Abstract
Rationale
Early life adversity impacts reward-related behaviors, including reward seeking for drugs of abuse. However, the effects of early stress on natural rewards, such as food and social rewards, which have strong implications for symptoms of psychiatric conditions such as major depressive disorder (MDD), are understudied. To fill this gap, we used the limited bedding and nesting (LBN) procedure to assess the impact of early resource scarcity on motivational drive for both food and social rewards in rats.
Methods
Male and female Long Evans rats were reared in either an LBN environment, with limited nesting materials and no enrichment, from their postnatal day 2–9 or control environment with ample nesting materials and enrichment. As adults, they were tested for reward-seeking behavior on progressive ratio operant tasks: food reward (sucrose) or social reward (access to a same-sex/age conspecific).
Results
We observed sex differences in the impact of LBN on motivation for natural rewards. In males, LBN increased motivation for both a sucrose and social reward. In females, LBN reduced motivation for sucrose but had no effect on social reward.
Conclusions
These results suggest that the effects of LBN on motivation for natural rewards are both sex- and reinforcer-dependent, with males and females showing differential motivation for food and social rewards following early scarcity. Our previous data revealed an LBN-driven reduction in motivation for morphine in males and no effect in females, highlighting the reinforcer-dependent impact of early resource scarcity on motivated behavior more widely.
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References
Agmo A (1997) Male rat sexual behavior. Brain Res Brain Res Protoc 1:203–209
al’Absi M, Ginty AT, Lovallo WR (2021) Neurobiological mechanisms of early life adversity, blunted stress reactivity and risk for addiction. Neuropharmacology 188:1–9
Angelini V, Howdon DDH, Mierau JO (2019) Childhood socioeconomic status and late-adulthood mental health: results from the survey on health, ageing and retirement in Europe. The J Gerontology: Series B 74:95–104
Bari AA, Pierce RC (2005) D1-like and D2 dopamine receptor antagonists administered into the shell subregion of the rat nucleus accumbens decrease cocaine, but not food, reinforcement. Neuroscience 135:959–968
Baskin-Sommers AR, Foti D (2015) Abnormal reward functioning across substance use disorders and major depressive disorder: considering reward as a transdiagnostic mechanism. Int J Psychophysiol 98:227–239
Bolton JL, Molet J, Regev L, Chen Y, Rismanchi N, Haddad E, Yang DZ, Obenaus A, Baram TZ (2018a) Anhedonia following early-life adversity involves aberrant interaction of reward and anxiety circuits and is reversed by partial silencing of amygdala corticotropin-releasing hormone gene. Biol Psychiatry 83:137–147
Bolton JL, Ruiz CM, Rismanchi N, Sanchez GA, Castillo E, Huang J, Cross C, Baram TZ, Mahler SV (2018b) Early-life adversity facilitates acquisition of cocaine self-administration and induces persistent anhedonia. Neurobiology of Stress 8:57–67
Butler-Struben HM, Kentner AC, Trainor BC (2022) What’s wrong with my experiment?: the impact of hidden variables on neuropsychopharmacology research. Neuropsychopharmacology 47:1285–1291
Cooper S, Robison AJ, Mazei-Robison MS (2017) Reward circuitry in addiction. Neurotherapeutics 14:687–697
Depoortere RY, Li DH, Lane JD, Emmett-Oglesby MW (1993) Parameters of self-administration of cocaine in rats under a progressive-ratio schedule. Pharmacol Biochem Behav 45:539–548
Eck SR, Ardekani CS, Salvatore M, Luz S, Kim ED, Rogers CM, Hall A, Lee DE, Famularo ST, Bhatnagar S, Bangasser DA (2019) The effects of early life adversity on growth, maturation, and steroid hormones in male and female rats. Eur J Neurosci.
Eck SR, Palmer JL, Bavley CC, Karbalaei R, Ordoñes Sanchez E, Flowers J, Holley A, Wimmer ME, Bangasser DA (2022) Effects of early life adversity on male reproductive behavior and the medial preoptic area transcriptome. Neuropsychopharmacology.
Evans GW (2004) The environment of childhood poverty. Am Psychol 59:77
Gallo M, Shleifer DG, Godoy LD, Ofray D, Olaniyan A, Campbell T, Bath KG (2019) Limited bedding and nesting induces maternal behavior resembling both hypervigilance and abuse. Frontiers in Behavioral Neuroscience 13.
Hopkins TJ, Rupprecht LE, Hayes MR, Blendy JA, Schmidt HD (2012) Galantamine, an acetylcholinesterase inhibitor and positive allosteric modulator of nicotinic acetylcholine receptors, attenuates nicotine taking and seeking in rats. Neuropsychopharmacology 37:2310–2321
Ivy AS, Brunson KL, Sandman C, Baram TZ (2008) Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 154:1132–1142
Ku KM, Weir RK, Silverman JL, Berman RF, Bauman MD (2016) Behavioral phenotyping of juvenile Long-Evans and Sprague-Dawley rats: implications for preclinical models of autism spectrum disorders. PLoS ONE 11:e0158150
Lee JO, Hill KG, Hartigan LA, Boden JM, Guttmannova K, Kosterman R, Bailey JA, Catalano RF (2015) Unemployment and substance use problems among young adults: does childhood low socioeconomic status exacerbate the effect? Soc Sci Med 143:36–44
LeMoult J, Humphreys KL, Tracy A, Hoffmeister J-A, Ip E, Gotlib IH (2020) Meta-analysis: exposure to early life stress and risk for depression in childhood and adolescence. J Am Acad Child Adolesc Psychiatry 59:842–855
Levis SC, Birnie MT, Bolton JL, Perrone CR, Montesinos JS, Baram TZ, Mahler SV (2022) Enduring disruption of reward and stress circuit activities by early-life adversity in male rats. Transl Psychiatry 12:251
Levis SC, Bentzley BS, Molet J, Bolton JL, Perrone CR, Baram TZ, Mahler SV (2019) On the early life origins of vulnerability to opioid addiction. Molecular Psychiatry.
Mietlicki-Baase EG, Rupprecht LE, Olivos DR, Zimmer DJ, Alter MD, Pierce RC, Schmidt HD, Hayes MR (2013) Amylin receptor signaling in the ventral tegmental area is physiologically relevant for the control of food intake. Neuropsychopharmacology 38:1685–1697
Molet J, Heins K, Zhuo X, Mei YT, Regev L, Baram TZ, Stern H (2016) Fragmentation and high entropy of neonatal experience predict adolescent emotional outcome. Transl Psychiatry 6:e702–e702
Nall RW, Heinsbroek JA, Nentwig TB, Kalivas PW, Bobadilla A-C (2021) Circuit selectivity in drug versus natural reward seeking behaviors. J Neurochem 157:1450–1472
Nestler EJ, Carlezon WA Jr (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59:1151–1159
Ordoñes Sanchez E, Bavley CC, Deutschmann AU, Carpenter R, Peterson DR, Karbalaei R, Flowers J, Rogers CM, Langrehr MG, Ardekani CS, Famularo ST, Bongiovanni AR, Knouse MC, Floresco SB, Briand LA, Wimmer ME, Bangasser DA (2021) Early life adversity promotes resilience to opioid addiction-related phenotypes in male rats and sex-specific transcriptional changes. Proc Natl Acad Sci 118:e2020173118
Pratt WE, Kelley AE (2004) Nucleus accumbens acetylcholine regulates appetitive learning and motivation for food via activation of muscarinic receptors. Behav Neurosci 118:730
Raineki C, Moriceau S, Sullivan RM (2010) Developing a neurobehavioral animal model of infant attachment to an abusive caregiver. Biol Psychiat 67:1137–1145
Ramsey LA, Holloman FM, Hope BT, Shaham Y, Venniro M (2022) Waving through the window: a model of volitional social interaction in female mice. Biol Psychiatry 91:988–997
Reiss F, Meyrose A-K, Otto C, Lampert T, Klasen F, Ravens-Sieberer U (2019) Socioeconomic status, stressful life situations and mental health problems in children and adolescents: results of the German BELLA cohort-study. PLoS ONE 14:e0213700
Rincón-Cortés M, Sullivan RM (2016) Emergence of social behavior deficit, blunted corticolimbic activity and adult depression-like behavior in a rodent model of maternal maltreatment. Transl Psychiatry 6:e930
Russo SJ, Nestler EJ (2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14:609–625
Sachs BD, Lumia AR (1981) Is stress due to shipment of animals a confounding variable in developmental research? Dev Psychobiol 14:169–171
Shupe EA, Clinton SM (2021) Neonatal resource scarcity alters maternal care and impacts offspring core temperature and growth in rats. Dev Psychobiol 63:e22144
Strzelewicz A, Sanchez E, Rondón-Ortiz A, Raneri A, Famularo S, Bangasser D, Kentner A (2019) Access to a high resource environment protects against accelerated maturation following early life stress: a translational animal model of high, medium and low security settings. Hormones and behavior.
Szczypiński JJ, Gola M (2018) Dopamine dysregulation hypothesis: the common basis for motivational anhedonia in major depressive disorder and schizophrenia? Rev Neurosci 29:727–744
Treadway MT, Zald DH (2013) Parsing anhedonia: translational models of reward-processing deficits in psychopathology. Curr Dir Psychol Sci 22:244–249
Venniro M, Shaham Y (2020) An operant social self-administration and choice model in rats. Nat Protoc 15:1542–1559
Venniro M, Zhang M, Caprioli D, Hoots JK, Golden SA, Heins C, Morales M, Epstein DH, Shaham Y (2018) Volitional social interaction prevents drug addiction in rat models. Nat Neurosci 21:1520–1529
Venniro M, Russell TI, Zhang M, Shaham Y (2019) Operant social reward decreases incubation of heroin craving in male and female rats. Biol Psychiatry 86:848–856
Walker C-D, Bath KG, Joels M, Korosi A, Larauche M, Lucassen PJ, Morris MJ, Raineki C, Roth TL, Sullivan RM, Taché Y, Baram TZ (2017) Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential. Stress 20:421–448
Walsh JJ, Christoffel DJ, Malenka RC (2022) Neural circuits regulating prosocial behaviors. Neuropsychopharmacology.
Wendel KM, Short AK, Noarbe BP, Haddad E, Palma AM, Yassa MA, Baram TZ, Obenaus A (2021) Early life adversity in male mice sculpts reward circuits. Neurobiology of Stress 15:100409
Funding
This work is supported by National Institute of Health grants: DA049837 to D.A.B., DA056534 to D.A.B. and M.E.W., DA046537 to M.E.W, and T32 DA007237 to A.V.W (PI Unterwald), and DA047976 to M.V. This is also funded by a BBRF Young Investigator Grant 28897 to M.V. This work was also supported by a National Science Foundation grant IOS1929829 to D.A.B.
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Williams, A.V., Flowers, J., Coates, K.S. et al. Early resource scarcity alters motivation for natural rewards in a sex- and reinforcer-dependent manner. Psychopharmacology 239, 3929–3937 (2022). https://doi.org/10.1007/s00213-022-06264-9
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DOI: https://doi.org/10.1007/s00213-022-06264-9