Elsevier

Physiology & Behavior

Volume 118, 13 June 2013, Pages 45-51
Physiology & Behavior

Contextual control of flavor neophobia

https://doi.org/10.1016/j.physbeh.2013.05.020Get rights and content

Highlights

  • Neophobia habituation interacts with context novelty/familiarity.

  • Dopamine levels affect to the neophobia habituation by context familiarity interaction.

  • Exploring a context without aversive consequences generates a safe memory trace of such context.

  • A context safe memory trace increases consumption of any flavor presented in its presence.

Abstract

The role of context in the retrieval of learned information has been widely analyzed in the associative learning domain. However, evidence about the effect of context on flavor memory retrieval is more limited. We have carried out four experiments with rats testing for possible interactions between neophobia habituation and the context in which flavors are presented, by manipulating prior experience with contexts. Our results point to the relevance of context familiarity for the establishment and recovery of a safe taste memory trace. More specifically, the use of the animals' home cages as experimental context favored neophobia habituation (Experiments 1A and 2), reduced dopamine levels induced by administration of the dopamine D1-like receptor antagonist SCH-23390 disrupted neophobia habituation when tested in presence of a new context (Experiment 1B), and testing in the animal's home cage increases the amount of flavor consumed, even when such flavor had a previous history of aversive conditioning (Experiment 3). We propose that exploring context without aversive consequences generates a safe memory trace of such context that becomes in the basis of increased flavor consumption.

Introduction

Any alteration in environmental conditions induces different responses that can change in intensity, duration or functionality depending on the stimulus characteristics and the novelty produced by its presentation or withdrawal. Thus, for instance, a new light or sound of medium intensity generates a set of orienting responses that allows to the animal to explore and process the stimulus more accurately. When the stimulus is presented repeatedly without consequence, the orienting responses gradually decline as the stimulus loses its novelty [1].

A particularly interesting case is that related to the responses that follow the tasting of a new flavor, because in this situation the potential value of the stimulus for the animal's survival is very high [2], [3]. As described by Bermudez-Rattoni [4] animal survival depends, among other factors, on their capacity to differentiate those foods that are edible from those that have toxic components. Animals are highly adaptive in that when they come into contact with a new flavor there appears to be an unconditioned response of rejection that results in minimum consumption of the substance with that flavor, which is known as neophobia [5]. When a period of time has elapsed since the flavored item was consumed, and as the flavor memory trace is consolidated as a “safe” stimulus (that is, a stimulus without aversive consequences), consumption progressively increases, a phenomenon termed habituation of neophobia [6]. Conversely, if flavor consumption is followed by any kind of negative consequence an aversive conditioning develops [7] that is behaviorally expressed in a sharp reduction of flavor ingestion. Therefore, as a function of the consequences that follow flavor ingestion, a flavor memory trace will be established that is either safe, favoring an increase in consumption of the flavor in future encounters, or aversive, which will result in a reduction or even the complete rejection of flavor consumption [4], [8].

This proposal is compatible with the learned safety theory [9], [10], but contrasts with other general interpretations of the habituation process that propose mechanisms either associative or non-associative. Thus, from a non-associative perspective, the Dual-Process Theory proposed by Groves and Thompson [11] suggests that repeated presentations of a stimulus induce two independent processes in the central nervous system that interact to produce a response. The first process takes place in the stimulus–response pathway and is responsible for the progressive reduction of the response. The second process acts in the state system and gives rise to an increase in response intensity due to sensitization.

An alternative theory of habituation, which has great influence in the analysis of the processes underlying habituation mechanisms, was proposed by Wagner [12], [13]. From his perspective, habituation depends on the association established between the stimulus and the context in which it appears. More specifically, Wagner proposes that, after repeated presentations of the stimulus, the contextual cues will activate a representation of the stimulus in short term memory which will prevent processing of the actual event, resulting in the reduction of the response to the stimulus that characterizes the habituation process.

All the theories mentioned recognize, in a more or less explicit way, the role of context in the habituation process. However, while for Wagner [12], [13] the context is considered an essential element in the associative process that produces habituation, for the Dual-Process Theory of habituation [11], on the other hand, context would have merely the status of a stimulus that is also subjected to habituation after repeated presentations. For the specific case of neophobia habituation, the learned safety theory [9], [10] implies that the context acquires properties as a modulator of the flavor significance by means of its capacity to recover the association between the flavor and the absence of consequences. In fact, there is some evidence showing contextual modulation of neophobia habituation. Thus, a context change, but only if the context is new, induces neophobia recovery [14], [6]. However, when the change involves a familiar context, neophobia habituation remains intact [6].

From a physiological perspective, the involvement of the dopaminergic system in appetitive learning [15] and in the role of context as a learning modulator [16] makes it a possible neurochemical candidate for the development the mentioned context-dependent safe flavor memory trace based in an association between the taste and the absence of aversive consequences. More specifically, previous studies have shown modulation of dopaminergic transmission as a function of the motivational valence and novelty of the stimuli [17]. In particular, it has been observed an increase in dopamine release in the nucleus accumbens (NAc) shell in response to appetitive but not aversive unfamiliar stimuli. It also has been demonstrated the role of dopamine in studies of context modulation of conditioning through a circuit which involves indirect projections from the ventral subiculum to the NAc [16].

The general purpose of the experiments that follow is to evaluate the role played by context familiarity on the development and the recovery of the safe memory trace of the flavor. To this end, we conducted four experiments using contexts that were new or the home cages, to evaluate a possible interaction between neophobia habituation and context novelty or familiarity (Experiment 1A), to evaluate whether dopamine levels differentially affect to the interaction between neophobia habituation and context familiarity (Experiment 1B), to check the role of novelty/familiarity by introducing in the experimental design a previously familiarized context in addition to the home and new environments (Experiment 2), and to analyze whether the intensity of a conditioned response after a taste aversion episode changes as a function of the test context degree of novelty (Experiment 3).

Section snippets

Experiments 1A and 1B

These experiments evaluated possible differences in the process of neophobia habituation as a function of the context (home cages vs. new experimental context) in which flavor is consumed (Experiment 1A) and the effect of dopamine D1-like receptor antagonist administration during saccharin habituation in the presence of the home cage vs. a new experimental context (Experiment 1B).

The available experimental evidence on contextual modulation of neophobia habituation shows that a context change,

Experiment 2

The results of Experiment 1A showed that neophobia habituation proceeded faster when flavor exposure was conducted in the animals' home cages as compared to when it took place in the new experimental cages. This result supports the idea that the home cage context favors the establishment of a safe flavor memory trace [19], [4]. However, the results do not allow us to identify whether the process responsible for the faster neophobia process is related to the mere familiarization that the animals

Experiment 3

The results of the previous experiments seem to indicate that exposing a flavor in a home cage context facilitates the learning of such flavor as “safe”, and that such an effect is based on previous familiarization with the context without consequences by mere pre-exposure. We could thus anticipate that a flavor previously associated with an aversive consequence would be perceived as less aversive if presented at the home cage than if presented in a new context.

To evaluate this possibility we

Discussion

The experimental results revealed that habituation of neophobia proceeds faster when the flavor is repeatedly presented without consequences in the presence of the animals' home cages as compared to the presence of a new experimental context (Experiments 1A and 2), and that neophobia habituation rate evaluated in a new context but not in a familiar context is modulated by dopaminergic activity (Experiment 1B). Finally, the expression of conditioned taste aversion was affected by a context

Acknowledgments

This research was supported by grants from Spanish Ministerio de Economia y Competitividad (PSI2009-7536, and PSI2012-32077), and Junta de Andalucia (SEJ-02618).

The authors wish to thank A. Mena, A. Orgaz, A. Fernandez, and A. Puente for their help in conducting the experiments.

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