Literature DB >> 27683900

Shared Neural Mechanisms for the Evaluation of Intense Sensory Stimulation and Economic Reward, Dependent on Stimulation-Seeking Behavior.

Agnes Norbury1, Vincent Valton2, Geraint Rees2, Jonathan P Roiser2, Masud Husain3.   

Abstract

UNLABELLED: Why are some people strongly motivated by intense sensory experiences? Here we investigated how people encode the value of an intense sensory experience compared with economic reward, and how this varies according to stimulation-seeking preference. Specifically, we used a novel behavioral task in combination with computational modeling to derive the value individuals assigned to the opportunity to experience an intense tactile stimulus (mild electric shock). We then examined functional imaging data recorded during task performance to see how the opportunity to experience the sensory stimulus was encoded in stimulation-seekers versus stimulation-avoiders. We found that for individuals who positively sought out this kind of sensory stimulation, there was common encoding of anticipated economic and sensory rewards in the ventromedial prefrontal cortex. Conversely, there was robust encoding of the modeled probability of receiving such stimulation in the insula only in stimulation-avoidant individuals. Finally, we found preliminary evidence that sensory prediction error signals may be positively signed for stimulation-seekers, but negatively signed for stimulation-avoiders, in the posterior cingulate cortex. These findings may help explain why high intensity sensory experiences are appetitive for some individuals, but not for others, and may have relevance for the increased vulnerability for some psychopathologies, but perhaps increased resilience for others, in high sensation-seeking individuals. SIGNIFICANCE STATEMENT: People vary in their preference for intense sensory experiences. Here, we investigated how different individuals evaluate the prospect of an unusual sensory experience (electric shock), compared with the opportunity to gain a more traditional reward (money). We found that in a subset of individuals who sought out such unusual sensory stimulation, anticipation of the sensory outcome was encoded in the same way as that of monetary gain, in the ventromedial prefrontal cortex. Further understanding of stimulation-seeking behavior may shed light on the etiology of psychopathologies such as addiction, for which high or low sensation-seeking personality has been identified as a risk factor.
Copyright © 2016 Norbury et al.

Entities:  

Keywords:  addiction; decision-making; impulsivity; individual differences; sensation-seeking; value

Mesh:

Year:  2016        PMID: 27683900      PMCID: PMC5039253          DOI: 10.1523/JNEUROSCI.1048-16.2016

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  45 in total

1.  Anticipation of increasing monetary reward selectively recruits nucleus accumbens.

Authors:  B Knutson; C M Adams; G W Fong; D Hommer
Journal:  J Neurosci       Date:  2001-08-15       Impact factor: 6.167

2.  Informatic parcellation of the network involved in the computation of subjective value.

Authors:  John A Clithero; Antonio Rangel
Journal:  Soc Cogn Affect Neurosci       Date:  2013-07-24       Impact factor: 3.436

Review 3.  Sensation-seeking: Dopaminergic modulation and risk for psychopathology.

Authors:  Agnes Norbury; Masud Husain
Journal:  Behav Brain Res       Date:  2015-04-20       Impact factor: 3.332

Review 4.  The reward circuit: linking primate anatomy and human imaging.

Authors:  Suzanne N Haber; Brian Knutson
Journal:  Neuropsychopharmacology       Date:  2010-01       Impact factor: 7.853

5.  The habenula encodes negative motivational value associated with primary punishment in humans.

Authors:  Rebecca P Lawson; Ben Seymour; Eleanor Loh; Antoine Lutti; Raymond J Dolan; Peter Dayan; Nikolaus Weiskopf; Jonathan P Roiser
Journal:  Proc Natl Acad Sci U S A       Date:  2014-07-28       Impact factor: 11.205

Review 6.  The root of all value: a neural common currency for choice.

Authors:  Dino J Levy; Paul W Glimcher
Journal:  Curr Opin Neurobiol       Date:  2012-07-03       Impact factor: 6.627

7.  Brain systems mediating aversive conditioning: an event-related fMRI study.

Authors:  C Büchel; J Morris; R J Dolan; K J Friston
Journal:  Neuron       Date:  1998-05       Impact factor: 17.173

Review 8.  The problem with value.

Authors:  John P O'Doherty
Journal:  Neurosci Biobehav Rev       Date:  2014-04-13       Impact factor: 8.989

9.  When errors are rewarding.

Authors:  Ellen R A de Bruijn; Floris P de Lange; D Yves von Cramon; Markus Ullsperger
Journal:  J Neurosci       Date:  2009-09-30       Impact factor: 6.167

10.  Dopamine Regulates Approach-Avoidance in Human Sensation-Seeking.

Authors:  Agnes Norbury; Zeb Kurth-Nelson; Joel S Winston; Jonathan P Roiser; Masud Husain
Journal:  Int J Neuropsychopharmacol       Date:  2015-04-09       Impact factor: 5.176

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  2 in total

1.  Tracking Deceased-Related Thinking with Neural Pattern Decoding of a Cortical-Basal Ganglia Circuit.

Authors:  Noam Schneck; Stefan Haufe; Tao Tu; George A Bonanno; Kevin Ochsner; Paul Sajda; J John Mann
Journal:  Biol Psychiatry Cogn Neurosci Neuroimaging       Date:  2017-07

2.  Systems genetics of sensation seeking.

Authors:  Price E Dickson; Tyler A Roy; Kathryn A McNaughton; Troy D Wilcox; Padam Kumar; Elissa J Chesler
Journal:  Genes Brain Behav       Date:  2018-10-08       Impact factor: 3.449

  2 in total

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