Not what you expect: experience but not expectancy predicts conditioned responses in human visual and supplementary cortex.

When paired with aversive events, visual conditioned stimuli (CS) provoke increased activations in visual cortex. It is unclear however whether these changes reflect cognitive processes such as expectancy of the aversive unconditioned stimulus (US), or implicit associative learning of the contingencies outside awareness. Here, we used the "gambler's fallacy" phenomenon to parametrically and inversely manipulate the expectancy of an US and the number of conditioning trials: Increasing the number of CS-US pairings was associated with participants expecting the US to be less likely and vice versa. Magnetocortical activity evoked by the CS in occipital and supplementary motor areas was linearly related to the associative strength (number of CS-US pairings), but decreased as a function of expectancy. These results suggest that the cortical facilitation of fear cue processing is determined by associative strength and previous exposure to learning contingencies rather than by the cognitive anticipation for the US.

[1]  Matthias M. Müller,et al.  Can the Spotlight of Attention Be Shaped Like a Doughnut? Evidence From Steady-State Visual Evoked Potentials , 2002 .

[2]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[3]  H. T. Nguyen,et al.  Expression of conditional fear with and without awareness , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Matthias M. Müller,et al.  Concurrent recording of steady-state and transient event-related potentials as indices of visual-spatial selective attention , 2000, Clinical Neurophysiology.

[5]  P. Perruchet A pitfall for the expectancy theory of human eyelid conditioning , 1985, The Pavlovian journal of biological science.

[6]  Fred J Helmstetter,et al.  Neural Substrates Mediating Human Delay and Trace Fear Conditioning , 2004, The Journal of Neuroscience.

[7]  Mats Fredrikson,et al.  Right-sided human prefrontal brain activation during acquisition of conditioned fear. , 2002, Emotion.

[8]  Martin Ingvar,et al.  On the unconscious subcortical origin of human fear , 2007, Physiology & Behavior.

[9]  L. Weiskrantz,et al.  Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. , 2001, Brain : a journal of neurology.

[10]  R. Blair,et al.  An exact statistical method for comparing topographic maps, with any number of subjects and electrodes , 2005, Brain Topography.

[11]  Elliot A. Stein,et al.  Functional MRI of human amygdala activity during Pavlovian fear conditioning: Stimulus processing versus response expression , 2003 .

[12]  Andreas Keil,et al.  Hypofunction of right temporoparietal cortex during emotional arousal in depression. , 2008, Archives of general psychiatry.

[13]  Andreas Keil,et al.  Fear but not awareness predicts enhanced sensory processing in fear conditioning. , 2006, Psychophysiology.

[14]  O. Jensen,et al.  A New Method to Identify Multiple Sources of Oscillatory Activity from Magnetoencephalographic Data , 2002, NeuroImage.

[15]  R. B. Silberstein,et al.  Steady-State Visually Evoked Potential Topography during Processing of Emotional Valence in Healthy Subjects , 2002, NeuroImage.

[16]  D. Regan Human brain electrophysiology: Evoked potentials and evoked magnetic fields in science and medicine , 1989 .

[17]  Andreas Keil,et al.  Adaptation in human visual cortex as a mechanism for rapid discrimination of aversive stimuli , 2007, NeuroImage.

[18]  Matthias M. Müller,et al.  Neuronal correlates of repetition priming of frequently presented objects: Insights from induced gamma band responses , 2007, Neuroscience Letters.

[19]  Harald T Schupp,et al.  Affective blindsight: intact fear conditioning to a visual cue in a cortically blind patient. , 2003, Brain : a journal of neurology.

[20]  A. Keil,et al.  Neural mechanisms of evoked oscillations: Stability and interaction with transient events , 2007, Human brain mapping.

[21]  Matthias M. Müller,et al.  Effects of picture repetition on induced gamma band responses, evoked potentials, and phase synchrony in the human EEG. , 2002, Brain research. Cognitive brain research.

[22]  W. Perlstein,et al.  Steady-state visual evoked potentials reveal frontally-mediated working memory activity in humans , 2003, Neuroscience Letters.

[23]  Joseph Ciorciari,et al.  Steady-State Visually Evoked Potential topography associated with a visual vigilance task , 2005, Brain Topography.

[24]  M. Bradley,et al.  Electrocortical and electrodermal responses covary as a function of emotional arousal: a single-trial analysis. , 2008, Psychophysiology.

[25]  Andreas Keil,et al.  Motivated attention in emotional picture processing is reflected by activity modulation in cortical attention networks , 2004, NeuroImage.

[26]  Joseph R. Manns,et al.  PSYCHOLOGICAL SCIENCE Research Article TRACE AND DELAY EYEBLINK CONDITIONING: Contrasting Phenomena of Declarative and Nondeclarative Memory , 2022 .

[27]  S. Hillyard,et al.  Selective attention to stimulus location modulates the steady-state visual evoked potential. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[28]  R. Rosenthal,et al.  Contrast Analysis: Focused Comparisons in the Analysis of Variance , 1985 .

[29]  A. Hamm,et al.  Affective learning: awareness and aversion. , 1996, Psychophysiology.

[30]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

[31]  Matthias M. Müller,et al.  Early modulation of visual perception by emotional arousal: Evidence from steady-state visual evoked brain potentials , 2003, Cognitive, affective & behavioral neuroscience.

[32]  Matthias M. Müller,et al.  Modulation of oscillatory brain activity and evoked potentials in a repetition priming task in the human EEG , 2004, The European journal of neuroscience.

[33]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[34]  D. Amaral Amygdalohippocampal and amygdalocortical projections in the primate brain. , 1986, Advances in experimental medicine and biology.

[35]  D. Louis Collins,et al.  Design and construction of a realistic digital brain phantom , 1998, IEEE Transactions on Medical Imaging.

[36]  Leslie G. Ungerleider,et al.  Visual awareness and the detection of fearful faces. , 2005, Emotion.

[37]  Joseph E LeDoux The emotional brain , 1996 .

[38]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  Adam P. Morris,et al.  Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression , 2004, The Journal of Neuroscience.

[41]  Andreas Keil,et al.  Cortical activation during Pavlovian fear conditioning depends on heart rate response patterns: an MEG study. , 2005, Brain research. Cognitive brain research.

[42]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

[43]  Karl J. Friston,et al.  Brain Systems Mediating Aversive Conditioning: an Event-Related fMRI Study , 1998, Neuron.

[44]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.