Deficits in episodic memory are related to uncontrolled eating in a sample of healthy adults.
Introduction
Deficits in self-regulatory control are widely implicated in the etiology of overeating and obesity (for reviews, see Lavagnino et al., 2016, Martin and Davidson, 2014). Several studies have shown that obese individuals often respond more impulsively (i.e., faster or more often) on behavioral tasks than normal weight individuals (for recent systematic reviews, see Bartholdy et al., 2016, McClelland et al., 2016). This general failure of self-control is thought to underpin failures in food-intake control, thereby contributing to the disinhibition of eating and eventual weight gain. In line with this possibility, studies have shown that impulsivity predicts greater food intake (Guerrieri et al., 2007, Guerrieri et al., 2012, Guerrieri et al., 2009, Jansen et al., 2009), increased weight gain over time (Francis and Susman, 2009, Seeyave et al., 2009), and resistance to weight loss (Nederkoorn et al., 2010, Nederkoorn et al., 2007). Likewise, disinhibited eating behavior (as assessed by self-report questionnaires) has been associated with greater impulsivity and risk-taking on behavioral measures of self-control (Yeomans & Brace, 2015).
In rodents, these relationships between impulsivity, overeating, and obesity have been attributed to a common underlying deficit in memory inhibition (for reviews, see Davidson et al., 2014, Kanoski and Davidson, 2011). Memory inhibition is the process which enables individuals to suppress or ignore unwanted or outdated associations from memory and, thus, helps to filter goal-relevant information from goal-irrelevant information (Levy & Anderson, 2002). As such, memory inhibition is critical for performing a variety of self-regulatory tasks, including most tasks associated with executive function such as working memory and cognitive flexibility (see Friedman and Miyake, 2017, Miyake et al., 2000; Akira Miyake & Friedman, 2012). Regarding food intake control, memory inhibition is critical for gating the incentive properties of food cues and, thus, our impetus to act on them (for a discussion of this account, see Martin & Davidson, 2014). Food and food cues are only capable of prompting us to eat if they remind us, via retrieval of learned associations, of food reward. Thus, food intake control depends not only upon the amount of behavioral control one possesses-- food intake control also depends upon how well one can resist thinking about the rewarding aspects of food that motivate one to eat in the first place (i.e., memory inhibition).
Supporting this possibility, studies in rodents have consistently shown that manipulations that weaken memory inhibition also weaken rats' self-control over their food intake and increase their susceptibility to overeat in response to external food cues. For instance, rats with deficits in memory inhibition exhibit greater food cue reactivity (i.e., “impulsive”, perseverative responding for food), overeating, and weight gain (for reviews, see Davidson et al., 2014, Kanoski, 2012, Kendig, 2014). Natural variations in memory inhibition have also been found to predict weight maintenance, with stronger memory inhibition predicting resistance to weight gain (Davidson et al., 2012, Davidson et al., 2013).
These findings implicate individual differences in memory inhibitory control as a predictor of uncontrolled eating. However, despite the links established in rodent studies, evidence examining the contribution of memory inhibition to human eating behavior is lacking. There is some evidence suggests that obese people and disinhibited eaters are more susceptible to food-related memory intrusions and are less effective at suppressing these food-related thoughts (Soetens and Braet, 2006, Soetens et al., 2006, Soetens et al., 2008; but see; Erskine and Georgiou, 2010, Soetens and Braet, 2007) but these studies have relied predominantly on subjective thought-suppression paradigms wherein participants are asked to monitor and record their own food-related thoughts. Thus, although previous studies in this area are broadly suggestive that deficits in cognitive control relate to lower levels of food intake control, there is a need for further research on this problem using objective measures of cognitive performance.
While memory inhibition helps to control food intake by gating our recollection of the incentive properties of food that entice people to eat, memory retrieval is not uniformly detrimental to food intake control. Evidence suggests that episodic memory can also protect against overeating by helping individuals recall past eating episodes (i.e., portion size, time of last meal, etc.) (Brunstrom et al., 2012, Higgs, 2016, Robinson et al., 2013). This recall of past eating episodes enables individuals to make meal-to-meal compensatory adjustments in their food intake, and thus helps ensure that individuals do not overeat throughout the day-- adjusting for a large breakfast by consuming a smaller lunch is difficult if one cannot accurately recall the size or nutritional content of one's breakfast! By this account, individual differences in episodic recall might also predict tendencies towards uncontrolled eating in humans (i.e., weaker recall predicting a greater susceptibility to overeat).
In support for this idea, studies have shown that individuals who demonstrate severe episodic memory deficits (and, thus, cannot remember their recent meals) also exhibit aberrant eating behavior. For instance, amnesiac individuals will eat two meals in a row without exhibiting any loss of appetite, and will often begin eating a third meal if not stopped (Hebben et al., 1985, Rozin et al., 1998). In non-amnesiacs, manipulating participants’ ability to encode or retrieve the memory of a recent meal has also been shown to influence appetite and moderate eating at the next meal, with better recall being associated with less hunger and lower intakes (Brunstrom et al., 2012, Higgs et al., 2012, Robinson et al., 2013). Evidence from rodent studies suggest that this ability to episodically recall past eating occasions is mediated by the dorsal hippocampus, and is especially important for satiety processing and meal initiation (i.e., helping to delay the onset of the next meal) (Parent, 2016). For instance, disrupting memory consolidation after a feeding episode (by pharmacologically inhibiting dorsal hippocampal neurons) has been found to reduce the inter-meal interval and increase the size of the next meal (Henderson et al., 2013, Parent et al., 2014). Together, these studies highlight the importance of memory for recent eating in appetite control, and implicate deficits in episodic memory as a contributor to overeating and obesity in humans.
Although memory for recent eating has been implicated as an important contributor to satiety and energy intake (Higgs, 2016), relatively few studies have experimentally examined whether general episodic recall ability is related to food intake control in normal (i.e., non-amnesic) individuals. As part of their research investigating the Western diet and its effects on hippocampal-function, Stevenson and colleagues have shown that verbal learning during a paired associates task is negatively associated with consumption of saturated fats and sugars (Francis & Stevenson, 2013) and that individuals with worse memory performance are resistant to the satiating effects of eating (i.e., exhibiting less reductions in 'wanting' food after consuming a standardized meal) (Attuquayefio et al., 2016). This finding was interpreted as evidence that consuming a Western diet disrupted memory, and thereby disrupted the ability to use satiety to inhibit pleasant food related memories (i.e., wanting) (for a review of this account, see Davidson, Kanoski, Walls, & Jarrard, 2005). Notably, that study (Attuquayefio et al., 2016) represents one of the few direct tests linking general (i.e., non-food) memory deficits in the development of eating dysregulation in humans, emphasizing the need for additional research in this area.
Here, we examined how natural variations in memory inhibitory control and episodic memory relate to individual differences in food intake control in healthy humans (N = 93). Food intake control was assessed for each participant using a revised version of the original Three Factor Eating Questionnaire (Stunkard & Messick, 1985) called the TFEQ-R18-V2 (Cappelleri et al., 2009), which discriminates between cognitive restraint, uncontrolled eating, and emotional eating. We also included additional subtypes of “Restraint-related” and “Disinhibition-related” eating behaviors which have been suggested by others (Bond et al., 2001, Westenhoefer et al., 1999). Individual differences in memory inhibition and episodic memory were assessed using a well-established, objective measure known as the Retrieval Practice (RP) (Anderson, Bjork, & Bjork, 1994). The RP paradigm includes both an episodic recall component (in which participants memorize a subset of word pairs), and a memory inhibitory component (a measurable amount of 'forgetting' that occurs for a subset of word pairs). Thus, the task allows us to measure the magnitude of memory inhibition in all subjects, and to relate the magnitude of that inhibitory effect to individual differences in disinhibited and restrained eating styles. We can also examine how individual differences in episodic recall relate to these eating behavior subtypes. We anticipated that disinhibitory tendencies towards eating behavior would be related to weaker memory inhibition and lower episodic recall, consistent with existing evidence linking impaired food intake control with deficits in memory control.
Section snippets
Study overview
Ninety-three (N = 93) adult subjects attended a single laboratory session where we assessed memory performance (RP Paradigm), eating behaviors (TFEQ), body composition (% adiposity via BODPOD), and energy and macronutrient intake. A priori hypothesized relationships between memory performance and uncontrolled eating were tested using multiple hierarchical regression analyses. Dietary intake and body composition, which were collected as part of a larger ongoing study examining links between diet
Results
Repeated measures ANOVA with a Greenhouse-Geisser correction confirmed that the memory task was effective in producing retrieval induced forgetting. As shown in Fig. 1, participants recalled fewer items from the RP- condition (the ‘inhibition’ condition) compared to the NP control condition (Main effect of Condition, F(1.844, 169.617) = 318.88, p < 0.001, ηp2 = 0.78), indicating retrieval induced forgetting. Participants also recalled nearly all of the RP + items, indicating good episodic
Discussion
Although deficits in behavioral inhibition have been studied as risk factors for uncontrolled eating (Bartholdy et al., 2016), studies examining the relationship between memory inhibition and eating behavior in humans are lacking. Further, although episodic memory has been implicated as a contributor to meal size, hunger, and overall intake (Higgs, 2016), few studies have examined how individual differences in general episodic recall relate to eating behavior in healthy (i.e., non-amnesic)
Conclusion
This study is one of the few to directly examine whether deficits in memory inhibition contribute to overeating in humans. Although our results did not reveal strong evidence that uncontrolled eating is mediated by memory inhibitory deficits, we did uncover a novel relationship between food intake control and episodic recall ability that has not been reported previously-- across several diagnostic eating behavior instruments, susceptibilities to overeat were associated with reductions in
Authors contributions
AM, TD, and MM designed the study; AM and MM conducted the research; AM analyzed the data and wrote the manuscript.
Acknowledgements
All authors have read and approved the manuscript as submitted. All authors declare no conflict of interest. This research was funded by the National Institutes of Health (P01HD052112-6; R01DK075862).
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2022, AppetiteCitation Excerpt :This result has now been replicated several times across several laboratories (Higgs, Williamson, & Attwood, 2008; Szypula, Ahern, & Cheke, 2020). Martin, Davidson, and McCrory (2018) examined how natural variations in memory inhibitory control and episodic memory relate to individual differences in food intake control in healthy individuals. The results showed that participants who reported being more susceptible to overeating (i.e., disinhibitory subtypes) exhibited poorer episodic memory recall.