Elsevier

Appetite

Volume 66, 1 July 2013, Pages 10-19
Appetite

Research report
Within- and between-session variety effects in a food-seeking habituation paradigm

https://doi.org/10.1016/j.appet.2013.01.025Get rights and content

Abstract

Appetitive behavior is stronger when organisms are given a variety of foods than when they are repeatedly given the same food (the variety effect). Two experiments examined the variety effect in an operant food-seeking task. In both experiments, rats received a 45-mg food pellet for every 4th lever press over a series of daily 30-min sessions. The rats responded at a high rate early in the session, but the rate declined systematically over time within the session. In Experiment 1, alternating unpredictably between grain and sucrose pellets caused a higher level of responding, and a slower within-session decline in responding, than presenting either type of pellet consistently. In groups receiving one pellet consistently, a switch to the alternate pellet caused lawful changes in response rate that reflected both habituation and incentive contrast processes. In Experiment 2, an experimental group received grain only and sucrose only in daily alternating sessions. In sucrose sessions, they responded more than controls that always received either sucrose or grain (a type of variety effect); in grain sessions, they responded less than the controls. The results indicated a within-session variety effect that was controlled by habituation processes and a between-session variety effect that was controlled by incentive contrast. Both types of processes can come into play when organisms are exposed to food variety.

Highlights

► Rats habituated to grain and/or sucrose pellets as they worked for them daily in an operant task. ► A mix of the two pellets motivated more responding than did either pellet alone. ► Manipulated within sessions, food variety slowed down the short-term habituation to food. ► Manipulated between sessions, variety created incentive contrast effects.

Introduction

Food consumption is higher when the meal or diet includes a variety of foods instead of a single food (e.g., Raynor & Epstein, 2001). This variety effect has been demonstrated in both humans and animals, and is one of many factors that might influence eating and overeating. One explanation of the variety effect is that exposure to a mixture of foods might retard the organism’s habituation to food. When organisms are repeatedly given the same food, consumption or instrumental responding for it decreases (e.g., Epstein, Temple, Roemmich, & Bouton, 2009). Exposure to different foods might slow the habituation process. For example, Temple, Giacomelli, Roemmich, and Epstein (2008) found that food variety influenced the rate of habituation in children engaged in a food-seeking task. Children received food rewards for playing a simple video game. When the food varied from occasion to occasion, the decline in response rate observed within a 30-min test session was slower than when the food was never varied. Similar results have been shown with adults (Myers Ernst & Epstein, 2002). In addition to demonstrating the influence of variety on food habituation, these studies, as well as others, suggest that habituation processes influence motivated food-seeking, that is, instrumental (operant) behavior that is reinforced by food.

Several well-known features of habituation could contribute to the variety effect. First, habituation is “stimulus-specific”; responding might recover from habituation to some extent whenever the food is changed (e.g., Epstein et al., 2003). Second, repeatedly changing the food might repeatedly cause dishabituation (e.g., Epstein, Rodefer, Wisniewski, & Caggiula, 1992), the recovery of responding that occurs to an habituated stimulus when another stimulus is presented. Third, presenting a variety of foods would increase the interval between successive presentations of the same food. Given stimulus-specificity, this might slow down the habituation of responding to a food, because the rate of habituation is generally thought to decrease by increasing the spacing between trials (e.g., Rankin et al., 2009). By any or all of these mechanisms, food variety might maintain appetite by slowing down the trial-to-trial habituation to food.

As in humans, food-seeking in animals may be influenced by food habituation. For example, many experiments have shown that food-reinforced operant behavior (e.g., lever pressing) can systematically decline within an experimental session (e.g., McSweeney et al., 1996, McSweeney and Murphy, 2009, McSweeney and Swindell, 1999). McSweeney and colleagues have presented evidence to suggest that the decline can be due at least partly to habituation to the reinforcer. However, the variety effect has received relatively little attention in animal instrumental food habituation paradigms. McSweeney, Murphy, and Kowal (2004) found that varying the duration of access to a food reinforcer can slow down the habituation of operant responding in pigeons and rats. But we know of only one experiment that studied the effects of qualitative variation in the appetitive reinforcer on habituation in an instrumental task (Melville, Rue, Rybiski, & Weatherly, 1997, Experiment 1). In that experiment, rats were reinforced for lever pressing with a grape flavored liquid. Variety was manipulated by substituting one of three pellet reinforcers (each a random third of the time) for the liquid; different groups received pellets on different percentages of the occasions. Although “variety” manipulated this way slowed the rate of habituation, the result is equally consistent with the possibility that the food pellets were merely more reinforcing than the grape solution they replaced. There is surprisingly little unambiguous evidence of the variety effect in animal food-seeking habituation paradigms.

The present experiments therefore studied the effects of variety on habituation in an operant learning task in rats. They extended a procedure introduced by Aoyama and McSweeney (2001). Over a series of daily 30-min sessions, the rats received a 45-mg food pellet for every fourth lever-press response (a Fixed Ratio [FR] 4 reinforcement schedule). As reported by Aoyama and McSweeney, the rate of lever pressing at the start of each session was very rapid, but declined systematically over time within the session. Although several factors could contribute to that decline (e.g., fatigue and/or satiation), a role for habituation was suggested by the fact that several dishabituating events (e.g., withdrawing the lever from the chamber for 3 min) introduced in the middle of the session increased the rate of responding subsequently. We reasoned that if the within-session decline were due to food habituation, then it should also be slowed by providing a mixture of different food pellets—a variety effect. We also reasoned that substituting an alternative pellet for the habituated pellet in the middle of the session should lead to an increase in responding—a stimulus-specificity effect. Although stimulus-specificity has been shown with the habituation of food consumption in animals (e.g., Swithers & Martinson, 1998), we are not aware of studies that have demonstrated it in a food-seeking (operant) task.

Section snippets

Experiment 1

The first experiment examined variety and stimulus-specificity effects in the Aoyama and McSweeney preparation. Three groups of rats were allowed to lever press on an FR-4 schedule over a series of daily 30-min sessions. During each session, an experimental (variety) group received an unpredictable mixture of 45-mg sucrose and grain-based pellets for lever pressing. Two control groups received only grain and only sucrose pellets in alternating sessions. One group received grain pellets on

Subjects

Thirty-two naive female Wistar rats purchased from Charles River Laboratories (St. Constance, Quebec) participated in the present study. They were between 75 and 90 days old at the start of the experiment and were individually housed in suspended wire mesh cages in a room maintained on a 16: 8-h light: dark cycle. Throughout the experiment, the rats were food deprived to 80% of their initial body weights via small daily feedings of the maintenance chow, P500 Prolab RMH 3000 (PMI Nutrition

Within-session patterns of food-seeking

The results of the acquisition phase are presented in Fig. 1, which shows responding for each group over time in the session (x axis) over successive 2-day blocks in Context A (separate panels). The groups rapidly acquired the food-seeking response, and quickly revealed the pattern of decreasing responding within each session that was reported by Aoyama and McSweeney (2001). Although responding for sucrose pellets was eventually higher than that for grain pellets, responding for the mixture

Discussion

The experiment produced several notable results. Consistent with Aoyama and McSweeney (2001), the rats began each session with a high rate of lever pressing which then declined systematically over the remainder of the session. The within-session decrease in response rate was evident early in training, e.g., on the first 2-day block in Context A (Fig. 1).

Several other results point to the role of within-session habituation to the pellet reinforcer. First, throughout acquisition there was a clear

Experiment 2

Experiment 2 compared responding in rats given alternating sessions with grain and sucrose pellets with groups that received grain- or sucrose-only every day. If mixing the pellet types between sessions creates a positive contrast effect, then the alternating group should respond more for sucrose pellets than the group that received sucrose daily. If it creates a negative contrast effect, then the alternating group should respond less for the grain pellets than the group that received them

Subjects

The subjects were 32 naïve female Wistar rats purchased from the same vendor as those in the previous experiment. They were maintained under the same conditions.

Apparatus

The apparatus was the same as that in Experiment 1.

Procedure

Daily 30-min sessions, alternating between Contexts A and B, were run in a manner identical to those in Experiment 1. Group Grain (n = 10) received grain pellets in both Contexts A and B. Group Sucrose (n = 10) received sucrose pellets in both contexts. Group Mix (n = 12) received grain

Within-session patterns of food-seeking

The results are presented in Fig. 5, which shows responding of the groups over two-session blocks of training in each context. The left and right columns correspond to sessions in Contexts A and B, where Group Mix received sucrose and grain pellets, respectively. The data were analyzed with a Group (Grain vs. Sucrose vs. Mix) × Context (A or B) × Time Bin (30) × Session Block (4) ANOVA. There was no main effect of Group, F < 1, however, all other main effects and interactions were significant.

Discussion

As in Experiment 1, a reliable decreasing pattern of responding over minutes in each session rapidly emerged (Aoyama & McSweeney, 2001). Responding for either sucrose or grain pellets throughout training produced a stable pattern of responding within and between sessions. However, alternating between sucrose and grain pellets over sessions (Group Mix) led to more responding for sucrose and less responding for grain. These effects are consistent with between-session positive and negative

General discussion

In the present experiments, the rate of lever pressing for grain or sucrose pellets declined rapidly within daily 30-min sessions, as reported by Aoyama and McSweeney (2001). However, there was evidence that the rate decline occurred more slowly when the rats received pellets that varied unpredictably between grain and sucrose (Experiment 1). This new demonstration of the variety effect suggests that the within-session decrease in lever pressing rate that otherwise occurred was not merely a

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Acknowledgement: This research was supported by Grants 9RO1 DA033123 from the National Institute on Drug Abuse to MEB and 1U01 DK088380 from the National Institute of Diabetes and Digestive and Kidney Diseases to LEH. The participation of Samuel León (who visited the University of Vermont from the University of Jaén) was enabled by Projects SEJ2007-267053/PSIC and BES-2008-003634 from the Spanish Ministry of Science and Innovation.

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