Fear but not awareness predicts enhanced sensory processing in fear conditioning.

It is not clear whether enhanced cortical processing of reinforced stimuli as reported by neuroimaging studies is due to expectancy of an aversive event alone or to activation of the fear system. The present study investigated cortical and autonomic responses of aware participants using an instructed fear conditioning design. Steady-state visual evoked fields (ssVEF) and heart rate change were recorded to assess sensory processing and activation of the fear system by reinforced (CS+) and nonreinforced stimuli (CS-). Participants who showed heart rate acceleration demonstrated increased ssVEFs in visual and parietal cortex during CS+ in acquisition trials. Heart rate decelerators did not show enhanced cortical activation with respect to the CS+. Participants in both groups reported awareness of CS-US contingencies. Awareness of stimulus contingency in fear conditioning seems not to be sufficient to elicit enhanced visual cortical processing.

[1]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

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

[3]  D. Heitjan,et al.  Mixed-effects models in psychophysiology. , 2000, Psychophysiology.

[4]  Peter J. Lang,et al.  Attention and Orienting : Sensory and Motivational Processes , 1997 .

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

[6]  O V Lipp,et al.  Human blink startle during aversive and nonaversive Pavlovian conditioning. , 1994, Journal of experimental psychology. Animal behavior processes.

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

[8]  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.

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

[10]  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.

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

[12]  Andreas Olsson,et al.  Learned Fear of “Unseen” Faces after Pavlovian, Observational, and Instructed Fear , 2004, Psychological science.

[13]  D. Shanks,et al.  The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implications. , 2002, Journal of experimental psychology. Animal behavior processes.

[14]  M. Bradley,et al.  Emotion and motivation I: defensive and appetitive reactions in picture processing. , 2001, Emotion.

[15]  Michael Davis,et al.  Neurobiology of fear responses: the role of the amygdala. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[16]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

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

[18]  Andreas Keil,et al.  Additive effects of emotional content and spatial selective attention on electrocortical facilitation. , 2005, Cerebral cortex.

[19]  H Fischer,et al.  Affective and attentive neural networks in humans: a PET study of Pavlovian conditioning , 1995, Neuroreport.

[20]  J. Pearce,et al.  A model for Pavlovian learning: Variations in the effectiveness of conditioned but not of unconditioned stimuli. , 1980 .

[21]  Fred J Helmstetter,et al.  Functional MRI of human amygdala activity during Pavlovian fear conditioning: stimulus processing versus response expression. , 2003, Behavioral neuroscience.

[22]  P. Lang,et al.  Stimulus repetition and the heart rate response. , 1962, Journal of comparative and physiological psychology.

[23]  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.

[24]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[25]  Changjun Shi,et al.  Visual Pathways Involved in Fear Conditioning Measured with Fear-Potentiated Startle: Behavioral and Anatomic Studies , 2001, The Journal of Neuroscience.

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

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

[28]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[29]  Matthias M. Müller,et al.  Magnetoencephalographic recording of steadystate visual evoked cortical activity , 2005, Brain Topography.

[30]  M. Bradley,et al.  Large-scale neural correlates of affective picture processing. , 2002, Psychophysiology.

[31]  J. R. Hughes,et al.  Human brain electrophysiology. Evoked potentials and evoked magnetic fields in science and medicine , 1989 .

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

[33]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.

[34]  Stefan Wiens,et al.  Effects of trial order and differential conditioning on acquisition of differential shock expectancy and skin conductance conditioning to masked stimuli. , 2003, Psychophysiology.

[35]  A. Hamm,et al.  The neuropsychology of fear learning and fear regulation. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[37]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[38]  Dianne P. O'Leary,et al.  The Use of the L-Curve in the Regularization of Discrete Ill-Posed Problems , 1993, SIAM J. Sci. Comput..

[39]  Stefan Wiens,et al.  Unawareness is more than a chance event: comment on Lovibond and Shanks (2002). , 2002, Journal of experimental psychology. Animal behavior processes.

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

[41]  D. Bates,et al.  Mixed-Effects Models in S and S-PLUS , 2001 .

[42]  U Dimberg,et al.  Nonconscious associative learning: Pavlovian conditioning of skin conductance responses to masked fear-relevant facial stimuli. , 1994, Psychophysiology.

[43]  P. Lang,et al.  Individual differences in autonomic response: conditioned association or conditioned fear? , 1985, Psychophysiology.

[44]  A. Coenen,et al.  Correlation between long latency evoked potentials from amygdala and evoked cardiac response to fear conditioned stimulus in rats. , 2002, Acta neurobiologiae experimentalis.

[45]  S. Holm.  A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[46]  M. Bradley,et al.  Activation of the visual cortex in motivated attention. , 2003, Behavioral neuroscience.

[47]  R. Ilmoniemi,et al.  Signal-space projection method for separating MEG or EEG into components , 1997, Medical and Biological Engineering and Computing.

[48]  K. Hugdahl,et al.  Cortical control of human classical conditioning: autonomic and positron emission tomography data. , 1998, Psychophysiology.

[49]  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.

[50]  Beatrice C. Lacey,et al.  Cognitive Modulation of Time‐Dependent Primary Bradycardia , 1980 .

[51]  Michael I. Posner,et al.  Brain Imaging of Attentional Networks in Normal and Pathological States , 2001, Journal of clinical and experimental neuropsychology.

[52]  Karl J. Friston,et al.  Brain systems mediating aversive conditioning: An event related fMRI study , 1998, NeuroImage.

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

[54]  S. Hillyard,et al.  Combining steady‐state visual evoked potentials and f MRI to localize brain activity during selective attention , 1997, Human brain mapping.

[55]  R. S. Wilson.  CARDIVAR: the statistical analysis of heart rate data. , 1974, Psychophysiology.

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

[57]  Harald T. Schupp,et al.  Emotional Facilitation of Sensory Processing in the Visual Cortex , 2003, Psychological science.

[58]  T. Elbert,et al.  Comparison of data transformation procedures to enhance topographical accuracy in time-series analysis of the human EEG , 2002, Journal of Neuroscience Methods.

[59]  Karl J. Friston,et al.  Variance Components , 2003 .

[60]  R. Hare,et al.  Defensive responses to phobic stimuli , 1975, Biological Psychology.

[61]  P Berg,et al.  A multiple source approach to the correction of eye artifacts. , 1994, Electroencephalography and clinical neurophysiology.

[62]  R. Rescorla.  Pavlovian conditioning. It's not what you think it is. , 1988, The American psychologist.

[63]  Joseph E LeDoux,et al.  Emotional networks in the brain , 2008 .

[64]  M. Bradley,et al.  Motivated attention: Affect, activation, and action. , 1997 .

[65]  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.

[66]  Jorge L. Armony,et al.  Modulation of auditory neural responses by a visual context in human fear conditioning , 2001, Neuroreport.

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