Adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal nets
Adolescence marks a sensitive period for neurodevelopment wherein exposure to drugs of abuse may disrupt maturation and induce persistent changes in neurophysiology which may exacerbate the risk for developing substance use disorders in adulthood. Adolescent nicotine exposure (ANE) enhances motivati...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-06-01
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| Series: | Addiction Neuroscience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2772392524000099 |
| _version_ | 1797303875273752576 |
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| author | S.C. Honeycutt A. Mukherjee M.S. Paladino E.A. Gilles-Thomas G.C. Loney |
| author_facet | S.C. Honeycutt A. Mukherjee M.S. Paladino E.A. Gilles-Thomas G.C. Loney |
| author_sort | S.C. Honeycutt |
| collection | DOAJ |
| description | Adolescence marks a sensitive period for neurodevelopment wherein exposure to drugs of abuse may disrupt maturation and induce persistent changes in neurophysiology which may exacerbate the risk for developing substance use disorders in adulthood. Adolescent nicotine exposure (ANE) enhances motivation to obtain drugs of abuse, particularly opioids, and increases vulnerability for the development of opioid use disorder (OUD). Here, we characterized ANE effects on learning about the adverse consequences of opioid consumption in adulthood in the absence of further nicotine administration. First, we show that ANE engenders punishment resistant fentanyl self-administration in a heterogenous seeking–taking chain schedule of reinforcement at least at the tested dose of fentanyl (0.75 µg/kg). We found that ANE rats consumed significantly more fentanyl and contingent foot shock punishment was less efficacious in limiting fentanyl seeking in ANE rats, relative to nicotine-naïve controls. Next, we demonstrated that ANE limits learning about the deleterious consequences of acute opioid intoxication in adulthood. In a combined conditioned taste avoidance and place preference paradigm we found that ANE resulted in significant reductions in the strength of morphine-induced CTA, and a simultaneous enhancement of CPP at a higher dose that was less capable of driving reinforcement in naïve controls. Finally, we examined the expression of perineuronal nets (PNNs) within insular cortex (IC) and found ANE rats to have increased density of PNNs across the anterior IC and significantly more parvalbumin-labeled IC cells relative to naïve controls. Together, these data lay the framework for a mechanistic explanation of the extreme comorbidity between nicotine use and development of OUDs. |
| first_indexed | 2024-03-07T23:59:55Z |
| format | Article |
| id | doaj.art-91b134c86d8e4ce899a35405c832c632 |
| institution | Directory Open Access Journal |
| issn | 2772-3925 |
| language | English |
| last_indexed | 2024-03-07T23:59:55Z |
| publishDate | 2024-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Addiction Neuroscience |
| spelling | doaj.art-91b134c86d8e4ce899a35405c832c6322024-02-18T04:44:44ZengElsevierAddiction Neuroscience2772-39252024-06-0111100150Adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal netsS.C. Honeycutt0A. Mukherjee1M.S. Paladino2E.A. Gilles-Thomas3G.C. Loney4204 Park Hall, Buffalo, New York 14260204 Park Hall, Buffalo, New York 14260204 Park Hall, Buffalo, New York 14260204 Park Hall, Buffalo, New York 14260Correspondence: Gregory C Loney, 204 Park Hall, Buffalo, New York 14260, 716-645-0241; 204 Park Hall, Buffalo, New York 14260Adolescence marks a sensitive period for neurodevelopment wherein exposure to drugs of abuse may disrupt maturation and induce persistent changes in neurophysiology which may exacerbate the risk for developing substance use disorders in adulthood. Adolescent nicotine exposure (ANE) enhances motivation to obtain drugs of abuse, particularly opioids, and increases vulnerability for the development of opioid use disorder (OUD). Here, we characterized ANE effects on learning about the adverse consequences of opioid consumption in adulthood in the absence of further nicotine administration. First, we show that ANE engenders punishment resistant fentanyl self-administration in a heterogenous seeking–taking chain schedule of reinforcement at least at the tested dose of fentanyl (0.75 µg/kg). We found that ANE rats consumed significantly more fentanyl and contingent foot shock punishment was less efficacious in limiting fentanyl seeking in ANE rats, relative to nicotine-naïve controls. Next, we demonstrated that ANE limits learning about the deleterious consequences of acute opioid intoxication in adulthood. In a combined conditioned taste avoidance and place preference paradigm we found that ANE resulted in significant reductions in the strength of morphine-induced CTA, and a simultaneous enhancement of CPP at a higher dose that was less capable of driving reinforcement in naïve controls. Finally, we examined the expression of perineuronal nets (PNNs) within insular cortex (IC) and found ANE rats to have increased density of PNNs across the anterior IC and significantly more parvalbumin-labeled IC cells relative to naïve controls. Together, these data lay the framework for a mechanistic explanation of the extreme comorbidity between nicotine use and development of OUDs.http://www.sciencedirect.com/science/article/pii/S2772392524000099Pavlovian conditioningPunishmentFentanylMorphineSelf-administrationCompulsive |
| spellingShingle | S.C. Honeycutt A. Mukherjee M.S. Paladino E.A. Gilles-Thomas G.C. Loney Adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal nets Addiction Neuroscience Pavlovian conditioning Punishment Fentanyl Morphine Self-administration Compulsive |
| title | Adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal nets |
| title_full | Adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal nets |
| title_fullStr | Adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal nets |
| title_full_unstemmed | Adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal nets |
| title_short | Adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal nets |
| title_sort | adolescent nicotine exposure promotes adulthood opioid consumption that persists despite adverse consequences and increases the density of insular perineuronal nets |
| topic | Pavlovian conditioning Punishment Fentanyl Morphine Self-administration Compulsive |
| url | http://www.sciencedirect.com/science/article/pii/S2772392524000099 |
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