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Adolescent brain and behavior: Age-related sensitivities to natural rewards and drugs

Adolescent brain and behavior: Age-related sensitivities to natural rewards and drugs. Linda Patia Spear Binghamton University Supported in part by grants R01 DA19071, R37 AA12525 and R01 AA12150. Adolescence. transition between childhood/immaturity and adulthood/maturity

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Adolescent brain and behavior: Age-related sensitivities to natural rewards and drugs

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  1. Adolescent brain and behavior: Age-related sensitivities to natural rewards and drugs Linda Patia Spear Binghamton University Supported in part by grants R01 DA19071, R37 AA12525 and R01 AA12150

  2. Adolescence • transition between childhood/immaturity and adulthood/maturity • prototypic age ranges: humans: 12-18 yrs. (early as 8-10; late as 25) rats: 28-42 days (early as 23-25; late as 55+) • highly conserved physiological transitions: • puberty • other hormonal changes; growth spurt • neural transformations • common age-typical behavioral characteristics • increases in peer-directed social behavior • risk taking/novelty seeking/sensation seeking, impulsivity, etc. [species-specific characteristics as well]

  3. Forebrain changes in Adolescents • Prefrontal Cortex (PFC) • Reduced excit. drive, myelination (humans, primates, rats) • Decrease in PFC volume (humans & rodents) • Peak of DA innervation (humans, primates, rats) • High DA turnover early followed by decline (rats) • Decline in NMDA-R binding (rats) • Nucleus Accumbens/ Striatum • Low DA turnover early followed by increase (rats) • Decline in DA-R binding (esp. striatum) (rats) • Hippocampus - myelination (humans, rodents) • Decline in NMDA-R binding (rats) • Amygdala • increased/altered patterns of activity (humans, rodents) • Increase in amygdala-PFC connectivity (rodents)

  4. Functional consequences of adolescent brain sculpting • Relationship to hormonal reawakening of puberty? • Reduction in brain energy utilization, and support of continued cognitive/emotional development • Modulate highly conserved adolescent behaviors directed towards natural rewards

  5. Characteristic adolescent behaviors • Increases in social interactions/peer affiliations • Develop social skills/support • Guide choice behavior • (may be associated with an increase in parent/ adolescent conflict)

  6. CONDITIONED PLACE PREFERENCE

  7. 60 Control Paired 45 30 15 0 Group Isolate Group Isolate Social CPP Adult Adolescent Coefficient (%) Subject Housing

  8. 75 group-housed isolate-housed partner partner 60 Control Paired 45 Coefficient (%) 30 15 0 Group Isolated Group Isolated Subject Housing For adolescents, social history of stimulus animal matters

  9. group-housed isolate-housed 75 partner partner 60 Control Paired 45 Coefficient (%) 30 15 0 Group Isolated Group Isolated Subject Housing For adolescents, social history of stimulus animal matters

  10. Adolescent 120 isolate-housed group-housed partner partner 90 60 Social Avoidance (s) 30 0 Group Isolate Group Isolate Social Avoidance during conditioning Subject Housing

  11. Adolescent 120 isolate-housed group-housed partner partner 90 60 Social Avoidance (s) 30 0 Group Isolate Group Isolate Subject Housing Social Avoidance during conditioning

  12. Social CPP Adolescent animals are unusually sensitive to social stimuli -Adolescents (but not adults) show social CPP even when socially replete -Socially deprived adolescents exhibit marked increases in social behavior and are socially “ostracized” by non-deprived peers

  13. Characteristic adolescent behaviors • Increases in social interactions/peer affiliations • Develop social skills/support • Guide choice behavior • (may be associated with an increase in parent/ adolescent conflict) • Increases in risk-taking, novelty-seeking, sensation-seeking, impulsivity • Impetus for exploring new territories, aiding in emigration • Enhance probability of reproductive success (Wilson & Daly) • Foster peer acceptance (Shedler & Block)

  14. Novelty CPP Adolescent Adult 60 Control 50 Paired 40 Coefficient (%) 30 20 10 0 Isolate Group Isolate Group Subject Housing Novelty CPP –males

  15. Adolescent Adult 60 225 Adolescent Adult Control 50 Paired 180 40 Coefficient (%) 135 30 Time with Object (s) 90 20 45 10 0 0 Isolate Group Isolate Group Group Isolate Group Isolate Subject Housing Subject Housing Novelty CPP –males Time with object during condit. Novelty CPP

  16. 225 Adolescent Adult 180 135 Time with Object (s) 90 45 0 Group Isolate Group Isolate Subject Housing Novelty CPP – females Time with object during condit.

  17. Adult Adolescent 60 225 Adolescent Adult Control Paired 50 180 40 Coefficient (%) 135 Time with Object (s) 30 90 20 45 10 0 0 Group Isolate Group Isolate Group Isolate Group Isolate Subject Housing Subject Housing Novelty CPP – females Time with object during condit. Novelty CPP

  18. Novelty CPP Novelty exploration increased during adolescence Novelty CPP more robust in adolescent than adult males No age difference in novelty CPP in females Novelty exploration ≠ novelty reward

  19. Impulsivity in adolescence

  20. % Pellets received from LDH 1.4 ADOL ADULT 1.2 Arc sine (% Pellets from LDH) 1.0 0.8 0.6 0.4 1 2 3 4 5 6 7 8 9 10 11 12 Experimental Day

  21. Interaction between impulsivity and ethanol intake Impulsivity defined as SDH pokes during delay on Day 7 Impulsivity defined as % rewarded pokes on Day 8 (b) (a) 10 10 LOW IMPUL LOW IMPUL HI IMPUL HI IMPUL 8 8 6 6 Ethanol intake (g/kg) Ethanol intake (g/kg) 4 4 2 2 0 0 ADOL ADULT ADOL ADULT Age Age

  22. Functional consequences of adolescent brain sculpting • Relationship to hormonal reawakening of puberty? • Support continued cognitive/emotional development • Modulate highly conserved adolescent behaviors directed towards natural rewards (social stimuli, risk taking/novelty seeking/impulsivity) • Influence sensitivity to and motivation for other reinforcing/rewarding stimuli, including drugs

  23. 50 Adolescents Adults 30 Initial Test 10 Coefficient (%) -10 -30 -50 Saline Nicotine Saline Nicotine Treatment Nicotine-induced CPP (0.6 mg/kg; biased design; 1 trial/day, saline control; group housed)

  24. 100 80 60 40 20 0 Locomotor Activity during Conditioning Adolescents Adults Number of Bouts Saline Nicotine 1 2 3 4 1 2 3 4 Exposures

  25. Summary • Adolescence as a highly conserved developmental stage with certain common neurobehavioral features • Sculpting of adolescent brain in mesocorticolimbic regions may influence reward-related behaviors • Indeed, adolescents generally: • spend more time engaged with social stimuli and novelty and are more impulsive than adults • find: • Social stimuli • Novelty • Nicotine more rewarding/rewarding under more circumstances than adults • Questions for the future: • Neural substrates underlying specific adolescent-typical behaviors • Adolescent-associated alterations in incentive motivation or hedonic value?

  26. FACULTY collaborators: Terry Deak Juan Molina Lena Varlinskaya Brent Vogt Norman Spear Undergrad. honors students: Bonnie Vastola Kristin Osiecki Tom Washburn Mike Hernandez Michelle Baretto Scott Falkowitz Former and current graduate trainees: Marisa Silveri James Campbell Nina Katovic Drew Douglas Raj Pottayil Steve Brunell Tammi Doremus Rob Ristuccia Courtney Vetter Amanda Willey Carrie Wilmouth Collaborators For futher info: lspear@binghamton.edu

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