Abstract
Background
Animal and human studies implicate forebrain neural circuits in maternal behavior.
Here, we hypothesized that human brain response to emotional stimuli relevant for
social interactions between infants and adults are modulated by sex- and experience-dependent
factors.
Methods
We used functional magnetic resonance imaging and examined brain response to infant
crying and laughing in mothers and fathers of young children and in women and men
without children.
Results
Women but not men, independent of their parental status, showed neural deactivation
in the anterior cingulate cortex, as indexed by decreased blood oxygenation level–dependent
signal, in response to both infant crying and laughing. The response pattern changed
fundamentally with parental experience: in the amygdala and interconnected limbic
regions, parents (independent of sex) showed stronger activation from crying, whereas
nonparents showed stronger activation from laughing.
Conclusions
Our data show sex- and experience-dependent modulation of brain response to infant
vocalizations. Successful recognition and evaluation of infant vocalizations can be
critical for bonding mechanisms and for offspring well-being and survival. Thus, the
modulation of responses by experience seems to represent an adaptive mechanism that
can be related to reproductive fitness.
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 accessOne-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 PsychiatryAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Neural systems for recognizing emotion.Curr Opin Neurobiol. 2002; 12: 169-177
- Neural science.Cell. 2000; 100: S1-S55
- Sex differences in response to children's toys in nonhuman primates (Cercopithecus aethiops sabaeus).Evol Hum Behav. 2002; 23: 467-479
- Normal neuroanatomical variation in the human brain.Am J Phys Anthropol. 2002; 118: 341-358
- Deciding advantageously before knowing the advantageous strategy.Science. 1997; 275: 1293-1295
- Human temporal-lobe response to vocal sounds.Brain Res Cogn Brain Res. 2002; 13: 17-26
- Voice-selective areas in human auditory cortex.Nature. 2000; 403: 309-312
Bradley MM, Lang PJ (1999): International Affective Digitized Sounds (IADS): Stimuli, Instruction Manual and Affective Ratings. Technical Report B-2, Gainsville, FL: The Center for Research in Psychophysiology, University of Florida
- Recognition of Mother's voice evokes metabolic activation in the medial prefrontal cortex and lateral thalamus of Octodon degus pups.Neuroscience. 2001; 103: 861-864
- Cognitive and emotional influences in anterior cingulate cortex.Trends Cogn Sci. 2000; 4: 215-222
- Amygdala response to happy faces as a function of extraversion.Science. 2002; 296: 2191
- Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors.Proc Natl Acad Sci U S A. 2001; 98: 12736-12741
- Software tools for analysis and visualization of fMRI data.NMR Biomed. 1997; 10: 171-178
- Depression.Annu Rev Psychol. 2002; 53: 545-574
- Effects of blood estrogen level on cortical activation patterns during cognitive activation as measured by functional MRI.Neuroimage. 2001; 13: 425-432
- Prolactin and parental behaviour in a male New World primate.Nature. 1982; 299: 551-553
- Emotion, cognition, and behavior.Science. 2002; 298: 1191-1194
- Neuroimaging and neuropathological studies of depression.Curr Opin Neurobiol. 2001; 11: 240-249
- Brain habituation during repeated exposure to fearful and neutral faces.Brain Res Bull. 2003; 59: 387-392
- Statistical parametric maps in functional imaging—a general linear approach.Hum Brain Mapp. 1995; 2: 189-210
- Event-related fMRI.Neuroimage. 1998; 7: 30-40
- Understanding emotional prosody activates right hemisphere regions.Arch Neurol. 1996; 53: 665-670
- Adaptive significance of male parental care in a monogamous mammal.Proc R Soc Lond B Biol Sci. 2000; 267: 147-150
- Sex differences in temporo-limbic and frontal brain volumes of healthy adults.Cereb Cortex. 2002; 12: 998-1003
- Searching for a baseline.Nat Rev Neurosci. 2001; 2: 685-694
- Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans.J Comp Neurol. 2001; 441: 197-222
- Origin of negative blood oxygenation level-dependent fMRI signals.J Cereb Blood Flow Metab. 2002; 22: 908-917
- Serotonin transporter genetic variation and the response of the human amygdala.Science. 2002; 297: 400-403
- Subdivisions of auditory cortex and processing streams in primates.Proc Natl Acad Sci U S A. 2000; 97: 11793-11799
- Behavioral treatment and bio-behavioral assessment.in: Sidowski J.B. Johnson J.H. Williams T.A. Technology in Mental Health Care Delivery Systems. Ablex, Norwood, NJ1980: 119-137
- Emotion circuits in the brain.Annu Rev Neurosci. 2000; 23: 155-184
- Adult perception of emotion intensity in human infant cries.Child Dev. 1996; 67: 3238-3249
- Feasibility of using fMRI to study mothers responding to infant cries.Depress Anxiety. 1999; 10: 99-104
- A potential role for thalamocingulate circuitry in human maternal behavior.Biol Psychiatry. 2002; 51: 431-445
- Brain evolution relating to family, play, and the separation call.Arch Gen Psychiatry. 1985; 42: 405-417
- Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations.Annu Rev Neurosci. 2001; 24: 1161-1192
- Functional MRI of the human amygdala?.Neuroimage. 2001; 14: 253-257
- Species-typical behavior of hamsters deprived from birth of the neocortex.Science. 1981; 213: 459-461
- Interhemispheric anatomical differences in human primary auditory cortex.Cereb Cortex. 1996; 6: 661-672
- Anatomical variability of the anterior cingulate gyrus and basic dimensions of human personality.Neuroimage. 2002; 15: 847-855
- Dynamic behavior of the auditory N100 elicited by a baby's cry.Int J Psychophysiol. 2001; 41: 271-278
- Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala.Neuron. 1997; 19: 613-624
- Topographical variation of the human primary cortices.Cereb Cortex. 1993; 3: 313-329
- Mechanisms and streams for processing of “what” and “where” in auditory cortex.Proc Natl Acad Sci U S A. 2000; 97: 11800-11806
- Hormonal changes in males of a naturally biparental and a uniparental mammal.Horm Behav. 1999; 35: 163-176
- Cytochrome oxidase, acetylcholinesterase, and NADPH-diaphorase staining in human supratem-poral and insular cortex.Neuroimage. 1997; 6: 288-304
- Audition of laughing and crying leads to right amygdala activation in a low-noise fMRI setting.Brain Res Brain Res Protoc. 2003; 11: 81-91
- Auditory perception of laughing and crying activates human amygdala regardless of attentional state.Brain Res Cogn Brain Res. 2001; 12: 181-198
- Spatiotemporal pattern of neural processing in the human auditory cortex.Science. 2002; 297: 1706-1708
- Sex differences in the functional organization of the brain for language.Nature. 1995; 373: 607-609
- Estrogen, progesterone, and pregnancy termination alter neural activity in brain regions that control maternal behavior in rats.Neuroendocrinology. 2002; 75: 12-23
- Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain.Neuron. 2002; 36: 1195-1210
- Wired for reproduction.Annu Rev Neurosci. 2002; 25: 507-536
- Emotion-induced changes in human medial prefrontal cortex.Proc Natl Acad Sci U S A. 2001; 98: 688-693
- Hormonal correlates of paternal responsiveness in new and expectant fathers.Evol Hum Behav. 2000; 21: 79-95
- Functional specialization in rhesus monkey auditory cortex.Science. 2001; 292: 290-293
- Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen.Proc R Soc Lond B Biol Sci. 2002; 269: 823-829
- The regulation of infanticide and parental behavior.Science. 1982; 215: 1270-1272
- The negative BOLD signal unmasked.Neuron. 2002; 36: 993-995
- Histochemical identification of cortical areas in the auditory region of the human brain.Exp Brain Res. 2002; 143: 499-508
Ward BD (2000): Simultaneous inference for fMRI data. Available at: http://afni.nimh.nih.gov/afni/docpdf/AlphaSim.pdf. Accessed September 3, 2003
- Fear, vigilance and ambiguity.Curr Dir Psychol Sci. 1998; 7: 177-188
- A functional MRI study of human amygdala responses to facial expressions of fear vs. anger.Emotion. 2001; 1: 70-83
- A general statistical analysis for fMRI data.Neuroimage. 2002; 15: 1-15
- A unified statistical approach for determining significant signals in images of cerebral activation.Hum Brain Mapp. 1996; 4: 58-73
- Hormonal changes in mammalian fathers.Horm Behav. 2001; 40: 139-145
- The human amygdala and the emotional evaluation of sensory stimuli.Brain Res Brain Res Rev. 2003; 41: 88-123
Article info
Publication history
Accepted:
June 19,
2003
Received in revised form:
June 19,
2003
Received:
April 16,
2003
Identification
Copyright
© 2003 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
