Advertisement
Research Article| Volume 56, ISSUE 4, P225-232, August 15, 2004

Download started.

Ok

Mothers' neural activation in response to pictures of their children and other children

      Background

      Considerable literature has focused on neural responses evoked by face viewing. We extend that literature and explore the neural correlates of maternal attachment with an fMRI study in which mothers view photographs of their own children.

      Method

      Seven mothers performed a one-back repetition detection task while viewing photographs of their own child, friends of their child, unfamiliar children, and unfamiliar adults.

      Results

      Viewing one's own child versus a familiar child was associated with activation in the amygdala, insula, anterior paracingulate cortex, and posterior superior temporal sulcus (STS). Viewing familiar versus unfamiliar children elicited increased activation in regions associated with familiarity in adults. Viewing unfamiliar children versus unfamiliar adults was associated with activation in the fusiform gyrus, intraparietal sulcus, precuneus, and posterior STS.

      Conclusions

      The sight of one's own child versus that of a familiar child activates regions that mediate emotional responses (amygdala, insula) and are associated with theory of mind functions (anterior paracingulate cortex, posterior superior temporal sulcus). These activations may reflect the intense attachment, vigilant protectiveness, and empathy that characterize normal maternal attachment. The sight of an unfamiliar child's face compared with that of an unfamiliar adult engages areas associated with attention as well as face perception.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bargh J.A.
        • Chen M.
        • Burrows L.
        Automaticity of social behavior.
        J Pers Soc Psychol. 1996; 71: 230-244
        • Bartels A.
        • Zeki S.
        The neural basis of romantic love.
        Neuroreport. 2000; 11: 3829-3834
        • Bradley M.M.
        • Lang P.J.
        Measuring emotion.
        J Behav Ther Exp Psychiatry. 1994; 25: 49-59
        • Breiter H.C.
        • Etcoff N.L.
        • Whalen P.J.
        • Kennedy W.A.
        • Rauch S.L.
        • Buckner R.L
        • et al.
        Response and habituation of the human amygdala during visual processing of facial expression.
        Neuron. 1996; 17: 875-887
        • Calder A.J.
        • Lawrence A.D.
        • Young A.W.
        Neuropsychology of fear and loathing.
        Nat Rev Neurosci. 2001; 2: 352-363
        • Canli T.
        • Sivers H.
        • Whitfield S.L.
        • Gotlib I.H.
        • Gabrieli J.D.
        Amygdala response to happy faces as a function of extraversion.
        Science. 2002; 296: 2191
        • Carr L.
        • Iacoboni M.
        • Dubeau M.C.
        • Mazziotta J.C.
        • Lenzi G.L.
        Neural mechanisms of empathy in humans.
        Proc Natl Acad Sci U S A. 2003; 100: 5497-5502
        • Castelli F.
        • Happe F.
        • Frith U.
        • Frith C.
        Movement and mind.
        Neuroimage. 2000; 12: 314-325
        • Critchley H.D.
        • Melmed R.N.
        • Featherstone E.
        • Mathias C.J.
        • Dolan R.J.
        Volitional control of autonomic arousal.
        Neuroimage. 2002; 16: 909-919
        • Davis M.
        • Whalen P.J.
        The amygdala.
        Mol Psychiatry. 2001; 1: 13-34
        • Farrow T.F.
        • Zheng Y.
        • Wilkinson I.D.
        • Spence S.A.
        • Deakin J.F.
        • Tarrier N
        • et al.
        Investigating the functional anatomy of empathy and forgiveness.
        Neuroreport. 2001; 12: 2433-2438
        • Ferstl E.C.
        • von Cramon D.Y.
        What does the frontomedial cortex contribute to language processing.
        Neuroimage. 2002; 17: 1599-1612
        • Fleming A.S.
        • Steiner M.
        • Corter C.
        Cortisol, hedonics, and maternal responsiveness in human mothers.
        Horm Behav. 1997; 32: 85-98
        • Fletcher P.C.
        • Frith C.D.
        • Baker S.C.
        • Shallice T.
        • Frackowiak R.S.
        • Dolan R.J.
        The mind's eye-precuneus activation in memory-related imagery.
        Neuroimage. 1995; 2: 195-200
        • Frith C.D.
        • Frith U.
        Interacting minds—a biological basis.
        Science. 1999; 286: 1692-1695
        • Gallagher H.L.
        • Frith C.D.
        Functional imaging of “theory of mind”.
        Trends Cogn Sci. 2003; 7: 77-83
        • Gallagher H.L.
        • Happe F.
        • Brunswick N.
        • Fletcher P.C.
        • Frith U.
        • Frith C.D.
        Reading the mind in cartoons and stories.
        Neuropsychologia. 2000; 38: 11-21
        • Gobbini M.I.
        • Leibenluft E.
        • Santiago N.
        • Haxby J.V.
        Social and emotional attachment in the neural representation of faces.
        Neuro Image. (in press);
        • Gorno-Tempini M.L.
        • Price C.J.
        • Josephs O.
        • Vandenberghe R.
        • Cappa S.F.
        • Kapur N
        • et al.
        The neural systems sustaining face and proper-name processing.
        Brain. 1998; 121: 2103-2118
        • Greenwald A.G.
        • Banaji M.R.
        Implicit social cognition.
        Psychol Rev. 1995; 102: 4-27
        • Gusnard D.A.
        • Raichle M.E.
        • Raichle M.E.
        Searching for a baseline.
        Nat Rev Neurosci. 2001; 2: 685-694
        • Hamann S.B.
        • Ely T.D.
        • Hoffman J.M.
        • Kilts C.
        Ecstasy and agony.
        Psychol Sci. 2002; 13: 135-141
        • Hamann S.
        • Mao H.
        Positive and negative emotional verbal stimuli elicit activity in the left amygdala.
        Neuroreport. 2002; 13: 15-19
        • Hart A.J.
        • Whalen P.J.
        • Shin L.M.
        • McInerney S.C.
        • Fischer H.
        • Rausch S.L.
        Differential response in the human amygdala to racial outgroup vs ingroup face stimuli.
        Neuroreport. 2000; 11: 2352-2355
        • Johnson S.C.
        • Baxter L.C.
        • Wilder L.S.
        • Pipe J.G.
        • Heiserman J.E.
        • Prigatano G.P.
        Neural correlates of self-reflection.
        Brain. 2002; 125: 1808-1814
        • Lane R.D.
        • Reiman E.M.
        • Ahern G.L.
        • Schwartz G.E.
        • Davidson R.J.
        Neuroanatomical correlates of happiness, sadness, and disgust.
        Am J Psychiatry. 1997; 154: 926-933
        • Leveroni C.L.
        • Seidenberg M.
        • Mayer A.R.
        • Mead L.A.
        • Binder J.R.
        • Rao S.M.
        Neural systems underlying the recognition of familiar and newly learned faces.
        J Neurosci. 2000; 20: 878-886
        • Liberzon I.
        • Phan K.L.
        • Decker L.R.
        • Taylor S.F.
        Extended amygdala and emotional salience.
        Neuropsychopharmacology. 2003; 28: 726-733
        • Lorberbaum J.P.
        • Newman J.D.
        • Horwitz A.R.
        • Dubno J.R.
        • Lydiard R.B.
        • Hamner M.B
        • et al.
        A potential role for thalamocingulate circuitry in human maternal behavior.
        Biol Psychiatry. 2002; 51: 431-445
        • Lorenz K.
        The concept of instinctive behavior.
        Folia Biotheoretica. 1937; 2: 17-50
        • Morris J.S.
        • Frith C.D.
        • Perrett D.I.
        • Rowland D.
        • Young A.W.
        • Calder A.J
        • et al.
        A differential neural response in the human amygdala to fearful and happy facial expressions.
        Nature. 1996; 383: 812-815
        • Nakamura K.
        • Kawashima R.
        • Sugiura M.
        • Kato T.
        • Nakamura A.
        • Hatano K
        • et al.
        Neural substrates for recognition of familiar voices.
        Neuropsychologia. 2001; 39: 1047-1054
        • Nelson E.E.
        • Panksepp J.
        Brain substrates of infant-mother attachment.
        Neurosci Biobehav Rev. 1998; 22: 437-452
        • Pedersen C.A.
        Oxytocin control of maternal behavior. Regulation by sex steroids and offspring stimuli.
        Ann N Y Acad Sci. 1997; 807: 126-145
        • Phelps E.A.
        • O'Connor K.J.
        • Cunningham W.A.
        • Funayama E.S.
        • Gatenby J.C.
        • Gore J.C.
        Performance on indirect measures of race evaluation predicts amygdala activation.
        J Cogn Neurosci. 2000; 12: 729-738
        • Phelps E.A.
        • O'Connor K.J.
        • Gatenby J.C.
        • Gore J.C.
        • Grillon C.
        • Davis M.
        Activation of the left amygdala to a cognitive representation of fear.
        Nat Neurosci. 2001; 4: 437-441
        • Phillips M.L.
        • Bullmore E.T.
        • Howard R.
        • Woodruff P.W.
        • Wright I.C.
        • Williams S.C
        • et al.
        Investigation of facial recognition memory and happy and sad facial expression perception.
        Psychiatry Res. 1998; 83: 127-138
        • Phillips M.L.
        • Drevets W.C.
        • Rauch S.L.
        • Lane R.
        Neurobiology of emotion perception I.
        Biol Psychiatry. 2003; 54: 504-514
        • Rossion B.
        • Schiltz C.
        • Robaye L.
        • Pirenne D.
        • Crommelinck M.
        How does the brain discriminate familiar and unfamiliar faces? A PET study of face categorical perception.
        J Cogn Neurosci. 2001; 13: 1019-1034
        • Sanfey A.G.
        • Rilling J.K.
        • Aronson J.A.
        • Nystrom L.E.
        • Cohen J.D.
        The neural basis of economic decision-making in the Ultimatum Game.
        Science. 2003; 300: 1755-1758
        • Schwartz C.E.
        • Wright C.I.
        • Shin L.M.
        • Kagan J.
        • Whalen P.J.
        • McMullin K.G.
        • Rauch S.L.
        Differential amygdala response to novel versus newly familiar neutral faces.
        Biol Psychiatry. 2003; 53: 854-862
        • Sergent J.
        • Ohta S.
        • MacDonald B.
        Functional neuroanatomy of face and object processing. A positron emission tomography study.
        Brain. 1992; 115: 15-36
        • Shah N.J.
        • Marshall J.C.
        • Zafiris O.
        • Schwab A.
        • Zilles K.
        • Markowitsch H.J.
        • Fink G.R.
        The neural correlates of person familiarity. A functional magnetic resonance imaging study with clinical implications.
        Brain. 2001; 124: 804-815
        • Sugiura M.
        • Kawashima R.
        • Nakamura K.
        • Sato N.
        • Nakamura A.
        • Kato T
        • et al.
        Activation reduction in anterior temporal cortices during repeated recognition of faces of personal acquaintances.
        Neuroimage. 2001; 13: 877-890
        • Talairach J.
        • Tournoux P.
        Co-Planar Stereotaxic Atlas of the Human Brain. 3-Dimensional Proportional System.
        Thieme Medical, New York1988
        • Todorov A.
        • Uleman J.S.
        Spontaneous trait inferences are bound to actors' faces.
        J Pers Soc Psychol. 2002; 83: 1051-1065
        • Williams J.B.
        • Gibbon M.
        • First M.B.
        • Spitzer R.L.
        • Davies M.
        • Borus J
        • et al.
        The Structured Clinical Interview for DSM-III-R (SCID). II. Multisite test–retest reliability.
        Arch Gen Psychiatry. 1992; 49: 630-636
        • Winston J.S.
        • Strange B.A.
        • O'Doherty J.
        • Dolan R.J.
        Automatic and intentional brain responses during evaluation of trustworthiness of faces.
        Nat Neurosci. 2002; 5: 277-283
        • Wright C.I.
        • Fischer H.
        • Whalen P.J.
        • McInerney S.C.
        • Rauch S.L.
        Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli.
        Neuroreport. 2001; 12: 379-383
        • Zalla T.
        • Koechlin E.
        • Pietrini P.
        • Basso G.
        • Aquino P.
        • Sirigu A
        • et al.
        Differential amygdala responses to winning and losing.
        Eur J Neurosci. 2000; 12: 1764-1770

      Linked Article

      • Erratum
        Biological PsychiatryVol. 56Issue 8
        • Preview
          The range for rating subjects using the Self-Assessment Manikin scale was presented incorrectly as 1–5 in Leibenluft et al “Mothers’ Neural Activation in Response to Pictures of Their Children and Other Children,” Biological Psychiatry 56:225–232. The error appears on page 226, under the Task heading within the Methods and Materials section, and on page 227, within the Table 1 legend. The correct rating scale for the question “How pleasant or unpleasant does this picture make you feel?” should be 1–9, with 1 being most positive, 5 neutral, and 9 negative.
        • Full-Text
        • PDF