Elsevier

NeuroImage

Volume 44, Issue 1, 1 January 2009, Pages 243-251
NeuroImage

The influence of feedback valence in associative learning

https://doi.org/10.1016/j.neuroimage.2008.08.038Get rights and content

Abstract

The neural systems engaged by intrinsic positive or negative feedback were defined in an associative learning task. Through trial and error, participants learned the arbitrary assignments of a set of stimuli to one of two response categories. Informative feedback was provided on less than 25% of the trials. During positive feedback blocks, half of the trials were eligible for informative feedback; of these, informative feedback was only provided when the response was correct. A similar procedure was used on negative feedback blocks, but here informative feedback was only provided when the response was incorrect. In this manner, we sought to identify regions that were differentially responsive to positive and negative feedback as well as areas that were responsive to both types of informative feedback. Several regions of interest, including the bilateral nucleus accumbens, caudate nucleus, anterior insula, right cerebellar lobule VI, and left putamen, were sensitive to informative feedback regardless of valence. In contrast, several regions were more selective to positive feedback compared to negative feedback. These included the insula, amygdala, putamen, and supplementary motor area. No regions were more strongly activated by negative feedback compared to positive feedback. These results indicate that the neural areas supporting associative learning vary as a function of how that information is learned. In addition, areas linked to intrinsic reinforcement showed considerable overlap with those identified in studies using extrinsic reinforcers.

Section snippets

Experimental design

Twelve right-handed participants (five male, seven female) aged 18 to 27 years (average age 20 years) gave written informed consent in accordance with the Dartmouth College human subjects committee. Subjects were told that the study would examine their ability to learn simple response associations through trial and error.

On each trial, the subject saw a single letter stimulus and pressed one of two response keys with either the index or middle finger of the right hand. The stimulus set

Behavior

We first examined how well the participants learned the associations under the limited feedback conditions employed in the current study. To this end, we looked at responses on trials to stimuli that had been previously linked to informative feedback (paired trials). Participants responded correctly on 80.69% ±  9.89 (average ± SD) of the paired trials in the positive feedback condition, and 73.62% ± 13.05 in the negative feedback condition. Both values were significantly greater than a chance

Discussion

Learning requires the use of feedback. Behavior can be positively reinforced to promote a desired behavior; alternatively, behavior can be negatively reinforced in an effort to decrease the likelihood of an undesirable behavior. In most empirical studies of reinforcement, positive and negative reinforcements are intermixed, at least implicitly. In the current study, we introduced a task in which feedback was completely uninformative on a large proportion of trials. In this way, we sought to

Conclusion

An important form of associative learning requires the arbitrary linkage of an action to a stimulus. Most studies of associative learning use a trial and error approach (Toni and Passingham, 1999, Toni et al., 2001) in which feedback is provided on every trial. This procedure makes it difficult to dissociate the effects of feedback unless a large temporal gap separates the stimulus, response, and feedback signals. By separating blocks that used positive and negative feedback in combination with

Acknowledgments

Supported by PHS grants NS33504 and NS40813. Corresponding author: Scott T. Grafton, M.D., Sage Center for the Study of Mind, Department of Psychology, Psychology East, UC Santa Barbara, Santa Barbara CA 93106.

References (67)

  • ItoM.

    Mechanisms of motor learning in the cerebellum

    Brain Res.

    (2000)
  • KringelbachM.L. et al.

    The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology

    Prog. Neurobiol.

    (2004)
  • McClureS.M. et al.

    Temporal prediction errors in a passive learning task activate human striatum

    Neuron

    (2003)
  • McClureS.M. et al.

    A computational substrate for incentive salience

    Trends Neurosci.

    (2003)
  • MiddletonF.A. et al.

    Basal ganglia and cerebellar loops: motor and cognitive circuits

    Brains Res. Rev.

    (2000)
  • NieuwenhuisS. et al.

    Activity in human reward-sensitive brain areas is strongly context dependent

    Neuroimage

    (2005)
  • PaulusM.P. et al.

    Decision making by methamphetamine-dependent subjects is associated with error-rate-independent decrease in prefrontal and parietal activation

    Biol. Psychiatry

    (2003)
  • PaulusM.P. et al.

    Superior temporal gyrus and insula provide response and outcome-dependent information during assessment and action selection in a decision-making situation

    Neuroimage

    (2005)
  • SangerT.

    Optimal unsupervised learning in a single-layer linear feedforward neural network

    Neural Netw.

    (1989)
  • SchultzW. et al.

    Reward prediction in primate basal ganglia and frontal cortex

    Neuropharmacology

    (1998)
  • ThompsonR.F. et al.

    Associative learning

    Int. Rev. Neurobiol.

    (1997)
  • ToniI. et al.

    Learning arbitrary visuomotor associations: temporal dynamic of brain activity

    NeuroImage

    (2001)
  • TricomiE.M. et al.

    Modulation of caudate activity by action contingency

    Neuron

    (2004)
  • Tzourio-MazoyerN. et al.

    Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain

    NeuroImage

    (2002)
  • ZinkC.F. et al.

    Human striatal responses to monetary reward depend on saliency

    Neuron

    (2004)
  • AblerB. et al.

    Neural correlates of frustration

    Neuroreport

    (2005)
  • AlexanderG.E. et al.

    Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions

  • AshburnerJ. et al.

    Nonlinear spatial normalization using basis functions

    Hum. Brain Mapp.

    (1999)
  • BaxterM.G. et al.

    The amygdala and reward

    Nat. Rev., Neurosci.

    (2002)
  • BernsG.S. et al.

    Predictability modulates human brain response to reward

    J. Neurosci.

    (2001)
  • Bischoff-GretheA. et al.

    Cerebellar involvement in response reassignment rather than attention

    J. Neurosci.

    (2002)
  • CaseyB.J. et al.

    Dissociation of response conflict, attentional selection, and expectancy with functional magnetic resonance imaging

    Proc. Natl. Acad. Sci. U. S. A.

    (2000)
  • CoolsR. et al.

    Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging

    J. Neurosci.

    (2002)
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