Elsevier

Neuroscience

Volume 158, Issue 2, 23 January 2009, Pages 721-731
Neuroscience

Cognitive Neuroscience
Neural, electrodermal and behavioral response patterns in contingency aware and unaware subjects during a picture–picture conditioning paradigm

https://doi.org/10.1016/j.neuroscience.2008.09.049Get rights and content

Abstract

One way of investigating affective learning is the use of aversive pictures as unconditioned stimuli (UCS) in conditioning paradigms. In the last decades, there has been a heated debate on the influence of contingency awareness on conditioned responses (CRs). Only a few studies found CRs in contingency unaware subjects whereas other studies only reported conditioned reactions in contingency aware participants. However, as a shortcoming, most studies employing picture–picture paradigms only investigated one response level (e.g. changes in subjective ratings). Further, changes in brain activity have so far been neglected in this field of research. The aim of the present study was to investigate different response levels with respect to contingency awareness: brain activity measured by functional magnetic resonance imaging (fMRI), skin conductance responses (SCRs) and valence ratings. A neutral geometric shape (conditioned stimulus, CS+) was followed by aversive pictures, whereas another shape (CS−) preceded neutral pictures. Unaware participants showed CRs in brain activity (e.g. the insula). Generally more activity was observed in the fear network (e.g. the amygdala, the lateral orbitofrontal cortex) in aware participants and in the nucleus accumbens (NAcc). Investigation of SCRs and valence ratings revealed that only aware participants showed conditioned reactions. Our results point toward dissociations between response levels (e.g. brain activity) not affected by contingency awareness and more cognitive response levels (e.g. subjective ratings and SCRs) which are affected by contingency awareness. As a unique finding in human aversive conditioning, we discuss the role of the nucleus accumbens as well as practical implications for affective learning models.

Section snippets

Subjects

A total of 32 subjects (18 females) with a mean age of 23.26 years (S.D.=3.90) participated in the study. All participants were right-handed and had normal or corrected-to-normal vision. None of the subjects had a history of psychiatric or neurological disorders. The majority were students, who responded to announcements posted at the campus of the University of Giessen. Participants were informed about the procedure in general (but not the conditioning paradigm until the experiment was

Contingency awareness

One principal aim was to investigate the influence of contingency awareness on SCRs, valence ratings and neural activity. A somewhat surprising finding was that a total of 18 participants (10 female; 8 male) did not recognize the association between CS and UCS (all chose the answer “d” in both cases). Fourteen participants (eight female; six male) could be classified as “aware.” All aware subjects chose answer “c” (“Before the aversive pictures, there was never a picture of a rhomb/of a

Discussion

The present study investigated CRs using aversive pictures as UCS in a differential fear conditioning paradigm. We assessed three different response systems: (1) subjective ratings, (2) SCRs and (3) BOLD responses as indicators of emotional learning. As the main finding, contingency aware and unaware subjects showed different conditioned reactions with respect to the response systems. Furthermore, we found increased NAcc activation to the CS+ in contingency aware subjects.

In detail, significant

Acknowledgments

This work was supported by the DFG Graduiertenkolleg GRK 885 “NeuroAct.”

References (75)

  • C. Martin-Soelch et al.

    Appetitive conditioning: neural bases and implications for psychopathology

    Neurosci Biobehav Rev

    (2007)
  • M.R. Milad et al.

    A role for the human dorsal anterior cingulate cortex in fear expression: stress and anxiety: Developmental and therapeutic perspectives

    Biol Psychiatry

    (2007)
  • J.S. Morris et al.

    Dissociable amygdala and orbitofrontal responses during reversal fear conditioning

    Neuroimage

    (2004)
  • B.O. Olatunji et al.

    Evaluative differential conditioning of disgust: a sticky form of relational learning that is resistant to extinction

    J Anxiety Disord

    (2007)
  • M.P. Paulus et al.

    An insular view of anxiety

    Biol Psychiatry

    (2006)
  • M.A. Pezze et al.

    Mesolimbic dopaminergic pathways in fear conditioning

    Prog Neurobiol

    (2004)
  • A. Simmons et al.

    Intolerance of uncertainty correlates with insula activation during affective ambiguity

    Neurosci Lett

    (2008)
  • J. Spicer et al.

    Sensitivity of the nucleus accumbens to violations in expectation of reward

    Neuroimage

    (2007)
  • R. Stark et al.

    Erotic and disgust-inducing pictures: differences in the hemodynamic responses of the brain

    Biol Psychol

    (2005)
  • R. Stark et al.

    Hemodynamic brain correlates of disgust and fear ratings

    Neuroimage

    (2007)
  • T. Straube et al.

    Effects of cognitive-behavioral therapy on brain activation in specific phobia

    Neuroimage

    (2006)
  • T. Straube et al.

    Neural mechanisms of automatic and direct processing of phobogenic stimuli in specific phobia

    Biol Psychiatry

    (2006)
  • T. Straube et al.

    Waiting for spiders: brain activation during anticipatory anxiety in spider phobics

    Neuroimage

    (2007)
  • T. Straube et al.

    Time course of amygdala activation during aversive conditioning depends on attention

    Neuroimage

    (2007)
  • K. Tabbert et al.

    Hemodynamic responses of the amygdala, the orbitofrontal cortex and the visual cortex during a fear conditioning paradigm: neurobiology of fear and disgust

    Int J Psychophysiol

    (2005)
  • K. Tabbert et al.

    Dissociation of neural responses and skin conductance reactions during fear conditioning with and without awareness of stimulus contingencies

    Neuroimage

    (2006)
  • M. Turnock et al.

    A neural network model of hippocampal-striatal-prefrontal interactions in contextual conditioning

    Brain Res

    (2008)
  • E.A. Antoniadis et al.

    Fornix, medial prefrontal cortex, nucleus accumbens, and mediodorsal thalamic nucleus: roles in a fear-based context discrimination task

    Neurobiol Learn Mem

    (2005)
  • D.J. Berlau et al.

    Basolateral amygdala lesions do not prevent memory of context-footshock training

    Learn Mem

    (2003)
  • M.M. Bradley et al.

    Activation of the visual cortex in motivated attention

    Behav Neurosci

    (2003)
  • S. Bray et al.

    Neural coding of reward-prediction error signals during classical conditioning with attractive faces

    J Neurophysiol

    (2007)
  • C. Büchel et al.

    Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging

    J Neurosci

    (1999)
  • J.M. Cisler et al.

    Towards a causal model for disgust in the anxiety disorders: an integration of evidence from neuroscience

    Curr Psychiatry Rev

    (2008)
  • C.R. Cloninger

    Biology of personality dimensions

    Curr Opin Psychiatry

    (2000)
  • J.C. Cooper et al.

    Valence and salience contribute to nucleus accumbens activation

    Neuroimage

    (2007)
  • M.E. Dawson et al.

    Construct validity of recall and recognition postconditioning measures of awareness

    J Exp Psychol

    (1973)
  • M.E. Dawson et al.

    Under what conditions can human affective conditioning occur without contingency awareness?Test of the evaluative conditioning paradigm

    Emotion

    (2007)
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