Expectancy and surprise predict neural and behavioral measures of attention to threatening stimuli

Attention is preferentially deployed toward those stimuli which are threatening and those which are surprising. The current paper examines the intersection of these phenomena; how do expectations about the threatening nature of stimuli influence the deployment of attention? The predictions tested were that individuals would direct attention toward stimuli which were expected to be threatening (regardless of whether they were or not) and toward stimuli which were surprising. As anxiety has been associated with deficient control of attention to threat, it was additionally predicted that high levels of trait anxiety would be associated with deficits in the use of threat-expectation to guide attention. During fMRI scanning, 29 healthy volunteers completed a simple task in which threat-expectation was manipulated by altering the frequency with which fearful or neutral faces were presented. Individual estimates of threat-expectation and surprise were created using a Bayesian computational model. The degree to which the model derived estimates of threat-expectation and surprise were able to explain both a behavioral measure of attention to the faces and activity in the visual cortex and anterior attentional control areas was then tested. As predicted, increased threat-expectation and surprise were associated with increases in both the behavioral and neuroimaging measures of attention to the faces. Additionally, regions of the orbitofrontal cortex and left amygdala were found to covary with threat-expectation whereas anterior cingulate and lateral prefrontal cortices covaried with surprise. Individuals with higher levels of trait anxiety were less able to modify neuroimaging measures of attention in response to threat-expectation. These results suggest that continuously calculated estimates of the probability of threat may plausibly be used to influence the deployment of visual attention and that use of this information is perturbed in anxious individuals.

[1]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[2]  J. Tanaka,et al.  The NimStim set of facial expressions: Judgments from untrained research participants , 2009, Psychiatry Research.

[3]  I..  THE ATTENTION SYSTEM OF THE HUMAN BRAIN , 2002 .

[4]  R. Rescorla.  A theory of pavlovian conditioning: The effectiveness of reinforcement and non-reinforcement , 1972 .

[5]  G. Logan,et al.  When it helps to be misled: Facilitative effects of increasing the frequency of conflicting stimuli in a Stroop-like task , 1979 .

[6]  Thomas M. Moerland,et al.  Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation , 2005, NeuroImage.

[7]  Timothy E. J. Behrens,et al.  Frontal Cortex Subregions Play Distinct Roles in Choices between Actions and Stimuli , 2008, The Journal of Neuroscience.

[8]  Karl J. Friston,et al.  A Dual Role for Prediction Error in Associative Learning , 2008, Cerebral cortex.

[9]  Jim M. Monti,et al.  Expectation and Surprise Determine Neural Population Responses in the Ventral Visual Stream , 2010, The Journal of Neuroscience.

[10]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[11]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[12]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[13]  M. Posner.  Measuring Alertness , 2008, Annals of the New York Academy of Sciences.

[14]  Mark W Woolrich,et al.  Associative learning of social value , 2008, Nature.

[15]  Guy M. Goodwin,et al.  Lateral Prefrontal Cortex Mediates the Cognitive Modification of Attentional Bias , 2010, Biological Psychiatry.

[16]  Christian Grillon,et al.  Startle reactivity and anxiety disorders: aversive conditioning, context, and neurobiology , 2002, Biological Psychiatry.

[17]  R. Adolphs,et al.  Annals of the New York Academy of Sciences What Does the Amygdala Contribute to Social Cognition? , 2022 .

[18]  David J. C. MacKay,et al.  Information Theory, Inference, and Learning Algorithms , 2004, IEEE Transactions on Information Theory.

[19]  Daniel Dewey,et al.  Learning What to Value , 2011, AGI.

[20]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[21]  S. Mineka,et al.  The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders. , 2008, Acta psychologica.

[22]  E. Rolls.  The functions of the orbitofrontal cortex , 1999, Brain and Cognition.

[23]  Sonia J. Bishop,et al.  Neurocognitive mechanisms of anxiety: an integrative account , 2007, Trends in Cognitive Sciences.

[24]  John M. Pearson,et al.  Surprise Signals in Anterior Cingulate Cortex: Neuronal Encoding of Unsigned Reward Prediction Errors Driving Adjustment in Behavior , 2011, The Journal of Neuroscience.

[25]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[26]  P. Ekman.  Pictures of Facial Affect , 1976 .

[27]  Pierre Baldi,et al.  Bayesian surprise attracts human attention , 2005, Vision Research.

[28]  D. Pfaff,et al.  Molecular and biophysical mechanisms of arousal, alertness, and attention. Preface. , 2008, Annals of the New York Academy of Sciences.

[29]  E. Murray.  The amygdala, reward and emotion , 2007, Trends in Cognitive Sciences.

[30]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[31]  N. Sadato,et al.  Neural substrates of phasic alertness: A functional magnetic resonance imaging study , 2010, Neurosciences research.

[32]  Karl J. Friston,et al.  A free energy principle for the brain , 2006, Journal of Physiology-Paris.