Variability of enriched environment does not enhance the enrichment effect on food neophobia in rats (Rattus norvegicus)

Highlights

• An enriched environment has a significant impact on reducing food neophobia.

• Environmental variability does not enhance the impact of enrichment.

• The presence of environmental affordances seems sufficient to ensure enrichment.

Abstract

Many studies report differences between animals raised in an enriched environment and those living in standard conditions. Animals reared in enriched conditions demonstrate better memory and learning abilities, increased activity, reduced level of anxiety, etc. However, there is a shortage of studies investigating the impact of environmental variability on animal behaviour, and few studies on this topic focus on animals with different initial anxiety levels.

This study was conducted on laboratory rats. Prior to the experiment, the rats were kept in three types of rearing conditions: an enriched stable environment; an enriched variable environment; and in standard laboratory conditions. The environment was enriched by providing a cognitively and physically stimulating living space. The variability of the environment involved altering the arrangement of the enriching objects on a daily basis. The level of reaction to food novelty was measured with a food neophobia test.

The study demonstrates that an enriched environment has a significant impact on reducing food neophobia. However, our findings suggest that the variability of the environment is not necessary and does not enhance the positive impact of enrichment on these aspects of behaviour.

Introduction

Numerous studies show that animals living in a complex and stimulating environment perform better in behavioural tasks e.g. learning tests (see Gardner et al., 1975; Hebb, 1946; Mohammed et al., 1990; Schrijver et al., 2002), engage in exploration more often and demonstrate a lower level of anxiety (e.g., Gardner et al., 1975; Genaro and Schmidek, 2001; Huck and Price, 1975). What is more, the complexity of the environment is related to an increased intensity of novelty-seeking behaviour (Fernandez-Teruel et al., 1997) and increased activity, while the level of anxiety is reduced (Benaroya‐Milshtein et al., 2004). The changes observed in behaviour are also linked to numerous changes in the brain (e.g., Baroncelli et al., 2010; Kolb and Whishaw, 1998; Lewis, 2004; Rosenzweig and Bennett, 1996) which occur not only in young individuals but in adults as well (e.g., Frick and Fernandez, 2003). These stimulating properties of the environment may contribute to the reversal of cognitive and emotional impairments (e.g., Dahlqvist et al., 2004; Francis et al., 2002; Jankowsky et al., 2005).

In laboratory settings, a stimulating and complex environment is created by enriching the living space with additional objects (wooden blocks, spinning wheels, houses, variable bedding) and more opportunities for social contact (e.g., Bloomsmith et al., 1991; Newberry, 1995). This kind of environmental enrichment results in a larger scope of affordances of the environment (for affordances, see Gibson, 2014; Rietveld and Kiverstein, 2014) by providing the animal with cognitive, physical and social stimuli enabling spontaneous exploration (Baroncelli et al., 2010). The higher the number of objects, the more affordances are available. It is also reasonable to expect that the same object may create new affordances when rearranged spatially or modified in terms of their properties.

In a typical experiment, the configuration of enriching objects remains relatively constant. There is a possibility for changes resulting from an animal’s activity, such as gnawing, carrying objects, exploiting the running wheels, etc. However, this kind of environmental changeability is not imposed by the experimental design or procedure. It should be noted that this kind of manipulation has relatively low ecological validity, as wild animals inhabit environments of different degrees of variability and encounter a wider range of environmental stimuli. It may therefore be hypothesized that environmental variability has a significant impact on the development of the nervous system and animal behaviour.

The impact of environmental variability on animal behaviour is also observed in the context of food-related behaviour, in particular food neophobia. Food neophobia (caution when encountering unfamiliar food – Barnett, 1958, 2009; Pliner and Hobden, 1992) is present in many species (for example, see Addessi et al., 2004; Barnett, 1958; Bryan, 1987; Launchbaugh et al., 1997; Pliner and Hobden, 1992). It occurs mainly in omnivores, which need to distinguish between edible novel food and inedible novel food (generalist’s dilemma - Rozin, 2000). Food neophobia manifests itself in the initial avoidance of novel food, followed by progressive food sampling (Barnett, 2009). If the new food does not evoke adverse bodily symptoms, its intake increases (Barnett, 2009; Mitchell, 1976). Contact with novel food elicits caution, but also an exploratory reaction towards the unfamiliar object (Hebb, 1946). One may discern two components of the reaction to food novelty, which comprises two steps: first, the animal has to overcome the hesitancy towards the novelty of the specific object (general neophobia) and then assess the quality and safety of the new food (Modlinska and Stryjek, 2016; Modlinska et al., 2015).

However, it is assumed that rats inhabiting highly variable environments often exhibit lower general neophobia and a relative absence of food neophobia (Boice, 1971; Barnett, 2005). For example, food neophobia seems to be absent in rats inhabiting landfill sites – an environment subject to frequent changes and frequent occurrence of novelty (Barnett, 2005; Boice, 1971). It may be hypothesised that inhabiting, from an early age, an environment which is not only rich in stimuli but also subject to frequent change (including change of the types of food available) will lower an animal’s neophobia threshold and allow it to consume foods with unknown properties (cf. Modlinska and Stryjek, 2016). In laboratory settings, researchers can simulate these ‘landfill site’ conditions by introducing the rats to a highly enriched and variable environment. This makes it possible to examine whether the anticipated decrease in food neophobia results from the complexity of the environment (which has a significant impact on behaviour in general) or whether it is also due to the variability of that environment.

Although a large number of studies show that living in a complex environment reduces state anxiety and attenuates stress responses in different contexts (e.g. Benaroya‐Milshtein et al., 2004; Goes et al., 2015; Harris et al., 2009; Klein et al., 1994; Ravenelle et al., 2013), the significance of environmental variability in this process is yet to be determined. However, we can hypothesise that if the beneficial effect of environmental enrichment is achieved by means of a complex stimulation of different regions of the brain, the variability of an enriched environment may trigger an even stronger positive response. On the other hand, the unpredictability of these changes and the lack of control over the surroundings may trigger a stress response (LaDage, 2015) and, in the long term, lead to an increase in general anxiety. It is also possible that constant presence of stimuli resulting from environmental variability may moderate emotional reactivity to novelty (Staddon, 2016, p. 204; Tarou and Bashaw, 2007).

The impact of environmental enrichment and its variability on emotional reactivity is also relevant in the context of food neophobia. Some studies suggest that there is a correlation between food neophobia and state anxiety, with individuals with higher state anxiety being more food neophobic (Galloway et al., 2003; Pliner and Hobden, 1992; Pliner and Salvy, 2006). These findings are supported by studies on animals involving the use of anxiolytic drugs (e.g. Cooper and McClelland, 1980; Johnson, 1978; Shephard and Estall, 1984). Therefore, the possible impact of the environment on food neophobia may be mediated by a reduction in anxiety levels.

In view of the above, we would like to put forward the following hypotheses. The first hypothesis is that environmental enrichment will reduce neophobic reactions to novel food in all groups of animals, as it generally has a beneficial effect on anxiety-like behaviour and reduction in stress response (e.g. Benaroya‐Milshtein et al., 2004). We expect that the animals from enriched conditions will limit food intake and will increase eating latency to lesser extent than the animals form standard conditions. The second hypothesis states that the variability of the environment will have a deeper, positive impact on food neophobia, as predicted by Boice (1971) and Barnett (2005), as well as stems from our previous observations (Modlinska and Stryjek, 2016). We predict that rats from the variable enriched environment will express fewer neophobic symptoms than the animals from the stable enriched environment. To test these hypotheses, we conducted food neophobia tests (Modlinska et al., 2015) on rat groups kept in three types of rearing conditions. The first group was reared in an enriched stable environment. Enrichment was ensured by providing the animals with a spacious pen, complex social opportunities and various objects placed inside the pen. The second group in an enriched but constantly changing environment. The changeability of the environment was implemented by changing the location and configuration of the objects inside the pen as well as by introducing small amounts of variable foods. The third group was reared under standard laboratory conditions (control group).