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Subliminal Instrumental Conditioning Demonstrated in the Human Brain

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Pessiglione, Mathias, Petrovic, Predrag, Daunizeau, Jean, Palminteri, Stefano, Dolan, Raymond J., Frith, Chris D.·2008·Neuron
DOI 10.1016/j.neuron.2008.07.005PMC PMC2572733
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Abstract

How the brain uses success and failure to optimize future decisions is a long-standing question in neuroscience. One computational solution involves updating the values of context-action associations in proportion to a reward prediction error. Previous evidence suggests that such computations are expressed in the striatum and, as they are cognitively impenetrable, represent an unconscious learning mechanism. Here, we formally test this by studying instrumental conditioning in a situation where we masked contextual cues, such that they were not consciously perceived. Behavioral data showed that subjects nonetheless developed a significant propensity to choose cues associated with monetary rewards relative to punishments. Functional neuroimaging revealed that during conditioning cue values and prediction errors, generated from a computational model, both correlated with activity in ventral striatum. We conclude that, even without conscious processing of contextual cues, our brain can learn their reward value and use them to provide a bias on decision making.

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Crossref · 10.1016/j.neuron.2008.07.005

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Figure 1 Subliminal Conditioning Task Successive screenshots displayed during a given trial are shown from left to right, with durations in milliseconds. After seeing a masked contextual cue flashed on a computer screen, subjects choose to press or not press a response button and subsequently observe the outcome. In this example, “Go” appears on the screen because the subject has pressed the button, following the cue associated with a rewarding outcome (winning £1).
Figure 1 Subliminal Conditioning Task Successive screenshots displayed during a given trial are shown from left to right, with durations in milliseconds. After seeing a masked contextual cue flashed on a computer screen, subjects choose to press or not press a response button and subsequently observe the outcome. In this example, “Go” appears on the screen because the subject has pressed the button, following the cue associated with a rewarding outcome (winning £1).CC BY · PubMed Central
Figure 2 Behavioral Data (A) Learning curves. Colors indicate cues for which button presses are rewarded (green), neutral (blue), or punished (red). Diamonds represent, across trials, percentages of subjects that pressed the button. Left: continuous lines join the diamonds to illustrate actual choices made by subjects. Right: continuous lines represent the probabilities of button press estimated by an optimized Q-learning model. (B) Preferences. After the conditioning phase, cues were unmasked and subjects rated them, from the most (3) to the least liked (1). The graph shows the average rating for reward (green), neutral (blue), and punishment (red) cues. Bars are ± intersubjects standard errors of the mean.
Figure 2 Behavioral Data (A) Learning curves. Colors indicate cues for which button presses are rewarded (green), neutral (blue), or punished (red). Diamonds represent, across trials, percentages of subjects that pressed the button. Left: continuous lines join the diamonds to illustrate actual choices made by subjects. Right: continuous lines represent the probabilities of button press estimated by an optimized Q-learning model. (B) Preferences. After the conditioning phase, cues were unmasked and subjects rated them, from the most (3) to the least liked (1). The graph shows the average rating for reward (green), neutral (blue), and punishment (red) cues. Bars are ± intersubjects standard errors of the mean.CC BY · PubMed Central
Figure 3 Neuroimaging Data Left: ventral striatal regions isolated by regression of monetary values against BOLD responses to cue display. Right: visual cortical regions isolated by correlation of cue-value regression coefficients with individual payoffs. Slices were taken at global maxima of interest indicated by red pointers on the above axial glass brains. Areas shown in gray/black on glass brains and in orange/yellow on coronal slices showed significant effect. The [x y z] coordinates of the maxima refer to the Montreal Neurological Institute space. (A) Statistical parametric maps using conservative threshold (p < 0.05 after familywise error correction for multiple comparisons). (B) Statistical parametric maps using liberal threshold (p < 0.001 uncorrected). (C) Regression coefficients of Q values (QV) and prediction errors (PE) against BOLD responses to cue and outcome display, respectively. Bars are ± intersubjects standard errors of the mean.
Figure 3 Neuroimaging Data Left: ventral striatal regions isolated by regression of monetary values against BOLD responses to cue display. Right: visual cortical regions isolated by correlation of cue-value regression coefficients with individual payoffs. Slices were taken at global maxima of interest indicated by red pointers on the above axial glass brains. Areas shown in gray/black on glass brains and in orange/yellow on coronal slices showed significant effect. The [x y z] coordinates of the maxima refer to the Montreal Neurological Institute space. (A) Statistical parametric maps using conservative threshold (p < 0.05 after familywise error correction for multiple comparisons). (B) Statistical parametric maps using liberal threshold (p < 0.001 uncorrected). (C) Regression coefficients of Q values (QV) and prediction errors (PE) against BOLD responses to cue and outcome display, respectively. Bars are ± intersubjects standard errors of the mean.CC BY · PubMed Central
Figure 4 Model-free Analyses of Brain Activations Ventral striatum (left) and visual cortex (right) correspond to voxels surviving familywise error correction on statistical parametric maps. (A) Regression coefficients. Histograms represent contrasts of the reward (green) or the punishment (red) condition with the neutral condition, at the times of cue and outcome display. For every contrast the two joint histograms correspond to the first (empty) and second (filled) halves of the conditioning sessions. (B) Time courses. BOLD responses were averaged across trials over conditioning sessions, for the reward (green) and punishment (red) conditions, relative to the neutral condition. Bars are ± intersubjects standard errors of the mean.
Figure 4 Model-free Analyses of Brain Activations Ventral striatum (left) and visual cortex (right) correspond to voxels surviving familywise error correction on statistical parametric maps. (A) Regression coefficients. Histograms represent contrasts of the reward (green) or the punishment (red) condition with the neutral condition, at the times of cue and outcome display. For every contrast the two joint histograms correspond to the first (empty) and second (filled) halves of the conditioning sessions. (B) Time courses. BOLD responses were averaged across trials over conditioning sessions, for the reward (green) and punishment (red) conditions, relative to the neutral condition. Bars are ± intersubjects standard errors of the mean.CC BY · PubMed Central

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Metadata

Authors
Pessiglione, M., Petrovic, P., Daunizeau, J., Palminteri, S., Dolan, R. J., & Frith, C. D.
Affiliations
  • Inserm (FR)
  • Wellcome Centre for Human Neuroimaging (GB)
Corresponding author
Pessiglione, Mathias
ORCID
Venue
Neuron
Publisher
Elsevier BV
Published
2008-08
Volume
59
Issue
4
Pages
561-567
ISSN
0896-6273 (ISSN-L)
DOI
10.1016/j.neuron.2008.07.005
PMC
PMC2572733
OpenAlex
W2123851461
Cited by
308
References
37
Citations by year
2026: 11 · 2025: 9 · 2024: 5 · 2023: 12 · 2022: 15 · 2021: 11 · 2020: 38 · 2019: 15 · 2018: 24 · 2017: 19 · 2016: 16 · 2015: 19 · 2014: 29 · 2013: 13 · 2012: 19
FWCI
8.96
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuron (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • Max Planck Digital Library (submittedVersion, other-oa)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders
Wellcome Trust
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
subliminal learning, operant conditioning, reward prediction error, ventral striatum, unconscious learning, decision-making, punishment, computational model
MeSH terms
Adult, Association Learning, Attention, Awareness, Brain Mapping, Choice Behavior, Conditioning, Operant, Consciousness, Decision Making, Discrimination, Psychological, Female, Humans, Magnetic Resonance Imaging, Male, Perceptual Masking, Reference Values, Subliminal Stimulation, Visual Cortex, Neostriatum, Intuition

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