Hedonic sensitivity to natural rewards is affected by prenatal stress in a sex-dependent manner

Marie Line Reynaert, Jordan Marrocco, Jérôme Mairesse, Luana Lionetto, Maurizio Simmaco, Lucie Deruyter, Delphine Allorge, Anna Moles, Anna Pittaluga, Stefania Maccari, Sara Morley-Fletcher, Gilles Van Camp, Ferdinando Nicoletti

Research output: Contribution to journalArticle

Abstract

Palatable food is a strong activator of the reward circuitry and may cause addictive behavior leading to eating disorders. How early life events and sex interact in shaping hedonic sensitivity to palatable food is largely unknown. We used prenatally restraint stressed (PRS) rats, which show abnormalities in the reward system and anxious/depressive-like behavior. Some of the hallmarks of PRS rats are known to be sex-dependent. We report that PRS enhanced and reduced milk chocolate-induced conditioned place preference in males and females, respectively. Male PRS rats also show increases in plasma dihydrotestosterone (DHT) levels and dopamine (DA) levels in the nucleus accumbens (NAc), and reductions in 5-hydroxytryptamine (5-HT) levels in the NAc and prefrontal cortex (PFC). In male rats, systemic treatment with the DHT-lowering drug finasteride reduced both milk chocolate preference and NAc DA levels. Female PRS rats showed lower plasma estradiol (E2 ) levels and lower DA levels in the NAc, and 5-HT levels in the NAc and PFC. E2 supplementation reversed the reduction in milk chocolate preference and PFC 5-HT levels. In the hypothalamus, PRS increased ERα and ERβ estrogen receptor and CARTP (cocaine-and-amphetamine receptor transcript peptide) mRNA levels in males, and 5-HT2C receptor mRNA levels in females. Changes were corrected by treatments with finasteride and E2 , respectively. These new findings show that early life stress has a profound impact on hedonic sensitivity to high-palatable food via long-lasting changes in gonadal hormones. This paves the way to the development of hormonal strategies aimed at correcting abnormalities in the response to natural rewards.

Original languageEnglish
Pages (from-to)1072-1085
Number of pages14
JournalAddiction Biology
Volume21
Issue number6
DOIs
Publication statusPublished - Nov 2016

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Pleasure
Nucleus Accumbens
Reward
Prefrontal Cortex
Finasteride
Dopamine
Serotonin
Milk
Dihydrotestosterone
Food
Receptor, Serotonin, 5-HT2C
Addictive Behavior
Gonadal Hormones
Messenger RNA
Psychological Stress
Estrogen Receptors
Hypothalamus
Estradiol
Peptides
Therapeutics

Keywords

  • Journal Article

Cite this

Reynaert, M. L., Marrocco, J., Mairesse, J., Lionetto, L., Simmaco, M., Deruyter, L., ... Nicoletti, F. (2016). Hedonic sensitivity to natural rewards is affected by prenatal stress in a sex-dependent manner. Addiction Biology, 21(6), 1072-1085. https://doi.org/10.1111/adb.12270

Hedonic sensitivity to natural rewards is affected by prenatal stress in a sex-dependent manner. / Reynaert, Marie Line; Marrocco, Jordan; Mairesse, Jérôme; Lionetto, Luana; Simmaco, Maurizio; Deruyter, Lucie; Allorge, Delphine; Moles, Anna; Pittaluga, Anna; Maccari, Stefania; Morley-Fletcher, Sara; Van Camp, Gilles; Nicoletti, Ferdinando.

In: Addiction Biology, Vol. 21, No. 6, 11.2016, p. 1072-1085.

Research output: Contribution to journalArticle

Reynaert, ML, Marrocco, J, Mairesse, J, Lionetto, L, Simmaco, M, Deruyter, L, Allorge, D, Moles, A, Pittaluga, A, Maccari, S, Morley-Fletcher, S, Van Camp, G & Nicoletti, F 2016, 'Hedonic sensitivity to natural rewards is affected by prenatal stress in a sex-dependent manner', Addiction Biology, vol. 21, no. 6, pp. 1072-1085. https://doi.org/10.1111/adb.12270
Reynaert ML, Marrocco J, Mairesse J, Lionetto L, Simmaco M, Deruyter L et al. Hedonic sensitivity to natural rewards is affected by prenatal stress in a sex-dependent manner. Addiction Biology. 2016 Nov;21(6):1072-1085. https://doi.org/10.1111/adb.12270
Reynaert, Marie Line ; Marrocco, Jordan ; Mairesse, Jérôme ; Lionetto, Luana ; Simmaco, Maurizio ; Deruyter, Lucie ; Allorge, Delphine ; Moles, Anna ; Pittaluga, Anna ; Maccari, Stefania ; Morley-Fletcher, Sara ; Van Camp, Gilles ; Nicoletti, Ferdinando. / Hedonic sensitivity to natural rewards is affected by prenatal stress in a sex-dependent manner. In: Addiction Biology. 2016 ; Vol. 21, No. 6. pp. 1072-1085.
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