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A cognitive neuroscience approach to individual differences in sensitivity to reward

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Abstract

The Reinforcement Sensitivity Theory proposes that a neurobiological system, the Behavioral Activation System, defines individual differences on the subject’s sensitivity and reactivity to appetitive stimuli associated with mesocorticolimbic structures, while this system does not mediate aversive stimulus processing. However, Jeffrey A. Gray’s model also predicts the system’s antagonism between this appetitive system and another aversive stimulus sensitive system, the Behavioral Inhibitory System/Fight-Flight-Freeze System, mostly associated with limbic structures. Therefore, direct modulation of brain activation during appetitive stimulus processing should be expected from the Behavioral Activation System, while inverse modulation during aversive stimulus processing may be expected to reflect the system’s antagonism. Using the Sensitivity to Reward scale of the SPSR questionnaire to assess individual differences in the activity of the reward system, we present different behavioral and neuroimaging data to illustrate our view. The first experiment was based on a simple letter-judgment task while viewing erotic and aversive pictures selected from the International Affective Picture System. A second experiment employed a task performed by participants to detect infrequent aversive (i.e., stop) signals when responding to reward. The results from these studies were consistent with the idea that Behavioral Activation System-related personality traits mediate the brain activation associated with appetitive stimulus processing in reward-related areas, while it also showed its antagonism to aversive systems through a negative mediation on the limbic cortex activation. To conclude, sensitivity to reward may be understood as a form of impulsivity related to both better appetitive learning and poorer aversive learning.

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References

  • Aharon I, N Etcoff, D Ariely, CF Chabris, E O’Connor and HC Breiter (2001) Beautiful faces have variable reward value: fMRI and behavioral evidence.Neuron 32, 537–551.

    Article  PubMed  CAS  Google Scholar 

  • Ávila C (1994) Sensitivity to punishment and resistance to extinction: a test of Gray’s behavioral inhibition system.Personality Indiv. Diff. 17, 845–847.

    Article  Google Scholar 

  • Ávila C (2001) Distinguishing BIS-mediated and BAS-mediated disinhibition mechanisms: a comparison of disinhibition models of Gray and Patterson and Newman.J. Personality Soc. Psychol. 80, 311–324.

    Article  Google Scholar 

  • Ávila C and MA Parcet (2000) The role of Gray’s impulsivity in anxiety-mediated differences in resistance to extinction.Eur. J. Personality 14, 185–198.

    Article  Google Scholar 

  • Ávila C and MA Parcet (2001) Personality and inhibitory deficits in the stop-signal task: the mediating role of Gray’s anxiety and impulsivity.Personality Indiv. Diff. 29, 975–986.

    Article  Google Scholar 

  • Ávila C and R Torrubia (2004) Personality, expectations and response to multiple choice question examinations in university students: a test of Gray’s hypotheses.Eur. J. Personality 18, 45–59.

    Article  Google Scholar 

  • Ávila C and R Torrubia (2008) Performance and conditioning studies, In:Reinforcement Sensitivity Theory of Personality (Corr P, Ed.) (Cambridge University Press: London).

    Google Scholar 

  • Ávila C, J Moltó, P Segarra and R Torrubia (1995) Sensitivity to primary or secondary reinforcers, what is the mechanism underlying passive avoidance deficits in extraverts?J. Res. Personality 29, 373–394

    Article  Google Scholar 

  • Azim E, D Mobbs, B Jo, V Menon and AL Reiss (2005) Sex differences in brain activation elicited by humor.Proc. Natl. Acad. Sci. USA 102, 16496–16501.

    Article  PubMed  CAS  Google Scholar 

  • Ball SA and M Zuckerman (1992) Sensation seeking, Eysenck’s personality dimensions and reinforcement sensitivity in concept formation.Personality Indiv. Diff. 11, 343–353.

    Article  Google Scholar 

  • Barrós-Loscertales A, V Meseguer, A Sanjuán, V Belloch, MA Parcet, R Torrubia and C Ávila (2006) Striatum gray matter reduction in males with an overactive Behavior Activation System.Eur. J. Neurosci. 24, 2071–2074.

    Article  PubMed  Google Scholar 

  • Beaver JD, AD Lawrence, J 1Van Ditzhuijzen, MH Davis, A Woods and AJ Calder (2006) Individual differences in reward drive predict neural responses to images of food.J. Neurosci. 26, 5160–5166.

    Article  PubMed  CAS  Google Scholar 

  • Caccioppo JT, and GG Bernston (1994) Relationship between attitudes and evaluativo space: a critical review, with emphasis on the separability of positive and negative substrates.Psychol.Bull. 115, 401–423.

    Article  Google Scholar 

  • Canli T, Z Zhao, JE Desmond, E Kang, J Gross and JDE Gabrieli (2001) An fMRI study of personality influences on brain reactivity to emotional stimuli.Behav. Neurosci. 115, 33–42.

    Article  PubMed  CAS  Google Scholar 

  • Carver SC (2004) Negative affects deriving from the Behavioral Approach System.Emotion 4, 3–22.

    Article  PubMed  Google Scholar 

  • Cloninger CR, D Svrakic and T Przybeck (1993) Apsychobiological model of temperament and character.Arch. Gen. Psychiatry 50, 975–990.

    PubMed  CAS  Google Scholar 

  • Cohen MX, J Young, J-M Baek, C Kessler and C Ranganath (2005) Individual differences in extraversion and dopamine genetics predict neural reward responses.Cogn. Brain Res. 25, 851–861.

    Article  CAS  Google Scholar 

  • Corr PJ (2004) Reinforcement sensitivity theory and personality.Neurosci. Biobehav. Rev. 28, 317–332.

    Article  PubMed  Google Scholar 

  • Delgado MR, VA Stenger and JA Fiez (2004) Motivation dependent responses in the human caudate nucleus.Cereb. Cor. 14, 1022–1030.

    Article  CAS  Google Scholar 

  • Delgado MR, MM Miller, S Inati and EA Phelps (2005) An fMRI study of reward-related probability learning.NeuroImage 24, 862–873.

    Article  PubMed  CAS  Google Scholar 

  • Depue RA and PF Collins (1999) Neurobiology of the structure of personality: dopamine, facilitation of incentive motivation, and extraversion.Behav. Brain Sci. 22, 491–569.

    PubMed  CAS  Google Scholar 

  • Fowles DC (1987) Application of a behavioral theory of motivation to the concepts of anxiety and impulsivity.J. Res. Personality 21 417–435.

    Article  Google Scholar 

  • Gorenstein EE and JP Newman (1980) Disinhibitory psychopathology: a new perspective and a model of research.Psychol. Rev. 87, 301–315.

    Article  PubMed  CAS  Google Scholar 

  • Gray JA (1970) The psychophysiological basis of introversionextraversion.Behav. Res. Ther. 8, 249–66.

    Article  PubMed  CAS  Google Scholar 

  • Gray JA (1982)The Neuropsychology of Anxiety: an Enquiry into the Functions of the Septo-Hippocampal System (Oxford University Press: Oxford).

    Google Scholar 

  • Gray JA (1987)The Psychology of Fear and Stress (Cambridge University Press: Cambridge).

    Google Scholar 

  • Gray JA and N McNaughton (2000)The Neuropsychology of Anxiety: an Enquiry in to the Functions of the Septo-Hippocampal System (Oxford University Press: Oxford).

    Google Scholar 

  • Gray JA, S Owen, N Davis, and E Tsaltas (1983) Psychological and physiological relations between anxiety and impulsivity, In:The Biological Bases of Sensation Seeking, Impulsivity and Anxiety (Zuckerman M, Ed.) (Erlbaum: Hillsdale, NJ), pp 189–217.

    Google Scholar 

  • Gupta S (1990) Personality and reinforcement in verbal operant conditioning: a test of Gray’s theory.Psychol. Stud. 35, 157–162.

    Google Scholar 

  • Haruno M, T Kuroda, K Doya, K Toyama, M Kimura, K Samejima, H Imamizu and M Kawato (2004) A neural correlate of reward-based behavioral learning in caudate nucleus: a functional magnetic resonance imaging study of a stochastic decision task.J. Neurosci. 24, 1660–1665.

    Article  PubMed  CAS  Google Scholar 

  • Kambouropoulos N and PK Staiger (2004) Personality and responses to appetitive and aversive stimuli: the joint influence of behavioural approach and inhibition systems.Personal. Ind. Diff. 37, 1153–1165.

    Article  Google Scholar 

  • Knutson B and J Bhanji (2005). Neural substrates for emotional traits: a case for extraversion, In:Biological Basis of Individual Differences (Canli T, Ed.) (Guilford Press: New York).

    Google Scholar 

  • Knutson B and JC Cooper (2005). Functional magnetic resonance imaging of reward prediction.Curr. Opin. Neurol. 18, 411–417.

    Article  PubMed  Google Scholar 

  • Knutson B, A Westdorp, E Kaiser and D Hommer (2000) fMRI visualization of brain activity during a monetary incentive delay task.Neuroimage 12, 20–27.

    Article  PubMed  CAS  Google Scholar 

  • Knutson B, CM Adams, GW Fong and D Hommer (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens.J. Neurosci. 21, 1–5.

    Google Scholar 

  • Knutson B, GW Fong, SM Bennett, CM Adams and D Hommer (2003) A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI.Neuroimage 18, 263–272.

    Article  PubMed  Google Scholar 

  • Lang PJ, MM Bradley and BN Cuthbert (1997)International Affective Picture System (IAPS): Technical Manual and Affective Ratings. Gainesville: The Center for Research in Psychophysiology, University of Florida.

    Google Scholar 

  • Matthews SC, AN Simmons, SD Lane and MP Paulus (2004) Selective activation of the nucleus accumbens during risk-taking decisión-making.Neuro Report 15, 2123–2127.

    Google Scholar 

  • McNaughton N and PJ Corr (2004) A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance.Neurosci. Biobehav. Rev. 28, 285–305.

    Article  PubMed  Google Scholar 

  • Meseguer V, MJ Romero, A Barrós-Loscertales, V Belloch, F Bosh-Morell, J Romero and C Ávila (2007) Mapping the appetitive and aversive systems with emotional pictures using a Block-design fMRI procedure.Psicothema 19, 483–488.

    PubMed  Google Scholar 

  • Mobbs D, CC Hagan, E Azim, V Menon and AL Reiss (2005) Personality predicts activity in reward and emotional regions associated with humor.Proc. Natl. Acad. Sci. 102, 16502–16506.

    Article  PubMed  CAS  Google Scholar 

  • Newman JP and DS Kosson (1986) Passive avoidance learning in psychopathic and nonpsychopathic offenders.J. Abnorm. Psychol. 95, 252–256.

    Article  PubMed  CAS  Google Scholar 

  • Newman JP, CS Widom and S Nathan (1985) Passive avoidance in syndromes of disinhibition: psychopathy and extra-version.J. Personality Soc. Psychol. 48, 1316–1327.

    Article  CAS  Google Scholar 

  • O’Doherty J, P Dayan, J Schultz, R Deichman, K Friston and RJ Dolan (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning.Science 304, 452–454.

    Article  PubMed  CAS  Google Scholar 

  • Patterson CM and JP Newman (1993) Reflectivity and learning from aversive events: toward a psychological mechanism for the syndromes of desinhibition.Psychol. Rev. 100, 716–736.

    Article  PubMed  CAS  Google Scholar 

  • Patterson CM, DS Kosson and JP Newman (1987) Reaction to punishment, reflectivity, and passive avoidance learning in extraverts.J. Personality Soc. Psychol. 52, 565–575.

    Article  CAS  Google Scholar 

  • Perkins AM and PJ Corr (2006) Reactions to threat and personality: psychometric differentiation of intensity and directions of human defensive behavior.Behav. Brain Res. 169, 21–28.

    Article  PubMed  Google Scholar 

  • Pickering AD and JA Gray (2001) Dopamine, appetitive reinforcement, and the neuropsychology of human learning: an individual differences approach, In:Advances in Individual Differences Research (Eliasz A and A Angleitner, Eds.) (PABST Science Publishers: Lengerich, Germany), pp 113–149.

    Google Scholar 

  • Pickering AD, PJ Corr, JH Powell, V Kumari, JC Thornton and JA Gray (1997) Individual differences in reactions to reinforcing stimuli are neither black nor white: to what extent are they gray?, In:The Scientific Study of Personality: Tribute to Hans J. Eysenck at Eighty (Nyborg H, Ed.) (Elsevier Sciences: London).

    Google Scholar 

  • Powell JH, S Al-Adawi, J Morgan and RJ Greenwood (1996) Motivational deficits after brain injury: effects of bromocriptine in 11 patients.J. Neurol. Neurosurg. Psychiatry 60, 416–421.

    Article  PubMed  CAS  Google Scholar 

  • Ramnai N, R Elliott, BS Athwal and RE Passingham (2004) Prediction error for free monetary reward in the human prefrontal cortex.NeuroImage 42, 777–786.

    Article  Google Scholar 

  • Rubia K, S Overmeyer, E Taylor, MJ Brammer, SCR Williams, A Simmons, C Andrew, V Giampietro and E Bullmore (2001) Mapping motor inhibition: conjunctive brain activations across different versions of go/no go and stop tasks.Neuroimage 13, 250–261.

    Article  PubMed  CAS  Google Scholar 

  • Segarra P, J Moltó J and R Torrubia (2000) Passive avoidance learning in extraverted females.Personality Ind. Diff. 29, 239–254.

    Article  Google Scholar 

  • Seidman LJ, EM Valera and N Makris (2005) Structural brain imaging of attention-deficit/hyperactivity disorder.Biol. Psychiatry 57, 1263–1272.

    Article  PubMed  Google Scholar 

  • Smillie LD and CJ Jackson (2005) The appetitive scale and other BAS measures in the prediction of approach and active avoidance.Personality Ind. Diff. 38, 981–994.

    Article  Google Scholar 

  • Smillie LD, AD Pickering and CJ Jackson (2006) The new reinforcement sensitivity theory: implications for personality measurement.Personality Soc. Psychol. Rev. 4, 320–335.

    Article  Google Scholar 

  • Tricomi EM, MR Delgado and JA Fiez (2004) Modulation of caudate activity by action contingency.Neuron 41, 281–292.

    Article  PubMed  CAS  Google Scholar 

  • Zinbarg RE and J Mohlman (1998) Individual differences in the acquisition of affectively valenced associations.J. Personality Soc. Psychol. 74, 1024–1040.

    Article  CAS  Google Scholar 

  • Zink CF, G Pagnoni, ME Martin-Skurski, JC Chappelow and GS Berns (2004) Human striatal responses to monetary reward depend on saliency.Neuron 42(3), 509–517.

    Article  PubMed  CAS  Google Scholar 

  • Zuckerman M (1994)Behavioural Expression and Biosocial Bases of Sensation Seeking (Cambridge University Press: New York).

    Google Scholar 

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Ávila, C., Parcet, M.A. & BarróS-Loscertales, A. A cognitive neuroscience approach to individual differences in sensitivity to reward. neurotox res 14, 191–203 (2008). https://doi.org/10.1007/BF03033810

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  • DOI: https://doi.org/10.1007/BF03033810

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