Ready for action: a role for the human midbrain in responding to infant vocalizations

Infant vocalizations are among the most biologically salient sounds in the environment and can draw the listener to the infant rapidly in both times of distress and joy. A region of the midbrain, the periaqueductal gray (PAG), has long been implicated in the control of urgent, survival-related behaviours. To test for PAG involvement in the processing of infant vocalizations, we recorded local field potentials from macroelectrodes implanted in this region in four adults who had undergone deep brain stimulation. We found a significant difference occurring as early as 49 ms after hearing a sound in activity recorded from the PAG in response to infant vocalizations compared with constructed control sounds and adult and animal affective vocalizations. This difference was not present in recordings from thalamic electrodes implanted in three of the patients. Time frequency analyses revealed distinct patterns of activity in the PAG for infant vocalisations, constructed control sounds and adult and animal vocalisations. These results suggest that human infant vocalizations can be discriminated from other emotional or acoustically similar sounds early in the auditory pathway. We propose that this specific, rapid activity in response to infant vocalizations may reflect the initiation of a state of heightened alertness necessary to instigate protective caregiving.

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

[2]  H. Ralston,et al.  Monosynaptic projections from the lateral periaqueductal gray to the nucleus retroambiguus in the rhesus monkey: Implications for vocalization and reproductive behavior , 2000, The Journal of comparative neurology.

[3]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[4]  P. Roberts,et al.  Responses to social vocalizations in the inferior colliculus of the mustached bat are influenced by secondary tuning curves. , 2007, Journal of neurophysiology.

[5]  R. Blair,et al.  An alternative method for significance testing of waveform difference potentials. , 1993, Psychophysiology.

[6]  C. Schroeder,et al.  How Local Is the Local Field Potential? , 2011, Neuron.

[7]  Uwe Jürgens,et al.  Afferents of vocalization-controlling periaqueductal regions in the squirrel monkey , 2005, Brain Research.

[8]  Morten L Kringelbach,et al.  Minor structural abnormalities in the infant face disrupt neural processing: A unique window into early caregiving responses , 2013, Social neuroscience.

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

[10]  Josef Syka,et al.  Representation of species-specific vocalizations in the medial geniculate body of the guinea pig , 2007, Experimental Brain Research.

[11]  R. L. Burgess,et al.  Adult physiological response to infant cries: effects of temperament of infant, parental status, and gender. , 1982, Child development.

[12]  Marc N. Potenza,et al.  Regional Brain Responses in Nulliparous Women to Emotional Infant Stimuli , 2012, PloS one.

[13]  M. Bornstein,et al.  Sex differences in directional brain responses to infant hunger cries , 2013, Neuroreport.

[14]  T. Aziz,et al.  Deep Brain Stimulation for Chronic Pain. , 2022, Neurosurgery clinics of North America.

[15]  N. Kraus,et al.  Musical experience and neural efficiency – effects of training on subcortical processing of vocal expressions of emotion , 2009, The European journal of neuroscience.

[16]  Morten L Kringelbach,et al.  Listening to infant distress vocalizations enhances effortful motor performance , 2012, Acta paediatrica.

[17]  Leila Reddy,et al.  Local Field Potentials and Spikes in the Human Medial Temporal Lobe are Selective to Image Category , 2007, Journal of Cognitive Neuroscience.

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

[19]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R Todd Constable,et al.  Maternal brain response to own baby-cry is affected by cesarean section delivery. , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[21]  M. G. Terenzi,et al.  Disruption of maternal behaviour by acute conspecific interaction induces selective activation of the lateral periaqueductal grey , 2007, The European journal of neuroscience.

[22]  Alexander S. Ecker,et al.  Feature Selectivity of the Gamma-Band of the Local Field Potential in Primate Primary Visual Cortex , 2008, Front. Neurosci..

[23]  Josef Syka,et al.  Representation of species-specific vocalizations in the inferior colliculus of the guinea pig. , 2003, Journal of neurophysiology.

[24]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[25]  U. Jürgens,et al.  The role of the periaqueductal grey in vocal behaviour , 1994, Behavioural Brain Research.

[26]  Erno J. Hermans,et al.  Testosterone administration modulates neural responses to crying infants in young females , 2010, Psychoneuroendocrinology.

[27]  N. Canteras,et al.  A Role for the Periaqueductal Gray in Switching Adaptive Behavioral Responses , 2006, The Journal of Neuroscience.

[28]  C L Ludlow,et al.  Functional neuroanatomy of human vocalization: an H215O PET study. , 2005, Cerebral cortex.

[29]  A. Fleming,et al.  Testosterone and Prolactin Are Associated with Emotional Responses to Infant Cries in New Fathers , 2002, Hormones and Behavior.

[30]  B. Woodside,et al.  Maternity: neural mechanisms, motivational processes, and physiological adaptations. , 2010, Behavioral neuroscience.

[31]  J. Karhu,et al.  Effects of maternity on auditory event-related potentials to human sound , 2001, Neuroreport.

[32]  E. Halgren,et al.  Responses of Human Anterior Cingulate Cortex Microdomains to Error Detection, Conflict Monitoring, Stimulus-Response Mapping, Familiarity, and Orienting , 2005, The Journal of Neuroscience.

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

[34]  M. Kringelbach,et al.  The functional neuroanatomy of the evolving parent–infant relationship , 2010, Progress in Neurobiology.

[35]  S. O'leary,et al.  Affective and physiological factors predicting maternal response to infant crying. , 2009, Infant behavior & development.

[36]  P. S. Zeskind,et al.  Pitch of infant crying and caregiver responses in a natural setting , 1987 .

[37]  N. Canteras,et al.  Periaqueductal gray cholecystokinin infusions block morphine-induced disruption of maternal behavior , 2007, Peptides.

[38]  O. W. Henson,et al.  The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus , 1990, Brain Research Reviews.

[39]  M. Kringelbach,et al.  BRIEF REPORT Interpreting Infant Vocal Distress: The Ameliorative Effect of Musical Training in Depression , 2012 .

[40]  Joseph E LeDoux Rethinking the Emotional Brain , 2012, Neuron.

[41]  Heidemarie K. Laurent,et al.  A cry in the dark: depressed mothers show reduced neural activation to their own infant's cry. , 2012, Social cognitive and affective neuroscience.

[42]  R. Shapley,et al.  Spatial Spread of the Local Field Potential and its Laminar Variation in Visual Cortex , 2009, The Journal of Neuroscience.

[43]  Jed A. Meltzer,et al.  Effects of Working Memory Load on Oscillatory Power in Human Intracranial EEG , 2007, Cerebral cortex.

[44]  David H. Zald,et al.  The Neural Correlates of Aversive Auditory Stimulation , 2002, NeuroImage.

[45]  T. Poggio,et al.  Object Selectivity of Local Field Potentials and Spikes in the Macaque Inferior Temporal Cortex , 2006, Neuron.

[46]  M. T. Shipley,et al.  Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? , 1994, Trends in Neurosciences.

[47]  M. Craske,et al.  A Specific and Rapid Neural Signature for Parental Instinct , 2008, PloS one.

[48]  M. Bakermans-Kranenburg,et al.  Oxytocin decreases handgrip force in reaction to infant crying in females without harsh parenting experiences. , 2012, Social cognitive and affective neuroscience.

[49]  M. Bakermans-Kranenburg,et al.  Physiological reactivity to infant crying: a behavioral genetic study , 2010, Genes, brain, and behavior.

[50]  J. Stern,et al.  Role of the Midbrain Periaqueductal Gray in Maternal Nurturance and Aggression: c-fos and Electrolytic Lesion Studies in Lactating Rats , 1997, The Journal of Neuroscience.

[51]  A. Fleming,et al.  Effects of motherhood on physiological and subjective responses to infant cries in teenage mothers: A comparison with non-mothers and adult mothers , 2008, Hormones and Behavior.

[52]  Richard Bandler,et al.  Brain mechanisms of aggression as revealed by electrical and chemical stimulation: suggestion of a central role for the midbrain periaqueductal grey region , 1988 .

[53]  P. Roberts,et al.  Over-representation of species-specific vocalizations in the awake mouse inferior colliculus , 2009, Neuroscience.

[54]  M. Carandini,et al.  Stimulus contrast modulates functional connectivity in visual cortex , 2009, Nature Neuroscience.

[55]  P. Belin,et al.  Thinking the voice: neural correlates of voice perception , 2004, Trends in Cognitive Sciences.

[56]  Henning Scheich,et al.  FMRI activations of amygdala, cingulate cortex, and auditory cortex by infant laughing and crying , 2007, Human brain mapping.

[57]  M. Carandini,et al.  Local Origin of Field Potentials in Visual Cortex , 2009, Neuron.

[58]  David Borsook,et al.  Neuroimaging of the periaqueductal gray: State of the field , 2012, NeuroImage.