Nociceptive Cortical Activity Is Dissociated from Nociceptive Behavior in Newborn Human Infants under Stress

Laura Jones; Lorenzo Fabrizi; Maria Laudiano-Dray; Kimberley Whitehead; Judith Meek; Madeleine Verriotis; Maria Fitzgerald

doi:10.1016/j.cub.2017.10.063

Nociceptive Cortical Activity Is Dissociated from Nociceptive Behavior in Newborn Human Infants under Stress

Laura Jones, Lorenzo Fabrizi, Maria Laudiano-Dray, Kimberley Whitehead, Judith Meek, Madeleine Verriotis, Maria Fitzgerald

Digital Health & Applied Tech Assessment

Univ London, Birkbeck University London, University College London, University of London Royal Veterinary College, University of London, St Georges University London, Imperial College London, Kings College London, Royal Holloway University London, Queen Mary University London, Div Populat Hlth Sci & Educ
UCL Hospitals NHS Foundation Trust

Research output: Contribution to journal › Article › peer-review

53 Citations (Scopus)

Abstract

Newborn infants display strong nociceptive behavior in response to tissue damaging stimuli, and this is accompanied by nociceptive activity generated in subcortical and cortical areas of the brain [1, 2]. In the absence of verbal report, these nociceptive responses are used as measures of pain sensation in newborn humans, as they are in animals [3, 4]. However, many infants are raised in a physiologically stressful environment, and little is known about the effect of background levels of stress upon their pain responses. In adults, acute physiological stress causes hyperalgesia [5-7], and increased background stress increases pain [8-10], but these data cannot necessarily be extrapolated to infants. Here we have simultaneously measured nociceptive behavior, brain activity, and levels of physiological stress in a sample of 56 newborn human infants aged 36-42 weeks. Salivary cortisol (hypothalamic pituitary axis), heart rate variability (sympathetic adrenal medullary system), EEG event-related potentials (nociceptive cortical activity), and facial expression (behavior) were acquired in individual infants following a clinically required heel lance. We show that infants with higher levels of stress exhibit larger amplitude cortical nociceptive responses, but this is not reflected in their behavior. Furthermore, while nociceptive behavior and cortical activity are normally correlated, this relationship is disrupted in infants with high levels of physiological stress. Brain activity evoked by noxious stimulation is therefore enhanced by stress, but this cannot be deduced from observation of pain behavior. This may be important in the prevention of adverse effects of early repetitive pain on brain development.

Original language	English
Pages (from-to)	3846-3851.e3
Journal	Current biology : CB
Volume	27
Issue number	24
DOIs	https://doi.org/10.1016/j.cub.2017.10.063
Publication status	Published - 18 Dec 2017

Keywords

Brain/physiology
Electroencephalography
Evoked Potentials
Facial Expression
Female
Heart Rate
Humans
Hydrocortisone/metabolism
Infant, Newborn
Male
Nociception
Saliva/chemistry
Stress, Physiological

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10.1016/j.cub.2017.10.063

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title = "Nociceptive Cortical Activity Is Dissociated from Nociceptive Behavior in Newborn Human Infants under Stress",

abstract = "Newborn infants display strong nociceptive behavior in response to tissue damaging stimuli, and this is accompanied by nociceptive activity generated in subcortical and cortical areas of the brain [1, 2]. In the absence of verbal report, these nociceptive responses are used as measures of pain sensation in newborn humans, as they are in animals [3, 4]. However, many infants are raised in a physiologically stressful environment, and little is known about the effect of background levels of stress upon their pain responses. In adults, acute physiological stress causes hyperalgesia [5-7], and increased background stress increases pain [8-10], but these data cannot necessarily be extrapolated to infants. Here we have simultaneously measured nociceptive behavior, brain activity, and levels of physiological stress in a sample of 56 newborn human infants aged 36-42 weeks. Salivary cortisol (hypothalamic pituitary axis), heart rate variability (sympathetic adrenal medullary system), EEG event-related potentials (nociceptive cortical activity), and facial expression (behavior) were acquired in individual infants following a clinically required heel lance. We show that infants with higher levels of stress exhibit larger amplitude cortical nociceptive responses, but this is not reflected in their behavior. Furthermore, while nociceptive behavior and cortical activity are normally correlated, this relationship is disrupted in infants with high levels of physiological stress. Brain activity evoked by noxious stimulation is therefore enhanced by stress, but this cannot be deduced from observation of pain behavior. This may be important in the prevention of adverse effects of early repetitive pain on brain development.",

keywords = "Brain/physiology, Electroencephalography, Evoked Potentials, Facial Expression, Female, Heart Rate, Humans, Hydrocortisone/metabolism, Infant, Newborn, Male, Nociception, Saliva/chemistry, Stress, Physiological",

author = "Laura Jones and Lorenzo Fabrizi and Maria Laudiano-Dray and Kimberley Whitehead and Judith Meek and Madeleine Verriotis and Maria Fitzgerald",

year = "2017",

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doi = "10.1016/j.cub.2017.10.063",

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T1 - Nociceptive Cortical Activity Is Dissociated from Nociceptive Behavior in Newborn Human Infants under Stress

AU - Jones, Laura

AU - Fabrizi, Lorenzo

AU - Laudiano-Dray, Maria

AU - Whitehead, Kimberley

AU - Meek, Judith

AU - Verriotis, Madeleine

AU - Fitzgerald, Maria

PY - 2017/12/18

Y1 - 2017/12/18

N2 - Newborn infants display strong nociceptive behavior in response to tissue damaging stimuli, and this is accompanied by nociceptive activity generated in subcortical and cortical areas of the brain [1, 2]. In the absence of verbal report, these nociceptive responses are used as measures of pain sensation in newborn humans, as they are in animals [3, 4]. However, many infants are raised in a physiologically stressful environment, and little is known about the effect of background levels of stress upon their pain responses. In adults, acute physiological stress causes hyperalgesia [5-7], and increased background stress increases pain [8-10], but these data cannot necessarily be extrapolated to infants. Here we have simultaneously measured nociceptive behavior, brain activity, and levels of physiological stress in a sample of 56 newborn human infants aged 36-42 weeks. Salivary cortisol (hypothalamic pituitary axis), heart rate variability (sympathetic adrenal medullary system), EEG event-related potentials (nociceptive cortical activity), and facial expression (behavior) were acquired in individual infants following a clinically required heel lance. We show that infants with higher levels of stress exhibit larger amplitude cortical nociceptive responses, but this is not reflected in their behavior. Furthermore, while nociceptive behavior and cortical activity are normally correlated, this relationship is disrupted in infants with high levels of physiological stress. Brain activity evoked by noxious stimulation is therefore enhanced by stress, but this cannot be deduced from observation of pain behavior. This may be important in the prevention of adverse effects of early repetitive pain on brain development.

AB - Newborn infants display strong nociceptive behavior in response to tissue damaging stimuli, and this is accompanied by nociceptive activity generated in subcortical and cortical areas of the brain [1, 2]. In the absence of verbal report, these nociceptive responses are used as measures of pain sensation in newborn humans, as they are in animals [3, 4]. However, many infants are raised in a physiologically stressful environment, and little is known about the effect of background levels of stress upon their pain responses. In adults, acute physiological stress causes hyperalgesia [5-7], and increased background stress increases pain [8-10], but these data cannot necessarily be extrapolated to infants. Here we have simultaneously measured nociceptive behavior, brain activity, and levels of physiological stress in a sample of 56 newborn human infants aged 36-42 weeks. Salivary cortisol (hypothalamic pituitary axis), heart rate variability (sympathetic adrenal medullary system), EEG event-related potentials (nociceptive cortical activity), and facial expression (behavior) were acquired in individual infants following a clinically required heel lance. We show that infants with higher levels of stress exhibit larger amplitude cortical nociceptive responses, but this is not reflected in their behavior. Furthermore, while nociceptive behavior and cortical activity are normally correlated, this relationship is disrupted in infants with high levels of physiological stress. Brain activity evoked by noxious stimulation is therefore enhanced by stress, but this cannot be deduced from observation of pain behavior. This may be important in the prevention of adverse effects of early repetitive pain on brain development.

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KW - Electroencephalography

KW - Evoked Potentials

KW - Facial Expression

KW - Female

KW - Heart Rate

KW - Humans

KW - Hydrocortisone/metabolism

KW - Infant, Newborn

KW - Male

KW - Nociception

KW - Saliva/chemistry

KW - Stress, Physiological

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JO - Current biology : CB

JF - Current biology : CB

IS - 24

ER -

Nociceptive Cortical Activity Is Dissociated from Nociceptive Behavior in Newborn Human Infants under Stress

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Keywords

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