Problem drinking alters gray matter volume and food cue responses of the lateral orbitofrontal cortex

Abstract

Alcohol misuse is associated with significant energy deficits. As feeding involves multiple sensory, cognitive, and affective processes, low food intake in problem drinkers likely reflects alterations in both regional and interregional responses. To investigate the effects of problem drinking on feeding-related neural activities and connectivities, we examined functional magnetic resonance imaging (fMRI) data in 82 drinkers who viewed palatable food and nonfood images in alternating blocks. Drinking severity was assessed with the Alcohol Use Disorders Identification Test (AUDIT). A wholebrain multiple regression with AUDIT scores as the predictor showed a negative correlation between drinking severity and activation to food vs nonfood cues in the lateral orbitofrontal cortex (lOFC). AUDIT scores were also negatively correlated with the gray matter volume (GMV) of the lOFC and regions that responded preferentially to food stimuli, including the left middle frontal gyrus, bilateral middle insula, and occipital cortices. Connectivity strength between the lOFC and these regions was negatively modulated by drinking severity. In contrast, there was no relationship between AUDIT scores and lOFC connectivity with regions that did not show either selectivity to food images or GMV loss. A mediation analysis further suggested that alcohol misuse may have compromised lOFC's structural integrity, which in turn disrupted lOFC interactions with regions that support the processing of visual food cues. Overall, the findings provide evidence for the effects of problem drinking on the brain substrates of feeding, potentially shedding light on the neural mechanisms underlying energy deficits in at-risk drinkers. KEYWORDS alcohol misuse, food cue processing, food intake, functional connectivity, gray matter volume, lateral orbitofrontal cortex 1 | INTRODUCTION Contrary to the short-term stimulating effects of acute alcohol ingestion on food consumption in casual drinkers, heavy drinking has been associated with depressed appetite, 2 low food consumption, 3 and decreased meal frequency, 1 leading to energy deficits. As feeding ensures organisms' survival, reduced food intake despite energy deficits likely reflects powerful changes in the neural substrates supporting feeding behavior. Indeed, excessive alcohol use has been associated with gray matter volume (GMV) loss in multiple brain regions involved in the regulation of food intake including the orbitofrontal, insular, medial prefrontal, and occipital cortices. 4-6 Previous research has implicated such regions in the reward, 7 cognitive control, 8 taste, 9 and visual processing of food stimuli, 10 respectively. Together, these

Brain Responses to High-Calorie Visual Food Cues in Individuals with Normal-Weight or Obesity: An Activation Likelihood Estimation Meta-Analysis

“…Our search identified 59 eligible studies (total m = 59) [ 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 , 74 , 75 , 76 , 77 , 78 , 79 , 80 , 81 , 82 , 83 , 84 , 85 , 86 , 87 , 88 , 89 , 90 , 91 ,…”

Age-related reduction in trait anxiety: Behavioral and neural evidence of automaticity in negative facial emotion processing

“…We conducted a generalized gPPI analysis with the mPFC as a seed (identified from whole-brain age regressions; see Results ) to explore age-related changes in functional connectivity during emotion processing. We followed the method as in our previous studies ( Le et al, 2021 ; Wang et al, 2021 ). A PPI model was created for each subject with three regressors: the physiological variable which represents temporally filtered, mean-corrected and deconvolved time series of the seed region mPFC, the psychological variable which represents the task contrasts (e.g., negative vs. neutral), and a PPI variable that was computed as element-by-element product of deconvolved time series of the seed and contrast, followed by re-convolution with the HRF.…”

Pain and reward circuits antagonistically modulate alcohol expectancy to regulate drinking

“…A general linear model (GLM) was constructed as in previous work with similar task designs 31,32 to differentiate regional activations to alcohol and neutral cues (Supplemental Methods). One-sample t-tests were conducted at the individual subject level to evaluate alcohol vs. neutral cue contrasts.…”