The influence of prior expectations on emotional face perception in adolescence.

Prior expectations influence the way incoming stimuli are processed. A standard, validated way of manipulating prior expectations is to bias participants to perceive a stimulus by instructing them to look out for this type of stimulus. Here, we investigated the influence of prior expectations on the processing of incoming stimuli (emotional faces) in adolescence. Using functional magnetic resonance imaging, we assessed activity and functional connectivity in 13 adolescents and 13 healthy adults (matched for gender and intelligence quotient), while they were presented with sequences of emotional faces (happy, fearful, or angry). A specific instruction at the start of each sequence instructed the participants to look out for fearful or angry faces in the subsequent sequence. Both groups responded more accurately and with shorter reaction times (RTs) to faces that were congruent with the instruction. For anger, this bias was lower in the adolescents (for RTs), and adults demonstrated greater activation than adolescents in the ventro-medial prefrontal cortex (vMPFC) and greater functional connectivity between the vMPFC and the thalamus when the face was congruent with the instruction. Our results demonstrate that the influence of prior expectations (in the form of an instruction) on the subsequent processing of face stimuli is still developing in the adolescent brain.

[1]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[2]  Geoffrey E. Hinton,et al.  The Helmholtz Machine , 1995, Neural Computation.

[3]  M. Kringelbach.  The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[4]  C. Summerfield,et al.  Expectation (and attention) in visual cognition , 2009, Trends in Cognitive Sciences.

[5]  C. Summerfield,et al.  A Neural Representation of Prior Information during Perceptual Inference , 2008, Neuron.

[6]  Catalina J. Hooper,et al.  Adolescents' performance on the Iowa Gambling Task: implications for the development of decision making and ventromedial prefrontal cortex. , 2004, Developmental psychology.

[7]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[8]  Ashley R. Smith,et al.  Developmental Differences in Posterior Mesofrontal Cortex Recruitment by Risky Rewards , 2007, The Journal of Neuroscience.

[9]  Carrie L. Masten,et al.  Entering Adolescence: Resistance to Peer Influence, Risky Behavior, and Neural Changes in Emotion Reactivity , 2011, Neuron.

[10]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[11]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[12]  B. Dosher,et al.  Mechanisms of perceptual learning , 1999, Vision Research.

[13]  J. Wallis.  Orbitofrontal cortex and its contribution to decision-making. , 2007, Annual review of neuroscience.

[14]  M. Phillips,et al.  Annotation: Development of facial expression recognition from childhood to adolescence: behavioural and neurological perspectives. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[15]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[16]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[17]  Monique Ernst,et al.  Developmental differences in neuronal engagement during implicit encoding of emotional faces: an event-related fMRI study. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[18]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[19]  Andrew N. Meltzoff,et al.  Brain Activation during Face Perception: Evidence of a Developmental Change , 2005, Journal of Cognitive Neuroscience.

[20]  C. Carter,et al.  Anterior cingulate cortex and conflict detection: An update of theory and data , 2007, Cognitive, affective & behavioral neuroscience.

[21]  C. Olson,et al.  Organization of cortical and subcortical projections to medial prefrontal cortex in the cat , 1988, The Journal of comparative neurology.

[22]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[23]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[24]  Deborah A. Yurgelun-Todd,et al.  Neural correlates of emotional intelligence in adolescent children , 2007, Cognitive, affective & behavioral neuroscience.

[25]  G. Bird,et al.  Social attitudes differentially modulate imitation in adolescents and adults , 2011, Experimental Brain Research.

[26]  G. Bruce Pike,et al.  Development of Functional Connectivity during Adolescence: A Longitudinal Study Using an Action–Observation Paradigm , 2011, Journal of Cognitive Neuroscience.

[27]  Monique Ernst,et al.  A developmental examination of gender differences in brain engagement during evaluation of threat , 2004, Biological Psychiatry.

[28]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[29]  E Zarahn,et al.  Cortical brain regions engaged by masked emotional faces in adolescents and adults: an fMRI study. , 2001, Emotion.

[30]  T. Jernigan,et al.  Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study , 2002, Developmental medicine and child neurology.

[31]  Andreas Schulze-Bonhage,et al.  The reliability of fMRI activations in the medial temporal lobes in a verbal episodic memory task , 2005, NeuroImage.

[32]  M. Phillips,et al.  The development of emotion-processing in children: effects of age, emotion, and intensity. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[33]  J. O'Doherty,et al.  The Role of the Ventromedial Prefrontal Cortex in Abstract State-Based Inference during Decision Making in Humans , 2006, The Journal of Neuroscience.

[34]  Erin B. McClure-Tone,et al.  Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. , 2008, Archives of general psychiatry.

[35]  B. Dosher,et al.  Mechanisms of perceptual learning , 1999, Vision Research.

[36]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[37]  Alessandra M Passarotti,et al.  Neural correlates of incidental and directed facial emotion processing in adolescents and adults. , 2009, Social cognitive and affective neuroscience.

[38]  Michael J. Brammer,et al.  Maturation of limbic corticostriatal activation and connectivity associated with developmental changes in temporal discounting , 2011, NeuroImage.

[39]  Frederic Dick,et al.  Developmental Changes in Effective Connectivity in the Emerging Core Face Network , 2010, Cerebral cortex.

[40]  Timothy Edward John Behrens,et al.  Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour , 2007, Trends in Cognitive Sciences.

[41]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[42]  Kelvin O. Lim,et al.  White Matter Integrity Predicts Delay Discounting Behavior in 9- to 23-Year-Olds: A Diffusion Tensor Imaging Study , 2009, Journal of Cognitive Neuroscience.

[43]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[44]  M. Bar,et al.  Magnocellular Projections as the Trigger of Top-Down Facilitation in Recognition , 2007, The Journal of Neuroscience.

[45]  T. Q. Irigaray,et al.  Intellectual abilities in Alzheimer's disease patients: Contributions from the Wechsler Abbreviated Scale of Intelligence (WASI) , 2010 .

[46]  G. Glover,et al.  Biological Substrates of Emotional Reactivity and Regulation in Adolescence During an Emotional Go-Nogo Task , 2008, Biological Psychiatry.

[47]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[48]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

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

[50]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[51]  Kevin S LaBar,et al.  Development of emotional facial recognition in late childhood and adolescence. , 2007, Developmental science.

[52]  E. Crone,et al.  Developmental Changes in Real Life Decision Making: Performance on a Gambling Task Previously Shown to Depend on the Ventromedial Prefrontal Cortex , 2004, Developmental neuropsychology.

[53]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[54]  J. Giedd.  Structural Magnetic Resonance Imaging of the Adolescent Brain , 2004, Annals of the New York Academy of Sciences.

[55]  Roberto Toro,et al.  Neural Mechanisms of Resistance to Peer Influence in Early Adolescence , 2007, The Journal of Neuroscience.

[56]  Ellen Leibenluft,et al.  Adolescent immaturity in attention-related brain engagement to emotional facial expressions , 2003, NeuroImage.

[57]  L. Pessoa.  On the relationship between emotion and cognition , 2008, Nature Reviews Neuroscience.