Enduring disruption of reward and stress circuit activities by early-life adversity in male rats
Abstract In humans, early-life adversity (ELA) such as trauma, poverty, and chaotic environment is linked to increased risk of later-life emotional disorders including depression and substance abuse. These disorders involve underlying disruption of reward circuits and likely vary by sex. Accordingly...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Publishing Group
2022-06-01
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| Series: | Translational Psychiatry |
| Online Access: | https://doi.org/10.1038/s41398-022-01988-w |
| _version_ | 1818555010981560320 |
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| author | Sophia C. Levis Matthew T. Birnie Jessica L. Bolton Christina R. Perrone Johanna S. Montesinos Tallie Z. Baram Stephen V. Mahler |
| author_facet | Sophia C. Levis Matthew T. Birnie Jessica L. Bolton Christina R. Perrone Johanna S. Montesinos Tallie Z. Baram Stephen V. Mahler |
| author_sort | Sophia C. Levis |
| collection | DOAJ |
| description | Abstract In humans, early-life adversity (ELA) such as trauma, poverty, and chaotic environment is linked to increased risk of later-life emotional disorders including depression and substance abuse. These disorders involve underlying disruption of reward circuits and likely vary by sex. Accordingly, we previously found that ELA leads to anhedonia for natural rewards and cocaine in male rodents, whereas in females ELA instead increases vulnerability to addiction-like use of opioid drugs and palatable food. While these findings suggest that ELA-induced disruption of reward circuitry may differ between the sexes, the specific circuit nodes that are influenced by ELA in either sex remain poorly understood. Here, in adult male Sprague-Dawley rats, we ask how ELA impacts opioid addiction-relevant behaviors that we previously tested after ELA in females. We probe potential circuit mechanisms in males by assessing opioid-associated neuronal activation in stress and reward circuit nodes including nucleus accumbens (NAc), amygdala, medial prefrontal cortex (mPFC), and paraventricular thalamus. We find that ELA diminishes opioid-seeking behaviors in males, and alters heroin-induced activation of NAc, PFC, and amygdala, suggesting a potential circuit-based mechanism. These studies demonstrate that ELA leads to behavioral and neurobiological disruptions consistent with anhedonia in male rodents, unlike the increased opioid seeking we previously saw in females. Our findings, taken together with our prior work, suggest that men and women could face qualitatively different mental health consequences of ELA, which may be essential for individually tailoring future intervention strategies. |
| first_indexed | 2024-12-12T09:47:38Z |
| format | Article |
| id | doaj.art-7d5c93c12e2b45248d0c2fbc5210959f |
| institution | Directory Open Access Journal |
| issn | 2158-3188 |
| language | English |
| last_indexed | 2024-12-12T09:47:38Z |
| publishDate | 2022-06-01 |
| publisher | Nature Publishing Group |
| record_format | Article |
| series | Translational Psychiatry |
| spelling | doaj.art-7d5c93c12e2b45248d0c2fbc5210959f2022-12-22T00:28:21ZengNature Publishing GroupTranslational Psychiatry2158-31882022-06-0112111110.1038/s41398-022-01988-wEnduring disruption of reward and stress circuit activities by early-life adversity in male ratsSophia C. Levis0Matthew T. Birnie1Jessica L. Bolton2Christina R. Perrone3Johanna S. Montesinos4Tallie Z. Baram5Stephen V. Mahler6Department of Anatomy & Neurobiology, University of California IrvineDepartment of Anatomy & Neurobiology, University of California IrvineDepartment of Anatomy & Neurobiology, University of California IrvineDepartment of Neurobiology & Behavior, University of California IrvineDepartment of Neurobiology & Behavior, University of California IrvineDepartment of Anatomy & Neurobiology, University of California IrvineDepartment of Neurobiology & Behavior, University of California IrvineAbstract In humans, early-life adversity (ELA) such as trauma, poverty, and chaotic environment is linked to increased risk of later-life emotional disorders including depression and substance abuse. These disorders involve underlying disruption of reward circuits and likely vary by sex. Accordingly, we previously found that ELA leads to anhedonia for natural rewards and cocaine in male rodents, whereas in females ELA instead increases vulnerability to addiction-like use of opioid drugs and palatable food. While these findings suggest that ELA-induced disruption of reward circuitry may differ between the sexes, the specific circuit nodes that are influenced by ELA in either sex remain poorly understood. Here, in adult male Sprague-Dawley rats, we ask how ELA impacts opioid addiction-relevant behaviors that we previously tested after ELA in females. We probe potential circuit mechanisms in males by assessing opioid-associated neuronal activation in stress and reward circuit nodes including nucleus accumbens (NAc), amygdala, medial prefrontal cortex (mPFC), and paraventricular thalamus. We find that ELA diminishes opioid-seeking behaviors in males, and alters heroin-induced activation of NAc, PFC, and amygdala, suggesting a potential circuit-based mechanism. These studies demonstrate that ELA leads to behavioral and neurobiological disruptions consistent with anhedonia in male rodents, unlike the increased opioid seeking we previously saw in females. Our findings, taken together with our prior work, suggest that men and women could face qualitatively different mental health consequences of ELA, which may be essential for individually tailoring future intervention strategies.https://doi.org/10.1038/s41398-022-01988-w |
| spellingShingle | Sophia C. Levis Matthew T. Birnie Jessica L. Bolton Christina R. Perrone Johanna S. Montesinos Tallie Z. Baram Stephen V. Mahler Enduring disruption of reward and stress circuit activities by early-life adversity in male rats Translational Psychiatry |
| title | Enduring disruption of reward and stress circuit activities by early-life adversity in male rats |
| title_full | Enduring disruption of reward and stress circuit activities by early-life adversity in male rats |
| title_fullStr | Enduring disruption of reward and stress circuit activities by early-life adversity in male rats |
| title_full_unstemmed | Enduring disruption of reward and stress circuit activities by early-life adversity in male rats |
| title_short | Enduring disruption of reward and stress circuit activities by early-life adversity in male rats |
| title_sort | enduring disruption of reward and stress circuit activities by early life adversity in male rats |
| url | https://doi.org/10.1038/s41398-022-01988-w |
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