Infant pain vs. pain with parental suppression: Immediate and enduring impact on brain, pain and affect

• Published in: PloS one 2023-11, Vol.18 (11), p.e0290871-e0290871
• Main Authors: Barr, Gordon A, Opendak, Maya, Perry, Rosemarie E, Sarro, Emma, Sullivan, Regina M
• Format: Article
• Language: English
• Subjects: Amygdala; Animals; Animals, Newborn; Babies; Behavior; Brain; Brain - physiology; Care and treatment; Caregivers; Carrageenan; Carrageenin; Comparative analysis; Emotional behavior; Female; G protein-coupled receptors; Gene expression; Genes; Hormones; Humans; Hyperalgesia; Hypothalamus; Infant; Infants; Intensive care; Juveniles; Long-term effects; Mothers; Neural networks; Odorants; Pain; Pain - metabolism; Pain management; Pain perception; Paraventricular nucleus; Periaqueductal gray area; Rats; Shock; Social Behavior; Tail shock
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0290871

In the short term, parental presence while a human infant is in pain buffers the immediate pain responses, although emerging evidence suggests repeated social buffering of pain may have untoward long-term effects. To explore the short- and long-term impacts of social buffering of pain, we first measured the infant rat pup's [postnatal day (PN) 8, or 12] response to mild tail shock with the mother present compared to shock alone or no shock. Shock with the mother reduced pain-related behavioral activation and USVs of pups at both ages and reduced Fos expression in the periaqueductal gray, hypothalamic paraventricular nucleus, and the amygdala at PN12 only. At PN12, shock with the mother compared to shock alone differentially regulated expression of several hundred genes related to G-protein-coupled receptors (GPCRs) and neural development, whereas PN8 pups showed a less robust and less coherent expression pattern. In a second set of experiments, pups were exposed to daily repeated Shock-mother pairings (or controls) at PN5-9 or PN10-14 (during and after pain sensitive period, respectively) and long-term outcome assessed in adults. Shock+mother pairing at PN5-9 reduced adult carrageenan-induced thermal hyperalgesia and reduced Fos expression, but PN10-14 pairings had minimal impact. The effect of infant treatment on adult affective behavior showed a complex treatment by age dependent effect. Adult social behavior was decreased following Shock+mother pairings at both PN5-9 and PN10-14, whereas shock alone had no effect. Adult fear responses to a predator odor were decreased only by PN10-14 treatment and the infant Shock alone and Shock+mother did not differ. Overall, integrating these results into our understanding of long-term programming by repeated infant pain experiences, the data suggest that pain experienced within a social context impacts infant neurobehavioral responses and initiates an altered developmental trajectory of pain and affect processing that diverges from experiencing pain alone.