Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates
Early life adverse experiences, including childhood maltreatment, are major risk factors for psychopathology, including anxiety disorders with dysregulated fear responses. Consistent with human studies, maltreatment by the mother (MALT) leads to increased emotional reactivity in rhesus monkey infant...
Saved in:
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2025-01-01
|
| Series: | Developmental Cognitive Neuroscience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1878929324001415 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832591815619903488 |
|---|---|
| author | Elyse L. Morin Erin R. Siebert Brittany R. Howell Melinda Higgins Tanja Jovanovic Andrew M. Kazama Mar M. Sanchez |
| author_facet | Elyse L. Morin Erin R. Siebert Brittany R. Howell Melinda Higgins Tanja Jovanovic Andrew M. Kazama Mar M. Sanchez |
| author_sort | Elyse L. Morin |
| collection | DOAJ |
| description | Early life adverse experiences, including childhood maltreatment, are major risk factors for psychopathology, including anxiety disorders with dysregulated fear responses. Consistent with human studies, maltreatment by the mother (MALT) leads to increased emotional reactivity in rhesus monkey infants. Whether this persists and results in altered emotion regulation, due to enhanced fear learning or impaired utilization of safety signals as shown in human stress-related disorders, is unclear. Here we used a rhesus model of MALT to examine long-term effects on state anxiety and threat/safety learning in 25 adolescents, using a fear conditioning paradigm (AX+/BX-) with acoustic startle amplitude as the peripheral measure. The AX+/BX- paradigm measures baseline startle, fear-potentiated startle, threat/safety cue discrimination, startle attenuation by safety signals, and extinction. Baseline startle was higher in MALT animals, suggesting elevated state anxiety. No differences in threat learning, or threat/safety discrimination were detected. However, MALT animals showed generalized blunted responses to the conditioned threat cue, regardless of the safety cue presence in the transfer test, and took longer to extinguish spontaneously recovered threat. These findings suggest adverse caregiving experiences have long-term impacts on adolescent emotion regulation, including elevated state anxiety and blunted fear conditioning responses, consistent with reports in children with maltreatment exposure. |
| format | Article |
| id | doaj-art-018a79da1b834b91971048864bd777f5 |
| institution | Kabale University |
| issn | 1878-9293 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Developmental Cognitive Neuroscience |
| spelling | doaj-art-018a79da1b834b91971048864bd777f52025-01-22T05:41:15ZengElsevierDevelopmental Cognitive Neuroscience1878-92932025-01-0171101480Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primatesElyse L. Morin0Erin R. Siebert1Brittany R. Howell2Melinda Higgins3Tanja Jovanovic4Andrew M. Kazama5Mar M. Sanchez6Department of Psychiatry & Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, United States; Emory National Primate Research Center, Emory University, Atlanta, GA, United StatesEmory National Primate Research Center, Emory University, Atlanta, GA, United StatesDepartment of Psychiatry & Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, United States; Emory National Primate Research Center, Emory University, Atlanta, GA, United States; Fralin Biomedical Research Institute at VTC, Roanoke, VA, United States; Department of Human Development and Family Science, Virginia Tech, Blacksburg, VA, United StatesSchool of Nursing, Emory University, Atlanta, GA, United StatesDepartment of Psychiatry & Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, United StatesDepartment of Psychiatry & Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, United States; Emory National Primate Research Center, Emory University, Atlanta, GA, United StatesDepartment of Psychiatry & Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, United States; Emory National Primate Research Center, Emory University, Atlanta, GA, United States; Center for Translational Social Neuroscience, Emory University, Atlanta, GA, United States; Correspondence to: Department of Psychiatry and Behavioral Sciences, School of Medicine, Emory National Primate Research Center, Emory University, 954 Gatewood Rd NE, Atlanta, GA 30329, United States.Early life adverse experiences, including childhood maltreatment, are major risk factors for psychopathology, including anxiety disorders with dysregulated fear responses. Consistent with human studies, maltreatment by the mother (MALT) leads to increased emotional reactivity in rhesus monkey infants. Whether this persists and results in altered emotion regulation, due to enhanced fear learning or impaired utilization of safety signals as shown in human stress-related disorders, is unclear. Here we used a rhesus model of MALT to examine long-term effects on state anxiety and threat/safety learning in 25 adolescents, using a fear conditioning paradigm (AX+/BX-) with acoustic startle amplitude as the peripheral measure. The AX+/BX- paradigm measures baseline startle, fear-potentiated startle, threat/safety cue discrimination, startle attenuation by safety signals, and extinction. Baseline startle was higher in MALT animals, suggesting elevated state anxiety. No differences in threat learning, or threat/safety discrimination were detected. However, MALT animals showed generalized blunted responses to the conditioned threat cue, regardless of the safety cue presence in the transfer test, and took longer to extinguish spontaneously recovered threat. These findings suggest adverse caregiving experiences have long-term impacts on adolescent emotion regulation, including elevated state anxiety and blunted fear conditioning responses, consistent with reports in children with maltreatment exposure.http://www.sciencedirect.com/science/article/pii/S1878929324001415Early life adversityInfant maltreatmentFear-potentiated startleAnxietyNonhuman primate |
| spellingShingle | Elyse L. Morin Erin R. Siebert Brittany R. Howell Melinda Higgins Tanja Jovanovic Andrew M. Kazama Mar M. Sanchez Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates Developmental Cognitive Neuroscience Early life adversity Infant maltreatment Fear-potentiated startle Anxiety Nonhuman primate |
| title | Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates |
| title_full | Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates |
| title_fullStr | Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates |
| title_full_unstemmed | Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates |
| title_short | Effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates |
| title_sort | effects of early maternal care on anxiety and threat learning in adolescent nonhuman primates |
| topic | Early life adversity Infant maltreatment Fear-potentiated startle Anxiety Nonhuman primate |
| url | http://www.sciencedirect.com/science/article/pii/S1878929324001415 |
| work_keys_str_mv | AT elyselmorin effectsofearlymaternalcareonanxietyandthreatlearninginadolescentnonhumanprimates AT erinrsiebert effectsofearlymaternalcareonanxietyandthreatlearninginadolescentnonhumanprimates AT brittanyrhowell effectsofearlymaternalcareonanxietyandthreatlearninginadolescentnonhumanprimates AT melindahiggins effectsofearlymaternalcareonanxietyandthreatlearninginadolescentnonhumanprimates AT tanjajovanovic effectsofearlymaternalcareonanxietyandthreatlearninginadolescentnonhumanprimates AT andrewmkazama effectsofearlymaternalcareonanxietyandthreatlearninginadolescentnonhumanprimates AT marmsanchez effectsofearlymaternalcareonanxietyandthreatlearninginadolescentnonhumanprimates |