainland, B. Johnson, E. Bremner, et al. 2005. Attentional modulation in human primary olfactory cortex. Nat. Neurosci. 8:114-120.
66. Zelano, C., J. Montag, R. Khan, and N. Sobel . 2009. A specialized odor memory buffer in primary olfactory cortex. PLoS One 4:e4965.
67. Zellner, D. A., A. M. Bartoli, and R. Eckard . 1991. Influence of color on odor identification and liking ratings. Am. J. Psychol. 104:547-561.
68. Zhou, W., X. Zhang, J. Chen, L. Wang, and D. Chen . 2012. Nostril-specific olfactory modulation of visual perception in binocular rivalry. J. Neurosci. 32:17225-17229.