The human parental brain: In vivo neuroimaging

doi:10.1016/j.pnpbp.2010.10.017

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volume 35, Issue 5, 1 July 2011, Pages 1242-1254

https://doi.org/10.1016/j.pnpbp.2010.10.017 Get rights and content

Abstract

Interacting parenting thoughts and behaviors, supported by key brain circuits, critically shape human infants' current and future behavior. Indeed, the parent–infant relationship provides infants with their first social environment, forming templates for what they can expect from others, how to interact with them and ultimately how they go on to themselves to be parents. This review concentrates on magnetic resonance imaging experiments of the human parent brain, which link brain physiology with parental thoughts and behaviors. After reviewing brain imaging techniques, certain social cognitive and affective concepts are reviewed, including empathy and trust—likely critical to parenting. Following that is a thorough study-by-study review of the state-of-the-art with respect to human neuroimaging studies of the parental brain—from parent brain responses to salient infant stimuli, including emotionally charged baby cries and brief visual stimuli to the latest structural brain studies. Taken together, this research suggests that networks of highly conserved hypothalamic–midbrain–limbic–paralimbic–cortical circuits act in concert to support parental brain responses to infants, including circuits for limbic emotion response and regulation. Thus, a model is presented in which infant stimuli activate sensory analysis brain regions, affect corticolimbic limbic circuits that regulate emotional response, motivation and reward related to their infant, ultimately organizing parenting impulses, thoughts and emotions into coordinated behaviors as a map for future studies. Finally, future directions towards integrated understanding of the brain basis of human parenting are outlined with profound implications for understanding and contributing to long term parent and infant mental health.

Research Highlights

► Review of brain imaging studies of human parent brains. ► Background of brain imaging and emotion regulation circuits. ► Includes structural plus functional magnetic resonance studies using baby picture and cries to stimulate human parent brains and correlate function with parenting thoughts, behaviors and hormones.

Section snippets

Brain imaging of human parent–infant relationships

Functional magnetic resonance imaging (fMRI) is a non-invasive technique that may be used to acquire data on the brain basis of human parental behavior and thoughts. Structural as well as functional data may be gathered by measuring the physical and blood–oxygen-dependant signals in response to infant auditory and visual stimuli. Thus, brain activity may be indirectly measured as changes in regional blood oxygenation. The differences between a region's oxygenated and deoxygenated hemoglobin,

Connecting the psychology and functional neuroanatomy of parenting

Brain imaging combined with behavioral paradigms over the last 10 years have made possible an increasingly sophisticated neurobiological understanding of affect and its regulation as well as empathy, and sociocultural cognitions such as inclusion/exclusion, trust and even attachment. In this section, I selectively review key studies in these fields.

Empathy, defined as appropriate perception, experience and response to another's emotion, is especially relevant to parenting in which infants' needs

Parental brains and baby cry stimuli

The first experiments using the pioneering approach of studying brain activity in mothers while they listen to infant cries were conducted by Lorberbaum and colleagues. Building on the thalamocingulate theory of maternal behavior in animals (MacLean, 1990), they initially predicted that baby cries would selectively activate cingulate and thalamus in mothers (ranging from 3 weeks to 3.5 years postpartum) exposed to an audio taped 30 s standard baby cry, not from their own infant (Lorberbaum et al.,

Parental brains and baby visual stimuli

Several groups are also using baby visual stimuli to activate parental brain circuits (Bartels and Zeki,2004b, Leibenluft et al.,2004, Nitschke et al.,2004, Noriuchi et al.,2008, Ranote et al.,2004, Strathearn et al.,2009, Strathearn et al.,2008, Strathearn et al.,2005, Swain et al.,2003, Swain et al.,2004b, Swain et al., 2006) with a variety of designs, parent populations and infant age—and again highlighting drive/motivation brain regions responding in concert with cortical regulation regions.

Parental brain structure

In a pioneering neuroimaging studies of parents, extended to include the dimension of brain structure as well as function, Kim and colleagues have begun to look at brain densities using voxel-based morphometry (Kim et al.,2010a, Kim et al.,2010b). First, this study attempts to address the effects of early-life events on later parenting, as elaborated in rodent and non-human primate models (Champagne,2010, Kaffman and Meaney,2007, Veenema, 2009), brain structure as well as functional responses

Special parent populations, specific behaviors

In addition to understanding normal human parenting in order to optimize health outcomes, research on parents with health risks from substance abuse and mood disorders to different conditions of birth and infant feeding are needed to improve the recognition and treatment of compromised parenting circumstances. Indeed, recently published follow-up data on the offspring of depressed and anxious mothers who have increased mental health risks (Brown et al.,1987, Heim et al.,1997, Kendler et al.,1993

Summary and model

Functional MRI experiments on parenting using baby stimuli are now making meaningful and complementary contributions to our understanding of the parental brain. The human parental brain is the concept of a discrete set of interacting brain circuits that serve as substrate for the human transition to parenting, integrate baby as well as internal information, and support key thoughts and behaviors for us to identify and react to baby stimuli. In support of this model, virtually all of the

Future directions

Future studies will add integrated and increasingly ethologically valid baby stimuli such as movies and perhaps even different sensory systems, such as the olfactory system, as well as more measures of parent responses to expand and refine our understanding of the parental brain. These approached will require careful consideration and study of how these patterns of brain activation may differ between attachment groups or across mental health measures. Do mothers with insecure patterns of

Acknowledgements

The authors would like to acknowledge the generous support of colleagues, research assistants and research participants at our respective institutions: JES was supported by grants from the Institute for Research on Unlimited Love (unlimitedloveinstitute.org), the National Alliance for Research on Schizophrenia and Depression (narsad.org), the Klingenstein Third Generation Foundation, Yale Center for Risk, Resilience and Recovery, Associates of the Yale Child Study Center and the Department of

Glossary for Tables 1 and 2

Activations and deactivations: measured by functional magnetic resonance imaging, satisfied significance criteria of random effects analysis at p < 0.05 or fixed effects analysis at p < 0.001at a minimum
T: Tesla (unit of magnetic field strength)
Blocks: periods of stimulus exposure and fMRI data acquisition
Events: brief exposures to infant stimuli during fMRI experiments
other cry: cry of an unfamiliar baby
own cry: cry of the subject's own baby
MPOA: medial preoptic area
BNST: bed nucleus of the stria terminalis
DLPFC

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Citation Excerpt :
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View full text

The human parental brain: In vivo neuroimaging

Abstract

Research Highlights

Section snippets

Brain imaging of human parent–infant relationships

Connecting the psychology and functional neuroanatomy of parenting

Parental brains and baby cry stimuli

Parental brains and baby visual stimuli

Parental brain structure

Special parent populations, specific behaviors

Summary and model

Future directions

Acknowledgements

Glossary for Tables 1 and 2

Neuroimage

Neuroimage

Physiol Behav

Psychiatry Res

Int J Psychophysiol

Brain Res

Psychoneuroendocrinology

Horm Behav.

J Am Acad Child Adolesc Psychiatry

Horm Behav

Trends Cogn Sci

Biol Psychiatry

Curr Opin Neurobiol

Curr Opin Neurobiol

Curr Opin Neurobiol

Prog Neurobiol

Biol Psychiatry

Biol Psychiatry

Neuron

Clin Neurosci Res

Metabolism

Neuroimage

Biol Psychiatry

Prog Neuropsychopharmacol Biol Psychiatry

Int J Psychophysiol

Front Neuroendocrinol

Neuroimage

Brain Res Brain Res Protoc

Curr Opin Neurobiol

Brain Res

Int JDev Neurosci

Biol Psychiatry

Am J Obstet Gynecol

Reward, motivation, and emotion systems associated with early-stage intense romantic love

J Neurophysiol

The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences

J AutismDevDisord

Quality of early parental care reported by mothers is related to anterior cingulate response to own infant stimuli: preliminary findings

Neuroimage

The neural basis of romantic love

NeuroReport

Functional brain mapping during free viewing of natural scenes

Hum Brain Mapp

Acute stroke effects on emotions: an interpretation through the mirror system

Curr Opin Neurol

Neural correlates of social and nonsocial emotions: an fMRI study

Neuroimage

Life events, vulnerability and onset of depression: some refinements

Br J Psychiatry

Measuring attachment representation in an fMRI environment: a pilot study

Psychopathology

Maternal depression and the emotional development of the child

Br J Psychiatry

Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas

Proc Natl Acad Sci USA

Enhancing attachment security in the infants of women in a jail-diversion program

Attach HumDev

Epigenetic influence of social experiences across the lifespan

Dev Psychobiol

Social exclusion in middle childhood: Rejection events, slow-wave neural activity, and ostracism distress

Soc Neurosci

Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders

Nat Neurosci

Neuroplasticity: changes in grey matter induced by training

Nature

Temporal and spatial dynamics of brain structure changes during extensive learning