Abstract
The aim was to investigate with very large-scale analyses whether there are underlying functional connectivity differences between humans that relate to food reward and whether these in turn are associated with being overweight. In 37 286 humans from the UK Biobank, resting-state functional connectivities of the orbitofrontal cortex (OFC), especially with the anterior cingulate cortex, were positively correlated with the liking for sweet foods (False Discovery Rate (FDR) P < 0.05). They were also positively correlated with the body mass index (BMI) (FDR P < 0.05). Moreover, in a sample of 502 492 people, the 'liking for sweet foods' was correlated with their BMI (r = 0.06, P < 10-125). In a cross-validation with 545 participants from the Human Connectome Project, a higher functional connectivity involving the OFC relative to other brain areas was associated with a high BMI (≥30) compared to a mid-BMI group (22-25; P = 6 × 10-5), and low OFC functional connectivity was associated with a low BMI (≤20.5; P < 0.024). It is proposed that a high BMI relates to increased efficacy of OFC food reward systems and a low BMI to decreased efficacy. This was found with no stimulation by food, so may be an underlying individual difference in brain connectivity that is related to food reward and BMI.
Highlights
The primate including human orbitofrontal cortex (OFC) is involved in food reward, in that neurons in it respond to the sight, smell, taste and texture of food only when hunger is present and the food is rewarding, and functional magnetic resonance imaging activations in humans follow suit (Rolls et al, 1989; Critchley and Rolls, 1996; Kringelbach et al, 2003; Rolls, 2016b, 2019b; Rolls, 2020, 2021b)
The first key finding was that the resting-state functional connectivity between the ventromedial prefrontal cortex (VMPFC) /OFC (VMPFC–OFC) and especially the anterior cingulate cortex was positively correlated with the liking for sweet foods (Figure 1)
There is much evidence that the OFC has neurons that respond to the reward value of the sight, smell taste and oral texture of food and that activations of the medial OFC in humans are related to the reward value of all of these sensory aspects of food (Rolls, 2015, 2016b, 2019b, 2021b; Rolls et al, 2020), but the evidence that the functional connectivity of these areas is higher in those who report a high liking for sweet foods provides an indication that these brain food reward systems may be more strongly connected in individuals who like sweet foods
Summary
Contribute (Kaye, 2008; Kaye et al, 2020). Much previous research on brain connectivity and obesity has focussed more on reduced functionality of brain systems related to executive function, rather than on an enhanced sensitivity of brain systems to food reward (Tregellas et al, 2011; Kullmann et al, 2012; Lips et al, 2014; Garcia-Garcia et al, 2015; Lowe et al, 2019; Donofry et al, 2020; Legget et al, 2021). Measurement of resting-state functional connectivity may provide a measure of whether the intrinsic brain circuitry is different in some individuals, even when it is not being used, for example, for food reward and the control of food intake. One is the anterior cingulate cortex, which has strong connections with the OFC, and is involved as a link from the reward-related OFC to output areas to perform actions to obtain rewards (Rolls, 2019a) This connectivity is highly correlated with sensation-seeking for reward (Wan et al, 2020). Only whether effects are present and of what their magnitude is to help guard against false-positive results in small studies Another feature of the investigation is that brain function was being measured in the resting state without the sight or taste or food, to investigate whether there are differences in OFC functional connectivity even when food is not available. This is the first time that discoveries of the type described here have been reported in large-scale studies, which are not subject to the vagaries of small-scale studies
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