Review: Impact of food, gut–brain signals and metabolic status on brain activity in the pig model: 10 years of nutrition research using in vivo brain imaging

Abstract

The purpose of this review is to offer a panorama on 10 years of nutrition research using in vivo brain imaging in the pig model. First, we will review some work describing the brain responses to food signals, including basic tastants such as sweet and bitter at both oral and visceral levels, as well as conditioned preferred and aversive flavours. Second, we will have a look at the impact of weight gain and obesity on brain metabolism and functional responses, drawing the parallel with obese human patients. Third, we will evoke the concept of the developmental origins of health and diseases, and how the pig model can shed light on the importance of maternal nutrition during gestation and lactation for the development of the gut-brain axis and adaptation abilities of the progeny to nutritional environments. Finally, three examples of preventive or therapeutic strategies will be introduced: the use of sensory food ingredients or pre-, pro-, and postbiotics to improve metabolic and cognitive functions; the implementation of chronic vagus nerve stimulation to prevent weight gain and glucose metabolism alterations; and the development of bariatric surgery in the pig model for the understanding of its complex mechanisms at the gut-brain level. A critical conclusion will brush the limitations of neurocognitive studies in the pig model and put in perspective the rationale and ethical concerns underlying the use of pig experimentation in nutrition and neurosciences. ImplicationsThe purpose of this review is to offer a panorama on 10 years of nutrition research using in vivo brain imaging in the pig model, and to improve the understanding of the gut-brain axis factors modulating brain activity. This research has implications in the context of animal and human nutrition and health, covering the scope of animal production as well as translational medicine. In addition to the original insight these provide in neurocognitive and developmental sciences, the scientific studies presented here are valuable for the development of new preventive, diagnosis and therapeutics solutions to fight against nutritional and behavioural disorders.

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

“…Moreover, digital stereotaxic atlases are available and many classical human imaging techniques have been implemented in the pig model [17,18]. Thus, pig is a particularly relevant model to study brain responses using in vivo imaging [17,19]. We have notably been working on the development of adequate techniques to discriminate the brain responses to gustatory [20] and olfactory stimulations [21] through fMRI in this model [17,19].…”

Hypothesis paper: electroacupuncture targeting the gut–brain axis to modulate neurocognitive determinants of eating behavior—toward a proof of concept in the obese minipig model

“…fMRI is a non-invasive neuroimaging approach that can be used to investigate sensory, cognitive, and hedonic integration of exteroceptive or interoceptive stimuli in healthy or pathological subjects. Our laboratory has a world-recognized 10-year experience in using functional brain imaging in the pig model for nutritional and translational research [31]. Notably, we previously described, using fMRI or nuclear brain imaging, the pig brain responses to sucrose stimulation or palatable food flavors [95,96] and demonstrated that obese minipigs have similar brain anomalies as obese humans [30].…”

“…All the technologies required for this proof of concept and identification of the best EA acupoints combination have already been implemented in the minipig model [31]. As stated before, this encompasses metabolic, physiological, and behavioral explorations, as well as minimally invasive neurobiological measures of the vagus nerve activity [97] and brain responses to various stimuli via fMRI [96,98].…”

“…In this hypothesis paper, we will first summarize the state of the art supporting an action of EA on the nervous and hormonal pathways connecting the gut to the brain, describing how modulation of the gut-brain communication can influence the central processes underlying food intake control. Second, in light of our 10-year experience in nutrition and neuroscience research in the minipig model at INRA [31], we will justify the implementation of EA in this model to investigate its outcomes in the context of obesity.…”

fMRI-Based Brain Responses to Quinine and Sucrose Gustatory Stimulation for Nutrition Research in the Minipig Model: A Proof-of-Concept Study

“…Olfactory and gustatory stimulations have already been widely investigated in the pig and minipig models. Roura and Fu (2017) and Val-Laillet (2018) have recently provided complete reviews on this topic and the scope of the methodologies used for this purpose come from ethology ( Clouard et al, 2012a , c ; Clouard and Val-Laillet, 2014 ) to electrophysiology ( Danilova et al, 1999 ) and nuclear imaging, such as single photon emission computed tomography (SPECT) or positron emission tomography (PET; Clouard et al, 2012a , 2014b ; Val-Laillet et al, 2015 ; Val-Laillet, 2018 ). These approaches provide either information about a long-term integration of the stimulation, i.e., behavior or nuclear imaging, or a direct but local impact, i.e., electrophysiology.…”