Regular exposure to a Citrus-based sensory functional food ingredient alleviates the BOLD brain responses to acute pharmacological stress in a pig model of psychosocial chronic stress

PLoS One. 2020 Dec 28;15(12):e0243893. doi: 10.1371/journal.pone.0243893. eCollection 2020.

Abstract

Psychosocial chronic stress is a critical risk factor for the development of mood disorders. However, little is known about the consequences of acute stress in the context of chronic stress, and about the related brain responses. In the present study we examined the physio-behavioural effects of a supplementation with a sensory functional food ingredient (FI) containing Citrus sinensis extract (D11399, Phodé, France) in a pig psychosocial chronic stress model. Female pigs underwent a 5- to 6-week stress protocol while receiving daily the FI (FI, n = 10) or a placebo (Sham, n = 10). We performed pharmacological magnetic resonance imaging (phMRI) to study the brain responses to an acute stress (injection of Synacthen®, a synthetic ACTH-related agonist) and to the FI odour with or without previous chronic supplementation. The olfactory stimulation with the ingredient elicited higher brain responses in FI animals, demonstrating memory retrieval and habituation to the odour. Pharmacological stress with Synacthen injection resulted in an increased activity in several brain regions associated with arousal, associative learning (hippocampus) and cognition (cingulate cortex) in chronically stressed animals. This highlighted the specific impact of acute stress on the brain. These responses were alleviated in animals previously supplemented by the FI during the entire chronic stress exposure. As chronic stress establishes upon the accumulation of acute stress events, any attenuation of the brain responses to acute stress can be interpreted as a beneficial effect, suggesting that FI could be a viable treatment to help individuals coping with repeated stressful events and eventually to reduce chronic stress. This study provides additional evidence on the potential benefits of this FI, of which the long-term consequences in terms of behaviour and physiology need to be further investigated.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / diagnostic imaging
  • Brain / drug effects
  • Brain / physiology*
  • Citrus / chemistry*
  • Female
  • Food Ingredients / analysis
  • France
  • Functional Food / analysis
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Smell / drug effects
  • Smell / physiology*
  • Stress, Psychological*
  • Swine

Substances

  • Food Ingredients

Grants and funding

The funder (Phodé (Terssac, France; https://www.phode.com/en/) provided the functional ingredient tested and support in the form of salaries for authors SM, VN, and PE but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of the authors affiliated to our private partner are articulated in the ‘author contributions’ section. Notably, authors PE and VN read and validated the final manuscript but did not decide which results to publish and how to interpret these results. The Association Nationale de la Recherche et de la Technologie (ANRT; http://www.anrt.asso.fr/fr), and the french Institut national de recherche pour l’agriculture, l’alimentation et l’environnement (INRAE; https://www.inrae.fr/) (PhD grant CIFRE of SM, N° 2016/0891) also provided funding for this study.