1 Frontiers in Human Neuroscience 2013 Vol: 7():. DOI: 10.3389/fnhum.2013.00278

Just watching the game ain't enough: striatal fMRI reward responses to successes and failures in a video game during active and vicarious playing

Although the multimodal stimulation provided by modern audiovisual video games is pleasing by itself, the rewarding nature of video game playing depends critically also on the players' active engagement in the gameplay. The extent to which active engagement influences dopaminergic brain reward circuit responses remains unsettled. Here we show that striatal reward circuit responses elicited by successes (wins) and failures (losses) in a video game are stronger during active than vicarious gameplay. Eleven healthy males both played a competitive first-person tank shooter game (active playing) and watched a pre-recorded gameplay video (vicarious playing) while their hemodynamic brain activation was measured with 3-tesla functional magnetic resonance imaging (fMRI). Wins and losses were paired with symmetrical monetary rewards and punishments during active and vicarious playing so that the external reward context remained identical during both conditions. Brain activation was stronger in the orbitomedial prefrontal cortex (omPFC) during winning than losing, both during active and vicarious playing. In contrast, both wins and losses suppressed activations in the midbrain and striatum during active playing; however, the striatal suppression, particularly in the anterior putamen, was more pronounced during loss than win events. Sensorimotor confounds related to joystick movements did not account for the results. Self-ratings indicated losing to be more unpleasant during active than vicarious playing. Our findings demonstrate striatum to be selectively sensitive to self-acquired rewards, in contrast to frontal components of the reward circuit that process both self-acquired and passively received rewards. We propose that the striatal responses to repeated acquisition of rewards that are contingent on game related successes contribute to the motivational pull of video-game playing.

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Figures
Figure 1: A sample sequence of gameplay events: player spawns in a random location on the battlefield and starts searching for the opponent (A), the player and opponent engage each other (B), until the player either manages to eliminate the opponent (C) or gets eliminated himself (D). Figure 2: Regions of interest (ROIs) in the (A) striatum, and (B) midbrain and frontal cortex. NAcc, nucleus accumbens; vCaud, ventral caudate; dCaud, dorsal caudate; vaPut, ventral anterior putamen; daPut, dorsal anterior putamen; pPut, posterior putamen; VTA/SN, ventral tegmental area/substantia nigra; omPFC, orbitomedial prefrontal cortex; vmPFC, ventromedial prefrontal cortex. Figure 3: Brain regions showing significantly stronger effects during vicarious than active playing (during win or loss gameplay events). The data have been thresholded at P < 0.05 (FWE-corrected; min. cluster size 50 voxels). Black horizontal line on the colorbar (on the right) illustrates the lowest significant T-value. Mid, midbrain; ITG, inferior temporal gyrus; Put, putamen; PoG, post-central gyrus. Figure 4: Region of interest analyses in the striatal (upper row), and mesial and frontal nodes (lower row) of the reward circuit. Error bars denote 95% confidence intervals. Asterisks denote significant simple effects (significant differences between wins vs. losses during either playing or watching) or significant interactions between game events and activities. *P < 0.05. **P < 0.001. ***P < 0.001. NAcc, nucleus accumbens; vCaud, ventral caudate; dCaud, dorsal caudate; vaPut, anterior ventral putamen; daPut, anterior dorsal putamen; pPut, posterior putamen; VTA/SN, ventral tegmental area and substantia nigra; vmPFC, ventromedial prefrontal cortex; omPFC, orbitomedial prefrontal cortex. Figure 5: Bivariate scatter plots for Positive Affect evaluations versus mean beta responses in regions of interest, for active and vicarious playing conditions. The solid and dashed lines depict best linear fits to the data. VTA/SN, ventral tegmental area and substantia nigra; NAcc, nucleus accumbens; vCaud, ventral caudate; dCaud, dorsal caudate; vaPut, anterior ventral putamen; daPut, anterior dorsal putamen; pPut, posterior putamen.
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References
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    • . . . Unlike in our previous analysis of active gameplay data, we now contrasted win and loss events separately, given that recent evidence suggests that striatal activations decrease both during wins and losses during active gameplay (Mathiak et al., 2011) . . .
    • . . . First, replicating similar previous findings (Mathiak et al., 2011), both win and loss events evoked deactivations with respect to generic gameplay levels during active but not during vicarious playing . . .
    • . . . Although similar striatal deactivations have been observed previously (Mathiak et al., 2011), reward circuit deactivations associated with rewarding gameplay events nevertheless warrant consideration . . .
    • . . . Although the present sample size was comparable to those of several recent fMRI studies utilizing video game stimuli (Mathiak and Weber, 2006; Weber et al., 2006; Mobbs et al., 2007; Ko et al., 2009; Mathiak et al., 2011; Klasen et al., 2012), future studies should consider using larger sample sizes to detect potentially more fine-grained differences between active and vicarious gameplay . . .
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    • . . . In future, this problem could be solved by showing participants video recording of their gameplay sessions, and asking them to continuously rate their emotional feelings during the gameplay; this technique has been proven successful for example when studying the brain basis of emotions elicited by movies (Nummenmaa et al., 2012) and already utilized in previous fMRI game studies (Klasen et al., 2008). . . .
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    • . . . Dopaminergic pathways extending from the midbrain (ventral tegmental area and substantia nigra, VTA/SN) to the ventral and dorsal striatum (nucleus accumbens, caudate nucleus, and putamen) and frontal cortex (orbitomedial and medial prefrontal cortex; omPFC and vmPFC) are involved in processing rewards and punishments (Kelley, 2004; O'Doherty, 2004; Bressan and Crippa, 2005; Knutson and Cooper, 2005; Schultz, 2006; Berridge and Kringelbach, 2008; Hikosaka et al., 2008; Haber and Knutson, 2010; Koob and Volkow, 2010) . . .
  44. J. P. O'Doherty; P. Dayan; J. Schultz; R. Deichmann; K. Friston; R. J. Dolan Dissociable roles of ventral and dorsal striatum in instrumental conditioning Science 304, 452-454 (2004) .
    • . . . This finding is consistent with both animal electrophysiology (Kawagoe et al., 1998; Schultz et al., 2000) and human neuroimaging (Elliott et al., 2004; O'Doherty et . . .
  45. J. P. O'Doherty; R. Deichmann; H. D. Critchley; R. J. Dolan Neural responses during anticipation of a primary taste reward Neuron 33, 815-826 (2002) .
    • . . . A spherical 10-mm ROI was defined for the VTA/SN (MNI coordinates 0, −22, −18) based on a previous study (O'Doherty et al., 2002) . . .
  46. A. K. Przybylski; C. S. Rigby; R. M. Ryan A motivational model of video game engagement Rev. Gen. Psychol 14, 154-166 (2010) .
    • . . . Ryan and Deci, 2000): most people play video games because they are inherently interesting and enjoyable rather than because they provide financial rewards or other external outcomes (Ryan et al., 2006; Przybylski et al., 2009, 2010) . . .
    • . . . Przybylski et al., 2010; see also Koepp et al., 1998) . . .
  47. A. K. Przybylski; R. M. Ryan; C. S. Rigby The motivating role of violence in video games Pers. Soc. Psychol. Bull 35, 243-259 (2009) .
    • . . . Ryan and Deci, 2000): most people play video games because they are inherently interesting and enjoyable rather than because they provide financial rewards or other external outcomes (Ryan et al., 2006; Przybylski et al., 2009, 2010) . . .
  48. N. Ravaja; T. Saari; M. Salminen; J. Laarni; K. Kallinen Phasic emotional reactions to video game events: a psychophysiological investigation Media Psychol 8, 343-367 (2006) .
    • . . . Third, successes are generally associated with pleasant and failures with unpleasant emotional responses—even though in some games this mapping may be more complex (Ravaja et al., 2006, 2008) . . .
  49. N. Ravaja; M. Turpeinen; T. Saari; S. Puttonen; L. Keltikangas-Järvinen The psychophysiology of James Bond: phasic emotional responses to violent video game events Emotion 8, 114-120 (2008) .
    • . . . Success- and failure-related gameplay events fulfil the three characteristics of rewards and punishments considered in animal learning (Schultz, 2004, 2006; Berridge and Kringelbach, 2008) . . .
  50. R. M. Ryan; E. L. Deci Intrinsic and extrinsic motivations: classic definitions and new directions Contemp. Edu. Psychol 25, 54-67 (2000) .
    • . . . Ryan and Deci, 2000): most people play video games because they are inherently interesting and enjoyable rather than because they provide financial rewards or other external outcomes (Ryan et al., 2006; Przybylski et al., 2009, 2010) . . .
  51. R. M. Ryan; C. S. Rigby; A. Przybylski The motivational pull of video games: a self-determination theory approach Motiv. Emot 30, 344-360 (2006) .
    • . . . Ryan and Deci, 2000): most people play video games because they are inherently interesting and enjoyable rather than because they provide financial rewards or other external outcomes (Ryan et al., 2006; Przybylski et al., 2009, 2010) . . .
  52. A. Savitzky; M. J. E. Golay Smoothing and differentiation of data by simplified least squares procedures Anal. Chem 36, 1627-1639 (1964) .
    • . . . Resulting position and velocity (i.e., the first derivative of position) tracks were low-pass filtered at 5 Hz using a first-order smoothing filter (Savitzky and Golay, 1964) . . .
  53. W. Schultz Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology Curr. Opin. Neurobiol 14, 139-147 (2004) .
    • . . . Success- and failure-related gameplay events fulfil the three characteristics of rewards and punishments considered in animal learning (Schultz, 2004, 2006; Berridge and Kringelbach, 2008) . . .
  54. W. Schultz Behavioral theories and the neurophysiology of reward Annu. Rev. Psychol 57, 87-115 (2006) .
    • . . . Success- and failure-related gameplay events fulfil the three characteristics of rewards and punishments considered in animal learning (Schultz, 2004, 2006; Berridge and Kringelbach, 2008) . . .
    • . . . Dopaminergic pathways extending from the midbrain (ventral tegmental area and substantia nigra, VTA/SN) to the ventral and dorsal striatum (nucleus accumbens, caudate nucleus, and putamen) and frontal cortex (orbitomedial and medial prefrontal cortex; omPFC and vmPFC) are involved in processing rewards and punishments (Kelley, 2004; O'Doherty, 2004; Bressan and Crippa, 2005; Knutson and Cooper, 2005; Schultz, 2006; Berridge and Kringelbach, 2008; Hikosaka et al., 2008; Haber and Knutson, 2010; Koob and Volkow, 2010) . . .
  55. W. Schultz; L. Tremblay; J. R. Hollerman Reward processing in primate orbitofrontal cortex and basal ganglia Cereb. Cortex 10, 272-284 (2000) .
    • . . . Monkey caudate neurons fire more frequently during motor actions leading to expected rewards than during non-rewarded actions (Kawagoe et al., 1998; Schultz et al., 2000) . . .
    • . . . This finding is consistent with both animal electrophysiology (Kawagoe et al., 1998; Schultz et al., 2000) and human neuroimaging (Elliott et al., 2004; O'Doherty et al., 2004; Tricomi et al., 2004; Zink et al., 2004; Guitart-Masip et al., 2011), showing that striatal reward responses depend critically on the recipients' own actions . . .
    • . . . Action-independent reward activations in the omPFC have been observed previously in both animal (Schultz et al., 2000) and human neuroimaging studies (Elliott et al., 2004) . . .
  56. H. R. Siebner; C. Limmer; A. Peinemann; P. Bartenstein; A. Drzezga; B. Conrad Brain correlates of fast and slow handwriting in humans: a PET-performance correlation analysis Eur. J. Neurosci 14, 726-736 (2001) .
    • . . . Our subjects used precision hand actions to manipulate the joystick, and thus it is critical to control for sensorimotor processes related to the acquisition of rewards, especially because the striatum is also involved in sensorimotor control over corrective hand movements (Siebner et al., 2001; Turner et al., 2003) . . .
  57. J. D. Steele; S. M. Lawrie Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis Neuroimage 21, 868-875 (2004) .
    • . . . A spherical 10-mm ROI was derived for the vmPFC (MNI 0, 46, 18) based on a previous meta-analysis (Steele and Lawrie, 2004) . . .
  58. E. M. Tricomi; M. R. Delgado; J. A. Fiez Modulation of caudate activity by action contingency Neuron 41, 281-92 (2004) .
    • . . . For example, dorsal caudate responds differentially to rewards and punishments only when they are perceived to be contingent on the participants' button presses (Tricomi et al., 2004) . . .
    • . . . This finding is consistent with both animal electrophysiology (Kawagoe et al., 1998; Schultz et al., 2000) and human neuroimaging (Elliott et al., 2004; O'Doherty et . . .
  59. R. S. Turner; M. Desmurget; J. Grethe; M. D. Crutcher; S. T. Grafton Motor subcircuits mediating the control of movement extent and speed J. Neurophysiol 90, 3958-3966 (2003) .
    • . . . Our subjects used precision hand actions to manipulate the joystick, and thus it is critical to control for sensorimotor processes related to the acquisition of rewards, especially because the striatum is also involved in sensorimotor control over corrective hand movements (Siebner et al., 2001; Turner et al., 2003) . . .
  60. P. Voorn; L. J. Vanderschuren; H. J. Groenewegen; T. W. Robbins; C. M. Pennartz Putting a spin on the dorsal-ventral divide of the striatum Trends Neurosci 27, 468-474 (2004) .
    • . . . Action-independent reward activations in the omPFC have been observed previously in both animal (Schultz et al., 2000) and human neuroimaging studies (Elliott et al., 2004) . . .
  61. R. Weber; U. Ritterfeld; K. Mathiak Does playing violent video games induce aggression? Empirical evidence of a functional magnetic resonance imaging study Media Psychol 8, 39-60 (2006) .
    • . . . Although the present sample size was comparable to those of several recent fMRI studies utilizing video game stimuli (Mathiak and Weber, 2006; Weber et al., 2006; Mobbs et al., 2007; Ko et al., 2009; Mathiak et al., 2011; Klasen et al., 2012), future studies should consider using larger sample sizes to detect potentially more fine-grained differences between active and vicarious gameplay . . .
  62. B. Weiner An attributional theory of achievement motivation and emotion Psychol. Rev 92, 548-573 (1985) .
    • . . . Successes and failures are among the most potent triggers for pleasant and unpleasant emotions (Nummenmaa and Niemi, 2004), and their affective salience is amplified when they can be attributed to internal (as during active gameplay) rather than external causes (Weiner, 1985) . . .
    • . . . In line with the attribution theory (Weiner, 1985), players' self-ratings confirmed that losses were experienced as more unpleasant during active than vicarious playing, even though the external monetary rewards and punishments for wins and losses were identical during active and vicarious playing conditions . . .
  63. G. Xue; Z. Lu; I. P. Levin; J. A. Weller; X. Li; A. Bechara Functional dissociations of risk and reward processing in the medial prefrontal cortex Cereb. Cortex 19, 1019-1027 (2009) .
    • . . . Given that some fMRI studies on reward processing have reported more inferior reward-sensitive activation clusters, an additional 10-mm spherical ROI was extracted for the omPFC (MNI 0, 58, −6) from a previous study (Xue et al., 2009). . . .
    • . . . Given that the win and loss events were associated with external monetary rewards and punishments, the omPFC activations are also consistent with the known role of omPFC in processing monetary gains and other secondary rewards (Xue et al., 2009) . . .
  64. C. F. Zink; G. Pagnoni; M. E. Martin-Skurski; J. C. Chappelow; G. S. Berns Human striatal responses to monetary reward depend on saliency Neuron 42, 509-517 (2004) .
    • . . . In line with this, brain imaging studies have shown that self-acquired rewards—such as those contingent on correct motor responses—rather than those delivered at random evoke stronger neural responses in the striatum (e.g., Zink et al., 2004) . . .
    • . . . This finding is consistent with both animal electrophysiology (Kawagoe et al., 1998; Schultz et al., 2000) and human neuroimaging (Elliott et al., 2004; O'Doherty et . . .
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