Cited by 22Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

Aversive Event Anticipation Affects Connectivity between the Ventral Striatum and the Orbitofrontal Cortex in an fMRI Avoidance Task

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Bolstad, Ingeborg, Andreassen, Ole A., Reckless, Greg E., Sigvartsen, Niels P., Server, Andres, Jensen, Jimmy·2013·PLoS ONE

Abstract

Ability to anticipate aversive events is important for avoiding dangerous or unpleasant situations. The motivation to avoid an event is influenced by the incentive salience of an event-predicting cue. In an avoidance fMRI task we used tone intensities to manipulate salience in order to study the involvement of the orbitofrontal cortex in processing of incentive salience. In the task, cues predicting either aversive or neutral avoidable tones were presented. Ventral striatum, amygdala and anterior insula activations were significantly stronger during presentation of cues for aversive than neutral tones. A psychophysiological interaction analysis showed stronger connectivity between the ventral striatum and the orbitofrontal cortex during aversive than neutral conditions. The present study shows an interaction between the ventral striatum, a structure previously linked to negative incentive salience, and the orbitofrontal cortex supporting a role for this region in processing salience. In addition, this study replicates previous findings suggesting that the task is robust.

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  • Several studies observed striatal activation during cue presentation, but they compared the BOLD responses within subjects during a threatening cue associated with an avoidance response and a nonthreatening cue in a single cohort of subjects.

    “Several studies observed striatal activation during cue presentation, but they compared the BOLD responses withinsubjects during a threatening cue associated with an avoidance response and a nonthreatening cue in a single cohort of subjects (Jensen et al., 2003; Levita et al., 2012; Bolstad et al., 2013; Collins et al., 2014).”

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References 47 · Cited by 22

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  1. [1]Horvitz JC (2002) Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum. Behav Brain Res 137: 65- 74. doi: 10.1016/S0166-4328(02)00285-1. PubMed: 12445716. 12445716 · DOI
  2. [2]Kapur S (2003) Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiatry 160: 13- 23. doi: 10.1176/appi.ajp.160.1.13. PubMed: 12505794. 12505794 · DOI · Paper page
  3. [6]Pohlack ST, Nees F, Ruttorf M, Schad LR, Flor H (2012) Activation of the ventral striatum during aversive contextual conditioning in humans. Biol Psychol 91: 74- 80. doi: 10.1016/j.biopsycho.2012.04.004. PubMed: 22560888. 22560888 · DOI
  4. [7]Delgado MR, Jou RL, Ledoux JE, Phelps EA (2009) Avoiding negative outcomes: tracking the mechanisms of avoidance learning in humans during fear conditioning. Front Behav Neurosci 3: 33-, Art. no. 33.. PubMed: 19847311 19847311 PMC2762377
  5. [8]Schultz W (2002) Getting formal with dopamine and reward. Neuron 36: 241- 263. doi: 10.1016/S0896-6273(02)00967-4. PubMed: 12383780. 12383780 · DOI · Paper page
  6. [9]Jensen J, Smith AJ, Willeit M, Crawley AP, Mikulis DJ et al. (2007) Separate brain regions code for salience vs. valence during reward prediction in humans. Hum Brain Mapp 28: 294- 302. doi: 10.1002/hbm.20274. PubMed: 16779798. 16779798 PMC6871333 · DOI
  7. [10]Esslinger C, Englisch S, Inta D, Rausch F, Schirmbeck F et al. (2012) Ventral striatal activation during attribution of stimulus saliency and reward anticipation is correlated in unmedicated first episode schizophrenia patients. Schizophr Res 140: 114- 121. doi: 10.1016/j.schres.2012.06.025. PubMed: 22784688. 22784688 · DOI
  8. [11]Kirsch P, Schienle A, Stark R, Sammer G, Blecker C et al. (2003) Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. Neuroimage 20: 1086- 1095. doi: 10.1016/S1053-8119(03)00381-1. PubMed: 14568478. 14568478 · DOI
  9. [12]Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH et al. (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27: 2349- 2356. doi: 10.1523/JNEUROSCI.5587-06.2007. PubMed: 17329432. 17329432 PMC2680293 · DOI · Paper page
  10. [13]Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214: 655- 667. doi: 10.1007/s00429-010-0262-0. PubMed: 20512370. 20512370 PMC2899886 · DOI · Paper page
  11. [15]Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306: 443- 447. doi: 10.1126/science.1100301. PubMed: 15486290. 15486290 · DOI · Paper page
  12. [16]Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ et al. (2011) The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 12: 154- 167. doi: 10.1038/nrg2963. PubMed: 21331082. 21331082 PMC3044650 · DOI
  13. [19]Ousdal OT, Reckless GE, Server A, Andreassen OA, Jensen J (2012) Effect of relevance on amygdala activation and association with the ventral striatum. NeuroImage 62: 95- 101. doi: 10.1016/j.neuroimage.2012.04.035. PubMed: 22546319. 22546319 · DOI
  14. [20]Cunningham WA, Raye CL, Johnson MK (2004) Implicit and explicit evaluation: fMRI correlates of valence, emotional intensity, and control in the processing of attitudes. J Cogn Neurosci 16: 1717- 1729. doi: 10.1162/0898929042947919. PubMed: 15701224. 15701224 · DOI · Paper page
  15. [22]Kringelbach ML, Rolls ET (2004) The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 72: 341- 372. doi: 10.1016/j.pneurobio.2004.03.006. PubMed: 15157726. 15157726 · DOI · Paper page
  16. [23]Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19: 1233- 1239. doi: 10.1016/S1053-8119(03)00169-1. PubMed: 12880848. 12880848 · DOI
  17. [24]Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O 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. doi: 10.1006/nimg.2001.0978. PubMed: 11771995. 11771995 · DOI · Paper page
  18. [25]Fox PT, Lancaster JL (1994) Neuroscience on the net. Science 266: 994- 996. doi: 10.1126/science.7973682. PubMed: 7973682. 7973682 · DOI
  19. [26]Nielsen FA, Hansen LK (2004) Finding related functional neuroimaging volumes. Artif Intell Med 30: 141- 151. doi: 10.1016/S0933-3657(03)00041-1. PubMed: 14992762. 14992762 · DOI
  20. [27]Haber SN, Knutson B (2010) The Reward Circuit: Linking Primate Anatomy and Human Imaging. Neuropsychopharmacology 35: 4- 26. doi: 10.1038/npp.2009.129. PubMed: 19812543. 19812543 PMC3055449 · DOI · Paper page
  21. [28]FitzGerald THB, Seymour B, Dolan RJ (2009) The Role of Human Orbitofrontal Cortex in Value Comparison for Incommensurable Objects. J Neurosci 29: 8388- 8395. doi: 10.1523/JNEUROSCI.0717-09.2009. PubMed: 19571129. 19571129 PMC2712081 · DOI · Paper page
  22. [29]Rolls ET (2004) The functions of the orbitofrontal cortex. Brain Cogn 55: 11- 29. doi: 10.1016/S0278-2626(03)00277-X. PubMed: 15134840. 15134840 · DOI · Paper page
  23. [30]Morrison SE, Salzman CD (2011) Representations of appetitive and aversive information in the primate orbitofrontal cortex. In: Schoenbaum G Gottfried JA Murray EA Ramus SJ Critical Contributions of the Orbitofrontal Cortex to Behavior. Oxford: Blackwell Publishing House Science Publishing pp. 59- 70. PMC3683838 22145876
  24. [31]Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21: RC159: Art. no.-RC159.. PubMed: 11459880. PMC6763187 11459880
  25. [32]Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action - functional interface between the limbic system and the motor system. Prog Neurobiol 14: 69- 97. doi: 10.1016/0301-0082(80)90018-0. PubMed: 6999537. 6999537 · DOI · Paper page
  26. [33]Schultz W, Apicella P, Scarnati E, Ljungberg T (1992) Neuronal activity in monkey ventral striatum related to the expectation of reward. J Neurosci 12: 4595- 4610. PubMed: 1464759. 1464759 PMC6575755
  27. [35]Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG et al. (2003) Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 6: 196- 202. doi: 10.1038/nn1001. PubMed: 12536208. 12536208 · DOI · Paper page
  28. [36]Hamann SB, Ely TD, Hoffman JM, Kilts CD (2002) Ecstasy and agony: Activation of the human amygdala in positive and negative emotion. Psychol Sci 13: 135- 141. doi: 10.1111/1467-9280.00425. PubMed: 11933997. 11933997 · DOI
  29. [38]Wager TD, Rilling JK, Smith EE, Sokolik A, Casey KL et al. (2004) Placebo-induced changes in fMRI in the anticipation and experience of pain. Science 303: 1162- 1167. doi: 10.1126/science.1093065. PubMed: 14976306. 14976306 · DOI · Paper page
  30. [39]Büchel C, Dolan RJ (2000) Classical fear conditioning in functional neuroimaging. Curr Opin Neurobiol 10: 219- 223. doi: 10.1016/S0959-4388(00)00078-7. PubMed: 10753800. 10753800 · DOI
  31. [40]Phelps EA, O’Connor KJ, Gatenby JC, Gore JC, Grillon C et al. (2001) Activation of the left amygdala to a cognitive representation of fear. Nat Neurosci 4: 437- 441. doi: 10.1038/86110. PubMed: 11276236. 11276236 · DOI · Paper page
  32. [41]Kim H, Shimojo S, O’Doherty JP (2006) Is avoiding an aversive outcome rewarding? Neural substrates of avoidance learning in the human brain. PLOS Biol 4: 1453- 1461. PMC1484497 16802856
  33. [42]Nitschke JB, Sarinopoulos I, Mackiewicz KL, Schaefer HS, Davidson RJ (2006) Functional neuroanatomy of aversion and its anticipation. NeuroImage 29: 106- 116. doi: 10.1016/j.neuroimage.2005.06.068. PubMed: 16181793. 16181793 · DOI · Paper page
  34. [44]Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 16: 331- 348. doi: 10.1006/nimg.2002.1087. PubMed: 12030820. 12030820 · DOI · Paper page
  35. [45]Mohr PNC, Biele G, Heekeren HR (2010) Neural Processing of Risk. J Neurosci 30: 6613- 6619. doi: 10.1523/JNEUROSCI.0003-10.2010. PubMed: 20463224. 20463224 PMC6632558 · DOI · Paper page
  36. [46]Shi CJ, Cassell MD (1998) Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex. J Comp Neurol 399: 469- 491. doi: 10.1002/(SICI)1096-9861(19981005)399:4. PubMed: 9741478. 9741478 · DOI
  37. [47]Ikemoto S (2007) Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56: 27- 78. doi: 10.1016/j.brainresrev.2007.05.004. PubMed: 17574681. 17574681 PMC2134972 · DOI · Paper page

Authors
Bolstad, I., Andreassen, O. A., Reckless, G. E., Sigvartsen, N. P., Server, A., & Jensen, J.
Affiliations
Oslo University Hospital (NO)
Corresponding author
Bolstad, Ingeborg
Venue
PLoS ONE
Published
2013-06-24
Volume
8
Issue
6
Pages
e68494
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2023773047
Cited by
22
References
47
Citations by year
2025: 1 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 2 · 2019: 2 · 2018: 1 · 2017: 2 · 2016: 6 · 2015: 1 · 2014: 2
FWCI
1.65
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Högskolan Kristianstad Publikationer (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • NORA - Norwegian Open Research Archives (submittedVersion, cc-by)
Funders
Norges Forskningsråd (199472)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
incentive salience, ventral striatum, orbitofrontal cortex, avoidance learning, amygdala, anterior insula, tone intensity, psychophysiological interaction
MeSH terms
Adult, Avoidance Learning, Basal Ganglia, Behavior, Cerebral Cortex, Cues, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neural Pathways, Oxygen, Task Performance and Analysis, Cluster Analysis, Anticipation, Psychological

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