Functional magnetic resonance imaging of temporally distinct responses to emotional facial expressions

Abstract Understanding the temporal dynamics of brain function contributes to models of learning and memory as well as the processing of emotions and habituation. In this article, we present a novel analysis technique to investigate spatiotemporal patterns of activation in response to blocked presentations of emotional stimuli. We modeled three temporal response functions (TRFs), which were maximally sensitive to the onset, early or sustained temporal component of a given block type. This analysis technique was applied to a data set of 29 subjects who underwent functional magnetic resonance imaging while responding to fearful, happy, and sad facial expressions. We identified brain regions that uniquely fit each of the three TRFs for each emotional condition and compared the results to the standard approach, which was based on the canonical hemodynamic response function. We found that voxels within the precuneus fit the onset TRF but did not fit the early or the sustained TRF in all the emotional conditions. On the other hand, voxels within the amygdala fit the sustained TRF, but not the onset or early TRF, during presentation of fearful stimuli, suggesting a spatiotemporal dissociation between these structures. This technique provides researchers with an additional tool in order to investigate the temporal dynamics of neural circuits.

[1]  Deborah A Yurgelun-Todd,et al.  Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces , 2004, NeuroImage.

[2]  D. Hay,et al.  Serial position effects in short-term visual memory: A SIMPLE explanation? , 2007, Memory & cognition.

[3]  Israel Liberzon,et al.  Habituation of Rostral Anterior Cingulate Cortex to Repeated Emotionally Salient Pictures , 2003, Neuropsychopharmacology.

[4]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[5]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

[6]  K. Luan Phan,et al.  Functional Neuroimaging Studies of Human Emotions , 2004, CNS Spectrums.

[7]  Steven C.R. Williams,et al.  Time courses of left and right amygdalar responses to fearful facial expressions , 2001, NeuroImage.

[8]  Edward T. Bullmore,et al.  Differential neural responses to overt and covert presentations of facial expressions of fear and disgust , 2000, NeuroImage.

[9]  Christopher Andrew,et al.  Differential neural responses to overt and covert presentations of facial expressions of fear and disgust , 2000, NeuroImage.

[10]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Richard J. Maddock,et al.  Separating subjective emotion from the perception of emotion-inducing stimuli: An fMRI study , 2006, NeuroImage.

[12]  Karl Magnus Petersson,et al.  The role of precuneus and left inferior frontal cortex during source memory episodic retrieval , 2005, NeuroImage.

[13]  G. Boynton,et al.  Adaptation: from single cells to BOLD signals , 2006, Trends in Neurosciences.

[14]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[15]  Ravi S. Menon,et al.  Spatial and temporal limits in cognitive neuroimaging with fMRI , 1999, Trends in Cognitive Sciences.

[16]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[17]  S E Petersen,et al.  Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Turner,et al.  Detecting Latency Differences in Event-Related BOLD Responses: Application to Words versus Nonwords and Initial versus Repeated Face Presentations , 2002, NeuroImage.

[19]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[20]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[21]  Randy L. Buckner,et al.  Mixed blocked/event-related designs separate transient and sustained activity in fMRI , 2003, NeuroImage.

[22]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[23]  R. Maddock,et al.  Time course of the subjective emotional response to aversive pictures: relevance to fMRI studies , 2001, Psychiatry Research: Neuroimaging.

[24]  S. Rauch,et al.  A functional MRI study of human amygdala responses to facial expressions of fear versus anger. , 2001, Emotion.

[25]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[26]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[27]  John E. Desmond,et al.  Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task , 2005, Neuropsychologia.

[28]  John G. Neuhoff,et al.  Spatiotemporal Pattern of Neural Processing in the Human Auditory Cortex , 2002, Science.

[29]  Tom Johnstone,et al.  Stability of amygdala BOLD response to fearful faces over multiple scan sessions , 2005, NeuroImage.

[30]  R. Dolan,et al.  fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. , 2004, Journal of neurophysiology.

[31]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[32]  Koji Inui,et al.  Temporal Dynamics of Neural Adaptation Effect in the Human Visual Ventral Stream , 2004, The Journal of Neuroscience.

[33]  Leslie G. Ungerleider,et al.  Repetition suppression of faces is modulated by emotion. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Randy L Buckner,et al.  The hemodynamic inverse problem: Making inferences about neural activity from measured MRI signals , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  David N. Kennedy,et al.  fMRI of sensitization to angry faces , 2005, NeuroImage.

[36]  J. Gorman,et al.  Differential time courses and specificity of amygdala activity in posttraumatic stress disorder subjects and normal control subjects , 2005, Biological Psychiatry.

[37]  S Braeutigam,et al.  Task-dependent early latency (30–60 ms) visual processing of human faces and other objects , 2001, Neuroreport.

[38]  P. Bandettini,et al.  Understanding neural system dynamics through task modulation and measurement of functional MRI amplitude, latency, and width , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[39]  H. Critchley,et al.  Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study , 2000, Human brain mapping.

[40]  R. Cox,et al.  Event‐related fMRI contrast when using constant interstimulus interval: Theory and experiment , 2000, Magnetic resonance in medicine.

[41]  T. Allison,et al.  Electrophysiological studies of human face perception. II: Response properties of face-specific potentials generated in occipitotemporal cortex. , 1999, Cerebral cortex.

[42]  A. Young,et al.  Task instructions modulate neural responses to fearful facial expressions , 2003, Biological Psychiatry.

[43]  Kathleen Moore,et al.  Creativity, oversensitivity, and rate of habituation , 1996 .

[44]  P. Whalen Fear, Vigilance, and Ambiguity , 1998 .

[45]  M. D’Esposito,et al.  The variability of human BOLD hemodynamic responses , 1998, NeuroImage.

[46]  R. Dolan,et al.  Neural Activation during Covert Processing of Positive Emotional Facial Expressions , 1996, NeuroImage.

[47]  M. Thase,et al.  Can’t shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals , 2002, Biological Psychiatry.

[48]  S. Rauch,et al.  Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli , 2001, Neuroreport.

[49]  A. David,et al.  Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies , 2008, Brain Research Reviews.

[50]  Murray B. Stein,et al.  Habituation of attentional networks during emotion processing , 2002, Neuroreport.