Intermittent feeding alters sensitivity to changes in reward value
Introduction
To optimize food-related behavior, both animals and humans must integrate knowledge regarding food expectation (that is, which actions lead to which food outcomes) with the current desirability or motivational value of those foods (Balleine and Dickinson, 1998, Balleine, 1992, Dickinson and Balleine, 1994). Successful integration of these elements ensures that food-seeking behaviors are goal-directed, thereby allowing the subject to flexibly adapt their behavior according to changes in their motivational state as well as environmental fluctuations.
An obesogenic diet can lead to a range of cognitive impairments, including deficits in food-related behaviors (Furlong et al., 2014, Kendig et al., 2013, Morris et al., 2015, Reichelt et al., 2016, Reichelt et al., 2014, Reichelt et al., 2015). For example, the consumption of palatable foods is associated with the loss of goal-directed control over food-seeking behavior (Furlong et al., 2014, Kendig et al., 2013). Corbit and colleagues have demonstrated that rats given long-term, intermittent access to a 10% sucrose solution (Kendig et al., 2013) or sweetened condensed milk (Furlong et al., 2014) fail to selectively reduce their responding for a food reward following outcome devaluation. Sensory-specific satiety (Rolls, 1986, Rolls et al., 1981), an important factor in food choice and meal duration (Hetherington & Rolls, 1996), is also disrupted in rats fed a high fat, high sugar diet (Reichelt et al., 2014). In the latter study, following ad libitum consumption of one food, rats fed a control diet showed sensory-specific satiety and rejected the pre-fed food while readily consuming a second food with distinct sensory properties. In contrast, rats fed a high fat, high sugar diet did not reject the pre-fed food and consumption of this food was similar to that of a non pre-fed food (Reichelt et al., 2014).
In addition to the consumption of high fat, high sugar diets, eating patterns alone can have a considerable impact on food-related behavior. Animal models of binge-like eating in humans show that intermittent feeding causes a range of abnormalities in consummatory behavior. For example, repeated cycles of restriction and refeeding of maintenance chow promote binge-like eating that persists after the cessation of restriction-refeeding cycles (Hagan & Moss, 1997) and, moreover, binge-eating prone rats subjected to restriction-refeeding cycles of chow and palatable food are more likely to tolerate foot-shock in order to gain access to palatable foods than non-cycled rats (Oswald, Murdaugh, King, & Boggiano, 2011). Sensory-specific satiety is also disrupted following binge-like feeding in rats (Ahn & Phillips, 2012). That is, rats exposed to a 30-day restriction-refeeding cycle, consisting in four days of restricted access followed by two days of ad libitum food, failed to reject a food recently eaten to satiety whereas rats maintained on food restriction consumed less of the prefed food compared to a novel food (Ahn & Phillips, 2012). Taken together, these studies provide clear evidence that intermittent feeding patterns can have dramatic effects on subsequent consummatory behavior. However, it remains to be determined if binge feeding, like high fat or high sugar diets, also promotes habitual food-seeking actions, which could have important consequences for food choices and decision making in general.
Following the work of Ahn and Phillips (2012), we assessed the impact of repeated cycles of restricted and unrestricted chow intake on sensory-specific satiety and goal-directed behavior in rats. Moderately food deprived rats were first trained to perform two actions for two different food rewards. Then, rats were either maintained on chow restriction or they were switched to an intermittent chow feeding schedule for one month. All rats were then food restricted prior to behavioral testing. We assessed goal-directed control, using specific satiety-induced outcome devaluation, followed by a simultaneous or sequential test of sensory-specific satiety.
Section snippets
Subjects
Forty-six experimentally naïve male outbred Long Evans rats (320–400 g) obtained from Monash University Animal Research Platform served as subjects. They were housed in plastic boxes (2–3 rats per box) located in a climate controlled colony room and were maintained on a 12 h light/dark cycle. Five days before the start of the behavioral procedures, the rats were handled daily and put on a food restriction schedule to maintain them at 85–90% of their ad libitum feeding weight. All experimental
Results
Lever pressing performance increased across instrumental training and did not differ between the rats allocated to each group (Fig. 2, left panel). Statistical analyses indicated a significant effect of session (F(1,44) = 312.60, p < 0.05), but no effect of group (F(1,44) = 1.58, p > 0.05) or significant session by group interaction (all F values < 2.45, p > 0.05).
Fig. 1 shows the percent weight change (top) and the body weight (bottom) for each group across the period of restriction-refeeding
Discussion
Our results indicate that intermittent feeding schedules can impair goal-directed responding for a food reward. Following devaluation of one of the rewards, rats maintained on food restriction selectively reduced their performance of the action that gained access to the now food, whereas rats that had experienced cyclic feeding did not. The failure to show goal-directed control did not result from insensitivity to satiety-induced outcome devaluation. When offered a choice between the devalued
Acknowledgements
This work was supported by a Laureate Fellowship from the Australian Research Council (ARC #FL0992409) awarded to BWB.
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Present address: CNRS, Institut de Neurosciences Cognitives et Intégratives d’Aquitaine, UMR 5287, Bordeaux 33076, France
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Present address: Neuroscience Research Australia, Sydney 2031, Australia
- 3
Present address: Parkwood Institute, St Joseph's Health Care, London, ON N6C OA7, Canada
- 4
Present address: School of Psychology, University of New South Wales, Sydney 2052, Australia