The Development of Face Recognition; Hippocampal and Frontal Lobe Contributions Determined with MEG

Face recognition skills improve steadily across childhood, yet few studies have investigated the development of the neural sources underlying these processes. We investigated the developmental changes in brain activity related specifically to face recognition, using magnetoencephalography (MEG). We studied 70 children (6–19 years) and 20 young adults. Photographs of 240 neutral faces were used in two blocks of 1-back recognition tasks; one block contained faces upright and in the other block, faces were presented inverted. MEG activity was recorded on a 151 sensor CTF/MISL system. A structural MRI was acquired for all subjects. We focussed on the repetition effects of the faces, in a 280–680 ms window, contrasting the repeated faces with the first presentation of the faces. The analyses showed reliable right hippocampal activation across all age groups, and a right inferior frontal activation that emerged for repeated, recognised faces at 10–11 years of age. The hippocampi are implicated in memory function and we demonstrate that the right hippocampus is specifically involved for face recognition. Further, we determined that this comes on-line by early school age, which is consistent with the known early maturation of the hippocampi. In contrast, we show that the right inferior frontal areas do not come on-line until later in childhood, consistent with the protracted development of the frontal cortices. These data support the hypothesis that different age groups use different strategies and neural structures for face recognition.

[1]  Margot J. Taylor,et al.  Face Recognition Memory and Configural Processing: A Developmental ERP Study using Upright, Inverted, and Contrast-Reversed Faces , 2004, Journal of Cognitive Neuroscience.

[2]  Anneli Kylliäinen,et al.  Face and gaze processing in normally developing children: a magnetoencephalographic study , 2006, The European journal of neuroscience.

[3]  James W. Tanaka,et al.  Face recognition in young children : When the whole is greater than the sum of its parts , 1998 .

[4]  Beatriz Luna,et al.  Brain Basis of Developmental Change in Visuospatial Working Memory , 2006, Journal of Cognitive Neuroscience.

[5]  Anders M. Fjell,et al.  Heterogeneity in Subcortical Brain Development: A Structural Magnetic Resonance Imaging Study of Brain Maturation from 8 to 30 Years , 2009, The Journal of Neuroscience.

[6]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[7]  Kiralee M. Hayashi,et al.  Dynamic mapping of normal human hippocampal development , 2006, Hippocampus.

[8]  O. Krastoshevsky,et al.  Hippocampal Contributions to Episodic Encoding : Insights From Relational and Item-Based Learning , 2002 .

[9]  Jay N Giedd,et al.  Anatomical brain magnetic resonance imaging of typically developing children and adolescents. , 2009, Journal of the American Academy of Child and Adolescent Psychiatry.

[10]  Gillian Rhodes,et al.  What's lost in inverted faces? , 1993, Cognition.

[11]  Jane E. Raymond,et al.  Neural Correlates of Enhanced Visual Short-Term Memory for Angry Faces: An fMRI Study , 2008, PloS one.

[12]  S. Platek,et al.  Is family special to the brain? An event-related fMRI study of familiar, familial, and self-face recognition , 2009, Neuropsychologia.

[13]  David Poeppel,et al.  Reconstructing spatio-temporal activities of neural sources using MEG vector beamformer , 2000, NeuroImage.

[14]  Deanna M. Barch,et al.  Functional developmental similarities and differences in the neural correlates of verbal and nonverbal working memory tasks , 2008, Neuropsychologia.

[15]  Margot J. Taylor,et al.  Unattended emotional faces elicit early lateralized amygdala–frontal and fusiform activations , 2010, NeuroImage.

[16]  M. Baenninger The development of face recognition: featural or configurational processing? , 1994, Journal of experimental child psychology.

[17]  A. Burton,et al.  Brain responses to repetitions of human and animal faces, inverted faces, and objects — An MEG study , 2007, Brain Research.

[18]  K. Nakayama,et al.  Rapid adaptation of the m170 response: importance of face parts. , 2008, Cerebral cortex.

[19]  F. Benes,et al.  Myelination of cortical-hippocampal relays during late adolescence. , 1989, Schizophrenia bulletin.

[20]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[21]  V. M. Cassia,et al.  The effect of inversion on 3- to 5-year-olds' recognition of face and nonface visual objects. , 2009, Journal of experimental child psychology.

[22]  T. Robbins,et al.  Dissociable roles of prefrontal subregions in self-ordered working memory performance , 2008, Neuropsychologia.

[23]  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.

[24]  Margot J. Taylor,et al.  Detection and localization of hippocampal activity using beamformers with MEG: A detailed investigation using simulations and empirical data , 2011, Human brain mapping.

[25]  V. Menon,et al.  Neural basis of protracted developmental changes in visuo-spatial working memory , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[26]  David Poeppel,et al.  Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique , 2001, IEEE Transactions on Biomedical Engineering.

[27]  J. Haxby,et al.  Neural response to the visual familiarity of faces , 2006, Brain Research Bulletin.

[28]  S. Carey Becoming a face expert. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  P. Ellen Grant,et al.  Developmental neural networks in children performing a Categorical N-Back Task , 2006, NeuroImage.

[30]  Masato Yumoto,et al.  Children are sensitive to averted eyes at the earliest stage of gaze processing , 2004, Neuroreport.

[31]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[32]  N. George,et al.  Older adults' configural processing of faces: role of second-order information. , 2011, Psychology and aging.

[33]  Lily Riggs,et al.  A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography , 2009, NeuroImage.

[34]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[35]  J. Karhu,et al.  Theta oscillations index human hippocampal activation during a working memory task. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. D’Esposito,et al.  Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information , 2001, Neuron.

[37]  Thomas Kailath,et al.  Performance analysis of the optimum beamformer in the presence of correlated sources and its behavior under spatial smoothing , 1987, IEEE Trans. Acoust. Speech Signal Process..

[38]  Margot J. Taylor,et al.  Attention inhibition of early cortical activation to fearful faces , 2010, Brain Research.

[39]  D. Maurer,et al.  The many faces of configural processing , 2002, Trends in Cognitive Sciences.

[40]  Margot J. Taylor,et al.  Inversion and contrast-reversal effects on face processing assessed by MEG , 2006, Brain Research.

[41]  Margot J. Taylor,et al.  Spatio temporal dynamics of face recognition. , 2008, Cerebral cortex.

[42]  Se Robinson,et al.  Functional neuroimaging by Synthetic Aperture Magnetometry (SAM) , 1999 .

[43]  E. Pang,et al.  Recognising upright and inverted faces: MEG source localisation , 2011, Brain Research.

[44]  R. Yin Looking at Upside-down Faces , 1969 .

[45]  Ricardo Insausti,et al.  Postnatal development of the human hippocampal formation. , 2009, Advances in anatomy, embryology, and cell biology.

[46]  Alumit Ishai,et al.  Recognition memory of newly learned faces , 2006, Brain Research Bulletin.

[47]  Danielle C. Turner,et al.  Association Between Response Inhibition and Working Memory in Adult ADHD: A Link to Right Frontal Cortex Pathology? , 2007, Biological Psychiatry.

[48]  M. D’Esposito,et al.  Longitudinal Evidence for Functional Specialization of the Neural Circuit Supporting Working Memory in the Human Brain , 2010, The Journal of Neuroscience.

[49]  Margot J. Taylor,et al.  Effects of repetition and configural changes on the development of face recognition processes. , 2004, Developmental science.

[50]  D. Maurer,et al.  Configural Face Processing Develops more Slowly than Featural Face Processing , 2002, Perception.

[51]  A. Bailey,et al.  Face‐ and gaze‐sensitive neural responses in children with autism: a magnetoencephalographic study , 2006, The European journal of neuroscience.

[52]  A. Minkowski,et al.  Regional Development of the Brain in Early Life , 1968 .

[53]  M. Rugg,et al.  Event-related potentials and recognition memory , 2007, Trends in Cognitive Sciences.

[54]  Jonas Persson,et al.  Common prefrontal activations during working memory, episodic memory, and semantic memory , 2003, Neuropsychologia.

[55]  Philip A. Kragel,et al.  Regional brain differences in the effect of distraction during the delay interval of a working memory task , 2007, Brain Research.

[56]  Elinor McKone,et al.  Early maturity of face recognition: No childhood development of holistic processing, novel face encoding, or face-space , 2009, Cognition.

[57]  Alumit Ishai,et al.  Let’s face it: It’s a cortical network , 2008, NeuroImage.

[58]  O. Pascalis,et al.  Recognition of faces of different species: a developmental study between 5 and 8 years of age , 2001 .

[59]  B. Kolb,et al.  Developmental changes in the recognition and comprehension of facial expression: Implications for frontal lobe function , 1992, Brain and Cognition.

[60]  D. Thomson,et al.  Development of face recognition. , 1995, British journal of psychology.

[61]  Douglas O. Cheyne,et al.  Reconstruction of correlated brain activity with adaptive spatial filters in MEG , 2010, NeuroImage.

[62]  George Zouridakis,et al.  Lateralization of Cerebral Activation in Auditory Verbal and Non-Verbal Memory Tasks Using Magnetoencephalography , 2004, Brain Topography.

[63]  Elizabeth W. Pang,et al.  Face Processing in Children: Novel MEG Findings , 2010 .

[64]  Robin M. Chan,et al.  Age-related differences in brain activation during emotional face processing , 2003, Neurobiology of Aging.

[65]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.