The scent of salience - Is there olfactory-trigeminal conditioning in humans?

NeuroImage

Volumn 77, Issue , 2013, Pages 93-104

  Moessnang, C ^a,b   Pauly, K ^a,b   Kellermann, T ^a,b   Kramer J ^a,b   Finkelmeyer, A ^c   Hummel, T ^d   Siegel, S J ^e   Schneider, F ^a,b   Habel, U ^a,b  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b JARA TRANSLATIONAL BRAIN MEDICINE   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Chemosensation; FMRI; Functional connectivity; Pavlovian conditioning; Salience

Indexed keywords

ACCURACY; ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONDITIONING; CONTROLLED STUDY; FEMALE; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; MOTOR CONTROL; NEUROIMAGING; OLFACTORY CORTEX; PARIETAL LOBE; PAVLOVIAN CONDITIONING; PRIORITY JOURNAL; SIGNAL DETECTION; SKIN CONDUCTANCE; STIMULUS RESPONSE; TASK PERFORMANCE; TEMPORAL LOBE;

ADULT; BRAIN; BRAIN MAPPING; CONDITIONING, CLASSICAL; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; OLFACTORY PERCEPTION; PAIN; TRIGEMINAL NERVE;

EID: 84876716541     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.03.049     Document Type: Article

References (100)

1. Albrecht J., Kopietz R., Frasnelli J., Wiesmann M., Hummel T., Lundstrom J.N. The neuronal correlates of intranasal trigeminal function-an ALE meta-analysis of human functional brain imaging data. Brain Res. Rev. 2010, 62:183-196.
2. Ashburner J., Friston K.J. Unified segmentation. NeuroImage 2005, 26:839-851.
3. Baas D., Aleman A., Kahn R.S. Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Res. Rev. 2004, 45:96-103.
4. Beckmann M., Johansen-Berg H., Rushworth M.F. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J. Neurosci. 2009, 29:1175-1190.
5. Benedek M., Kaernbach C. Decomposition of skin conductance data by means of nonnegative deconvolution. Psychophysiology 2010, 47:647-658.
6. Bensafi M., Frasnelli J., Reden J., Hummel T. The neural representation of odor is modulated by the presence of a trigeminal stimulus during odor encoding. Clin. Neurophysiol. 2007, 118:696-701.
7. Best A.R., Wilson D.A. Coordinate synaptic mechanisms contributing to olfactory cortical adaptation. J. Neurosci. 2004, 24:652-660.
8. Bouton M.E. Context and behavioral processes in extinction. Learn. Mem. 2004, 11:485-494.
9. Büchel C., Dolan R.J., Armony J.L., Friston K.J. Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging. J. Neurosci. 1999, 19:10869-10876.
10. Bulsing P.J., Smeets M.A., Hummel T., van den Hout M.A. Influence of chemosensory pain-expectancy on olfactory event-related potentials. NeuroImage 2007, 38:164-170.
11. Bulsing P.J., Smeets M.A., Gemeinhardt C., Laverman M., Schuster B., Van den Hout M.A., Hummel T. Irritancy expectancy alters odor perception: evidence from olfactory event-related potential research. J. Neurophysiol. 2010, 104:2749-2756.
12. Busch C.J., Evans I.M. The effectiveness of electric shock and foul odor as unconditioned stimuli in classical aversive conditioning. Behav. Res. Ther. 1977, 15:167-175.
13. Carmichael S.T., Clugnet M.C., Price J.L. Central olfactory connections in the macaque monkey. J. Comp. Neurol. 1994, 346:403-434.
14. Caspers S., Geyer S., Schleicher A., Mohlberg H., Amunts K., Zilles K. The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability. NeuroImage 2006, 33:430-448.
15. Cauda F., D'Agata F., Sacco K., Duca S., Geminiani G., Vercelli A. Functional connectivity of the insula in the resting brain. NeuroImage 2011, 55:8-23.
16. Choi H.J., Zilles K., Mohlberg H., Schleicher A., Fink G.R., Armstrong E., Amunts K. Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus. J. Comp. Neurol. 2006, 495:53-69.
17. Costafreda S.G., Brammer M.J., David A.S., Fu C.H. Predictors of amygdala activation during the processing of emotional stimuli: a meta-analysis of 385 PET and fMRI studies. Brain Res. Rev. 2008, 58:57-70.
18. Craig A.D. How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10:59-70.
19. Cunningham W.A., Brosch T. Motivational salience: amygdala tuning from traits, needs, values, and goals. Curr. Dir. Psychol. Sci. 2012, 21:45-59.
20. d'Acremont M., Lu Z.L., Li X., Van der Linden M., Bechara A. Neural correlates of risk prediction error during reinforcement learning in humans. NeuroImage 2009, 47:1929-1939.
21. Dalton P. Psychophysical and behavioral characteristics of olfactory adaptation. Chem. Senses 2000, 25:487-492.
22. Damasio A.R. Descartes' error and the future of human life. Sci. Am. 1994, 271:144.
23. Dawson M.E., Reardon P. Construct validity of recall and recognition postconditioning measures of awareness. J. Exp. Psychol. 1973, 98:308-315.
24. Diedrichsen J., Balsters J.H., Flavell J., Cussans E., Ramnani N. A probabilistic MR atlas of the human cerebellum. NeuroImage 2009, 46:39-46.
25. Doty R.L., Brugger W.E., Jurs P.C., Orndorff M.A., Snyder P.J., Lowry L.D. Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans. Physiol. Behav. 1978, 20:175-185.
26. Downar J., Mikulis D.J., Davis K.D. Neural correlates of the prolonged salience of painful stimulation. NeuroImage 2003, 20:1540-1551.
27. Drabant E.M., Kuo J.R., Ramel W., Blechert J., Edge M.D., Cooper J.R., Goldin P.R., Hariri A.R., Gross J.J. Experiential, autonomic, and neural responses during threat anticipation vary as a function of threat intensity and neuroticism. NeuroImage 2011, 55:401-410.
28. Dunsmoor J.E., Bandettini P.A., Knight D.C. Impact of continuous versus intermittent CS-UCS pairing on human brain activation during Pavlovian fear conditioning. Behav. Neurosci. 2007, 121:635-642.
29. Eckert M.A., Menon M., Walczac A., Ahlstrom J., Denslow S., Horwitz A., Dubno J.R. At the heart of the ventral attentional system: the right anterior insula. Hum. Brain Mapp. 2009, 30:2530-2541.
30. Eickhoff S.B., Heim S., Zilles K., Amunts K. Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. NeuroImage 2006, 32:570-582.
31. Eickhoff S.B., Schleicher A., Zilles K., Amunts K. The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. Cereb. Cortex 2006, 16:254-267.
32. Farrell M.J., Laird A.R., Egan G.F. Brain activity associated with painfully hot stimuli applied to the upper limb: a meta-analysis. Hum. Brain Mapp. 2005, 25:129-139.
33. Frasnelli J., Hummel T., Berg J., Huang G., Doty R.L. Intranasal localizability of odorants: influence of stimulus volume. Chem. Senses 2011, 36:405-410.
34. Geyer S. The microstructural border between the motor and the cognitive domain in the human cerebral cortex. Adv. Anat. Embryol. Cell Biol. 2004, 174(I-VIII):1-89.
35. Geyer S., Ledberg A., Schleicher A., Kinomura S., Schormann T., Burgel U., Klingberg T., Larsson J., Zilles K., Roland P.E. Two different areas within the primary motor cortex of man. Nature 1996, 382:805-807.
36. Geyer S., Schleicher A., Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex. NeuroImage 1999, 10:63-83.
37. Gottfried J.A. Smell: central nervous processing. Adv. Otorhinolaryngol. 2006, 63:44-69.
38. Gottfried J.A., O'Doherty J., Dolan R.J. Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging. J. Neurosci. 2002, 22:10829-10837.
39. Grefkes C., Geyer S., Schormann T., Roland P., Zilles K. Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. NeuroImage 2001, 14:617-631.
40. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:253-258.
41. Habas C., Kamdar N., Nguyen D., Prater K., Beckmann C.F., Menon V., Greicius M.D. Distinct cerebellar contributions to intrinsic connectivity networks. J. Neurosci. 2009, 29:8586-8594.
42. Hautzinger M., Keller F., Kühner C. Beck Depressions-Inventar (BDI-II) 2006, Harcourt Test Services, Frankfurt/Main, (Revision).
43. Heinz A., Schlagenhauf F. Dopaminergic dysfunction in schizophrenia: salience attribution revisited. Schizophr. Bull. 2010, 36:472-485.
44. Hermann C., Ziegler S., Birbaumer N., Flor H. Pavlovian aversive and appetitive odor conditioning in humans: subjective, peripheral, and electrocortical changes. Exp. Brain Res. 2000, 132:203-215.
45. Hilgard E.R., Campbell R.K., Sears W.N. Conditioned discrimination: the effect of knowledge of stimulus relationships. Am. J. Psychol. 1937, 51:498-506.
46. Hsu M., Bhatt M., Adolphs R., Tranel D., Camerer C.F. Neural systems responding to degrees of uncertainty in human decision-making. Science 2005, 310:1680-1683.
47. Hummel T., Konnerth C.G., Rosenheim K., Kobal G. Screening of olfactory function with a four-minute odor identification test: reliability, normative data, and investigations in patients with olfactory loss. Ann. Otol. Rhinol. Laryngol. 2001, 110:976-981.
48. Iannetti G.D., Mouraux A. From the neuromatrix to the pain matrix (and back). Exp. Brain Res. 2010, 205:1-12.
49. Jensen J., Willeit M., Zipursky R.B., Savina I., Smith A.J., Menon M., Crawley A.P., Kapur S. The formation of abnormal associations in schizophrenia: neural and behavioral evidence. Neuropsychopharmacology 2008, 33:473-479.
50. Kelly R.M., Strick P.L. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J. Neurosci. 2003, 23:8432-8444.
51. Klucken T., Kagerer S., Schweckendiek J., Tabbert K., Vaitl D., Stark R. Neural, electrodermal and behavioral response patterns in contingency aware and unaware subjects during a picture-picture conditioning paradigm. Neuroscience 2009, 158:721-731.
52. Kober H., Barrett L.F., Joseph J., Bliss-Moreau E., Lindquist K., Wager T.D. Functional grouping and cortical-subcortical interactions in emotion: a meta-analysis of neuroimaging studies. NeuroImage 2008, 42:998-1031.
53. Koster E.P., Degel J., Piper D. Proactive and retroactive interference in implicit odor memory. Chem. Senses 2002, 27:191-206.
54. Leonard D.W. Partial reinforcement effects in classical aversive conditioning in rabbits and human beings. J. Comp. Physiol. Psychol. 1975, 88:596-608.
55. Livermore A., Hummel T., Kobal G. Chemosensory event-related potentials in the investigation of interactions between the olfactory and the somatosensory (trigeminal) systems. Electroencephalogr. Clin. Neurophysiol. 1992, 83:201-210.
56. Lovibond P.F., Shanks D.R. The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implications. J. Exp. Psychol. Anim. Behav. Process. 2002, 28:3-26.
57. Ludvig E.A., Sutton R.S., Kehoe E.J. Evaluating the TD model of classical conditioning. Learn. Behav. 2012, 40:305-319.
58. Lundstrom J.N., Boesveldt S., Albrecht J. Central processing of the chemical senses: an overview. ACS Chem. Neurosci. 2011, 2:5-16.
59. Malikovic A., Amunts K., Schleicher A., Mohlberg H., Eickhoff S.B., Wilms M., Palomero-Gallagher N., Armstrong E., Zilles K. Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/MT+: a probabilistic, stereotaxic map of area hOc5. Cereb. Cortex 2007, 17:562-574.
60. Marinkovic K., Schell A.M., Dawson M.E. Awareness of the CS-UCS contingency and classical conditioning of skin conductance responses with olfactory CSs. Biol. Psychol. 1989, 29:39-60.
61. Mechias M.L., Etkin A., Kalisch R. A meta-analysis of instructed fear studies: implications for conscious appraisal of threat. NeuroImage 2010, 49:1760-1768.
62. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 2010, 214:655-667.
63. Moessnang C., Habel U., Schneider F., Siegel S.J. The electrophysiological signature of motivational salience in mice and implications for schizophrenia. Neuropsychopharmacology 2012, 37:2846-2854.
64. Morris J.S., Büchel C., Dolan R.J. Parallel neural responses in amygdala subregions and sensory cortex during implicit fear conditioning. NeuroImage 2001, 13:1044-1052.
65. Mouraux A., Diukova A., Lee M.C., Wise R.G., Iannetti G.D. A multisensory investigation of the functional significance of the "pain matrix". NeuroImage 2011, 54:2237-2249.
66. Nasser H.M., McNally G.P. Appetitive-aversive interactions in Pavlovian fear conditioning. Behav. Neurosci. 2012, 126:404-422.
67. Oertel B.G., Preibisch C., Martin T., Walter C., Gamer M., Deichmann R., Lotsch J. Separating brain processing of pain from that of stimulus intensity. Hum. Brain Mapp. 2012, 33:883-894.
68. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 1971, 9:97-113.
69. O'Reilly J.X., Woolrich M.W., Behrens T.E., Smith S.M., Johansen-Berg H. Tools of the trade: psychophysiological interactions and functional connectivity. Soc. Cogn. Affect. Neurosci. 2012, 7:604-609.
70. Peyron R., Laurent B., Garcia-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol. Clin. 2000, 30:263-288.
71. Picard N., Strick P.L. Imaging the premotor areas. Curr. Opin. Neurobiol. 2001, 11:663-672.
72. Rescorla R.A. Behavioral studies of Pavlovian conditioning. Annu. Rev. Neurosci. 1988, 11:329-352.
73. Roiser J.P., Stephan K.E., den Ouden H.E., Barnes T.R., Friston K.J., Joyce E.M. Do patients with schizophrenia exhibit aberrant salience?. Psychol. Med. 2009, 39:199-209.
74. Rottschy C., Eickhoff S.B., Schleicher A., Mohlberg H., Kujovic M., Zilles K., Amunts K. Ventral visual cortex in humans: cytoarchitectonic mapping of two extrastriate areas. Hum. Brain Mapp. 2007, 28:1045-1059.
75. Ruan Y., Zheng X.Y., Zhang H.L., Zhu W., Zhu J. Olfactory dysfunctions in neurodegenerative disorders. J. Neurosci. Res. 2012, 90:1693-1700.
76. Scheperjans F., Hermann K., Eickhoff S.B., Amunts K., Schleicher A., Zilles K. Observer-independent cytoarchitectonic mapping of the human superior parietal cortex. Cereb. Cortex 2008, 18:846-867.
77. Schmahmann J.D., Sherman J.C. The cerebellar cognitive affective syndrome. Brain 1998, 121(Pt 4):561-579.
78. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
79. Sehlmeyer C., Schoning S., Zwitserlood P., Pfleiderer B., Kircher T., Arolt V., Konrad C. Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One 2009, 4:e5865.
80. Seymour B., O'Doherty J.P., Dayan P., Koltzenburg M., Jones A.K., Dolan R.J., Friston K.J., Frackowiak R.S. Temporal difference models describe higher-order learning in humans. Nature 2004, 429:664-667.
81. Shackman A.J., Salomons T.V., Slagter H.A., Fox A.S., Winter J.J., Davidson R.J. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 2011, 12:154-167.
82. Shepherd G.M. The human sense of smell: are we better than we think?. PLoS Biol. 2004, 2:e146.
83. Singer T., Critchley H.D., Preuschoff K. A common role of insula in feelings, empathy and uncertainty. Trends Cogn. Sci. 2009, 13:334-340.
84. Spoormaker V.I., Andrade K.C., Schroter M.S., Sturm A., Goya-Maldonado R., Samann P.G., Czisch M. The neural correlates of negative prediction error signaling in human fear conditioning. NeuroImage 2011, 54:2250-2256.
85. Sridharan D., Levitin D.J., Menon V. A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:12569-12574.
86. Sterzer P., Kleinschmidt A. Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct. Funct. 2010, 214:611-622.
87. Stoodley C.J. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum 2012, 11:352-365.
88. Stoodley C.J., Schmahmann J.D. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 2010, 46:831-844.
89. Tabbert K., Stark R., Kirsch P., Vaitl D. Hemodynamic responses of the amygdala, the orbitofrontal cortex and the visual cortex during a fear conditioning paradigm. Int. J. Psychophysiol. 2005, 57:15-23.
90. Tabbert K., Stark R., Kirsch P., Vaitl D. Dissociation of neural responses and skin conductance reactions during fear conditioning with and without awareness of stimulus contingencies. NeuroImage 2006, 32:761-770.
91. Tabbert K., Merz C.J., Klucken T., Schweckendiek J., Vaitl D., Wolf O.T., Stark R. Influence of contingency awareness on neural, electrodermal and evaluative responses during fear conditioning. Soc. Cogn. Affect. Neurosci. 2011, 6:495-506.
92. Taylor K.S., Seminowicz D.A., Davis K.D. Two systems of resting state connectivity between the insula and cingulate cortex. Hum. Brain Mapp. 2009, 30:2731-2745.
93. Todrank J., Byrnes D., Wrzniewski A., Rozin P. Odors can change preferences for people in photographs: a cross-modal evaluative conditioning study with olfactory USs and visual CSs. Learn. Motiv. 1995, 26:116-140.
94. Torta D.M., Cauda F. Different functions in the cingulate cortex, a meta-analytic connectivity modeling study. NeuroImage 2011, 56:2157-2172.
95. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using macroscopic anatomical parcellation of the MNI MRI single subject brain. NeuroImage 2002, 15:273-289.
96. Vogt B.A. Pain and emotion interactions in subregions of the cingulate gyrus. Nat. Rev. Neurosci. 2005, 6:533-544.
97. Wager T.D., Phan K.L., Liberzon I., Taylor S.F. Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. NeuroImage 2003, 19:513-531.
98. Weinberger N.M. Specific long-term memory traces in primary auditory cortex. Nat. Rev. Neurosci. 2004, 5:279-290.
99. Wiech K., Lin C.S., Brodersen K.H., Bingel U., Ploner M., Tracey I. Anterior insula integrates information about salience into perceptual decisions about pain. J. Neurosci. 2010, 30:16324-16331.
100. Wittchen H.U., Zaudig M., Fydrich T. SKID-I/II: Strukturiertes klinisches Interview für DSM-IV 1997, Hogrefe, Göttingen.