Regional Brain Responses in Nulliparous Women to Emotional Infant Stimuli

Infant cries and facial expressions influence social interactions and elicit caretaking behaviors from adults. Recent neuroimaging studies suggest that neural responses to infant stimuli involve brain regions that process rewards. However, these studies have yet to investigate individual differences in tendencies to engage or withdraw from motivationally relevant stimuli. To investigate this, we used event-related fMRI to scan 17 nulliparous women. Participants were presented with novel infant cries of two distress levels (low and high) and unknown infant faces of varying affect (happy, sad, and neutral) in a randomized, counter-balanced order. Brain activation was subsequently correlated with scores on the Behavioral Inhibition System/Behavioral Activation System scale. Infant cries activated bilateral superior and middle temporal gyri (STG and MTG) and precentral and postcentral gyri. Activation was greater in bilateral temporal cortices for low- relative to high-distress cries. Happy relative to neutral faces activated the ventral striatum, caudate, ventromedial prefrontal, and orbitofrontal cortices. Sad versus neutral faces activated the precuneus, cuneus, and posterior cingulate cortex, and behavioral activation drive correlated with occipital cortical activations in this contrast. Behavioral inhibition correlated with activation in the right STG for high- and low-distress cries relative to pink noise. Behavioral drive correlated inversely with putamen, caudate, and thalamic activations for the comparison of high-distress cries to pink noise. Reward-responsiveness correlated with activation in the left precentral gyrus during the perception of low-distress cries relative to pink noise. Our findings indicate that infant cry stimuli elicit activations in areas implicated in auditory processing and social cognition. Happy infant faces may be encoded as rewarding, whereas sad faces activate regions associated with empathic processing. Differences in motivational tendencies may modulate neural responses to infant cues.

[1]  Henrik Walter,et al.  Genetic variation in CYP2D6 impacts neural activation during cognitive tasks in humans , 2012, NeuroImage.

[2]  E. Stice,et al.  Reward abnormalities among women with full and subthreshold bulimia nervosa: a functional magnetic resonance imaging study. , 2011, The International journal of eating disorders.

[3]  Jessica L. Montoya,et al.  Maternal Neural Responses to Infant Cries and Faces: Relationships with Substance Use , 2011, Frontiers in Psychiatry.

[4]  S. Taylor,et al.  Social appraisal in chronic psychosis: role of medial frontal and occipital networks. , 2011, Journal of psychiatric research.

[5]  Kristin Prehn,et al.  Neuronal Correlates of Cognitive Reappraisal in Borderline Patients with Affective Instability , 2011, Biological Psychiatry.

[6]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[7]  J. Weber,et al.  Prefrontal–striatal pathway underlies cognitive regulation of craving , 2010, Proceedings of the National Academy of Sciences.

[8]  K. Lorenz,et al.  Die angeborenen Formen möglicher Erfahrung. , 2010 .

[9]  G. Pearlson,et al.  Investigating the behavioral and self-report constructs of impulsivity domains using principal component analysis , 2009, Behavioural pharmacology.

[10]  Kaarin J Anstey,et al.  Hippocampal volume is positively associated with behavioural inhibition (BIS) in a large community-based sample of mid-life adults: the PATH through life study. , 2008, Social cognitive and affective neuroscience.

[11]  Peter Fonagy,et al.  What's in a Smile? Maternal Brain Responses to Infant Facial Cues , 2008, Pediatrics.

[12]  R. Dolan,et al.  Learning affective values for faces is expressed in amygdala and fusiform gyrus. , 2008, Social cognitive and affective neuroscience.

[13]  Y. Kikuchi,et al.  The Functional Neuroanatomy of Maternal Love: Mother’s Response to Infant’s Attachment Behaviors , 2008, Biological Psychiatry.

[14]  Samet Kose,et al.  Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[15]  Martin P. Paulus,et al.  Time and decision making: differential contribution of the posterior insular cortex and the striatum during a delay discounting task , 2007, Experimental Brain Research.

[16]  M. Iacoboni,et al.  The mirror neuron system and the consequences of its dysfunction , 2006, Nature Reviews Neuroscience.

[17]  R. Saxe.  Uniquely human social cognition , 2006, Current Opinion in Neurobiology.

[18]  J. Decety,et al.  The power of simulation: Imagining one's own and other's behavior , 2006, Brain Research.

[19]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

[20]  Gilles Pourtois,et al.  Emotion and attention interactions in social cognition: Brain regions involved in processing anger prosody , 2005, NeuroImage.

[21]  Henning Scheich,et al.  Left Auditory Cortex and Amygdala, but Right Insula Dominance for Human Laughing and Crying , 2005, Journal of Cognitive Neuroscience.

[22]  Conny F. Schmidt,et al.  Face perception is mediated by a distributed cortical network , 2005, Brain Research Bulletin.

[23]  P. Skudlarski,et al.  Neural activity associated with stress-induced cocaine craving: a functional magnetic resonance imaging study , 2005, Psychopharmacology.

[24]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[25]  Matthew C. Keller,et al.  Increased sensitivity in neuroimaging analyses using robust regression , 2005, NeuroImage.

[26]  K. Scherer,et al.  The voices of wrath: brain responses to angry prosody in meaningless speech , 2005, Nature Neuroscience.

[27]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[28]  J. O'Doherty,et al.  Reward representations and reward-related learning in the human brain: insights from neuroimaging , 2004, Current Opinion in Neurobiology.

[29]  John Suckling,et al.  Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study. , 2004, Archives of general psychiatry.

[30]  E. Leibenluft,et al.  Mothers' neural activation in response to pictures of their children and other children , 2004, Biological Psychiatry.

[31]  J. Deakin,et al.  The neural basis of maternal responsiveness to infants: an fMRI study , 2004, Neuroreport.

[32]  J. Leckman,et al.  The development of parent-infant attachment through dynamic and interactive signaling loops of care and cry , 2004, Behavioral and Brain Sciences.

[33]  Andreas Bartels,et al.  The neural correlates of maternal and romantic love , 2004, NeuroImage.

[34]  Eric E. Nelson,et al.  Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants , 2004, NeuroImage.

[35]  D. Perrett,et al.  Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness , 2003, Neuropsychologia.

[36]  Erich Seifritz,et al.  Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents , 2003, Biological Psychiatry.

[37]  S. Haber.  The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[38]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

[39]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  E T Rolls,et al.  Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. , 2003, Cerebral cortex.

[41]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[42]  R. Elliott,et al.  Differential Response Patterns in the Striatum and Orbitofrontal Cortex to Financial Reward in Humans: A Parametric Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

[43]  M. Buonocore,et al.  Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task , 2003, Human brain mapping.

[44]  Dietrich Lehmann,et al.  Affective Judgments of Faces Modulate Early Activity (∼160 ms) within the Fusiform Gyri , 2002, NeuroImage.

[45]  Mark S. George,et al.  A potential role for thalamocingulate circuitry in human maternal behavior , 2002, Biological Psychiatry.

[46]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[47]  I. Wilkinson,et al.  Investigating the functional anatomy of empathy and forgiveness , 2001, Neuroreport.

[48]  Brian Knutson,et al.  Parametric FMRI confirms selective recruitment of nucleus accumbens during anticipation of monetary reward , 2001, NeuroImage.

[49]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[50]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[51]  W. Schultz.  Multiple reward signals in the brain , 2000, Nature Reviews Neuroscience.

[52]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[53]  E. Rolls.  The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[54]  E. Rolls,et al.  The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. , 1999, Neuroreport.

[55]  R. Lane,et al.  Neural Correlates of Levels of Emotional Awareness: Evidence of an Interaction between Emotion and Attention in the Anterior Cingulate Cortex , 1998, Journal of Cognitive Neuroscience.

[56]  J. Lorberbaum,et al.  Feasibility Of Using fMRI To Study Mothers Responding To Infant Cries , 1998, NeuroImage.

[57]  C. Carver,et al.  Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales , 1994 .

[58]  R. C. Fraley,et al.  Attachment and Loss , 2018 .

[59]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[60]  G. Gustafson,et al.  Individual recognition of human infants on the basis of cries alone. , 1983, Developmental psychobiology.

[61]  E. Azmitia.  The neuropsychology of anxiety: an enquiry into the functions of the Septo-Hippocampal system, Gray J.A.. Oxford University Press, New York (1981), pp. 523.,£27.50 , 1983 .

[62]  J. Gray,et al.  Précis of The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system , 1982, Behavioral and Brain Sciences.

[63]  R. Voss,et al.  ‘1/fnoise’ in music and speech , 1975, Nature.

[64]  J. Bowlby,et al.  Attachment and Loss, Volume I: Attachment , 1970 .

[65]  U. Habel,et al.  Neuronal Correlates of Facial Emotion Discrimination in Early Onset Schizophrenia , 2009, Neuropsychopharmacology.

[66]  Dietrich Lehmann,et al.  Affective judgments of faces modulate early activity (approximately 160 ms) within the fusiform gyri. , 2002, NeuroImage.

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

[68]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.