Testing experience and environmental enrichment potentiated open-field habituation and grooming behaviour in rats

doi:10.1016/j.anbehav.2018.01.018

Animal Behaviour

Volume 137, March 2018, Pages 225-235

https://doi.org/10.1016/j.anbehav.2018.01.018 Get rights and content

Highlights

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We studied the emergence of grooming in the context of open-field tests.
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Body licking was enhanced concomitantly with habituation in enriched rats.
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Increased testing experience promoted body licking in nonenriched rats.
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Grooming sequences that included body licking were increased by habituation.
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Some grooming subtypes seem to be involved in emotional de-arousal.

In laboratory rats, one of the most used paradigms to assess habituation to novelty is the open-field test. Environmental enrichment has proved to be a reliable way to enhance open-field test habituation. Experiment 1, therefore, was designed to test whether grooming behaviour in the open-field test increases concomitantly with the habituation of exploratory behaviours (locomotion and rearing behaviour, an alert upright posture). To this aim, after a baseline measure, rats were raised in environmentally enriched and standard housing conditions and then tested 30 and 60 days later. As some grooming subtypes are differentially displayed in the open-field test, we hypothesized that only the grooming subtype that included longer and more complex sequences (e.g. body licking) would increase with habituation. We found that environmental enrichment enhanced short-term (within days) and long-term (between days) open-field test habituation, and increased grooming, particularly body licking. To provide evidence that grooming in the open-field test is part of the habituation process and not a by-product of environmental enrichment, habituation was promoted by exposing a different group of rats that had been reared in standard housing to four consecutive open-field tests in experiment 2. We supposed that the diminution of exploratory open-field test behaviours would be accompanied by an increase in body licking. We found that as locomotion and rearing behaviour decreased, body licking increased gradually both within and between days, suggesting that the appearance of more complex and longer grooming sequences are part of a de-arousal inhibition system subserving novelty habituation. A detailed analysis of grooming, therefore, may provide information about the emotional state of the rat that cannot otherwise be obtained from assessing exploratory activity.

Section snippets

Animals

In experiment 1, we used 60 male Sprague–Dawley rats (21 days old at arrival) obtained from LEBi facilities (University of Costa Rica, San José). Animals were housed with their littermates in transparent, polycarbonate standard cages (56 × 35 × 20 cm) in a colony room with a 12:12 h light:dark cycle (on at 06:00 hours), a temperature of 25.5 °C (±4.5 °C) and 10 air cycles per hour during 1 week for acclimatization. Food and water was provided ad libitum and refilled twice per week during bedding

Experiment 1: EE Potentiated Habituation in the OFT and Increased Type 3 Grooming

As expected, during baseline, no group differences in locomotion (F_1,50 = 0.36, P = 0.55, η_p² = 0.01), rearing (F_1,50 = 0.42, P = 0.52, η_p² = 0.01) or grooming (F_1,50 = 2.88, P = 0.1, η_p² = 0.05) were observed (Fig. 1a–c). However, all animals showed a progressive reduction in time spent in locomotion (F_{6.44, 322.17} = 108.90, P = 0.001, η_p² = 0.68) and rearing (F_6.93,346.67 = 29.30, P = 0.001, η_p² = 0.37), and a progressive increase in time spent grooming (F_{5.81, 290.54} = 2.46, P = 0.03, η_p² = 0.05) throughout the testing period (

Discussion

At the behavioural level, habituation is normally inferred when responses progressively decline as a consequence of prolonged or repeated exposure to stimuli (Groves and Thompson, 1970, Poon and Young, 2006). In the context of habituation to novelty and mild stress in rats (i.e. OFT), limited progress has been made on describing the behavioural shift from active exploratory and defensive responses to other behavioural responses; that is, what behaviours progressively emerge while habituation is

Acknowledgments

This research was partially supported by the projects 837-B7-603, 837-B5-184, 837-B5-185 and 723-B4-192, Vice-Rectory of Research, University of Costa Rica. This work was awarded with the Support Found for Final Graduation Work, Vice-Rectory of Research, University of Costa Rica, and also with the grant Young Researcher in Psychology, Institute for Psychological Research, University of Costa Rica.

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Citation Excerpt :
The OFT is used to assess the emotional (Heredia et al., 2014) and psychomotor reactivity of rodents (Etaee et al., 2019), based on conflicting propensities to explore their surroundings and avoid open areas (Kraeuter et al., 2019; Wu et al., 2022). Animals' distance traveled in the OFT is a measurement of locomotor activity (Ortman et al., 2021) while the percentage of time spent in the central area, rearing and defecation are often used as parameters for anxiety-like behavior in the OFT (Kameyama et al., 1980; Lepicard et al., 2000; Rojas-Carvajal et al., 2018; Sousa et al., 2006). Repeated testing of subjects in various behavioral experiments is often required to reduce variability of data and, more importantly, to assess the effect of pharmacological treatments (Maggi et al., 2004).
The open field test (OFT) is a commonly used protocol to measure anxiety-like behaviors in rodents. Exploration in the central area of the open field and rearing frequency are often readouts of anxiety measurement. However, concerns about carry-over effects associated with repeated assessments limit its application, with the underlying mechanisms of this phenomenon still to be fully described. Here, we showed that repeated OFTs in the same mice led to reductions in the percentage of time spent in the central area and frequency of rearing. This effect reduced with an increase in the intervals between test. The decay caused by repeated OFTs was due to habituation, rather than frequent handling of the experimenter, since novel environments could prevent decay from repeated OFTs. Our results also indicated that tactile cues of the environment played important roles in the habituation of repeated OFTs. Furthermore, the decay of central area activity and rearing behavior during repeated OFTs would be blocked if the hippocampal CA1 was lesioned, suggesting that CA1 is a crucial region for habituation of the OFT in mice. Taken together, our study uncovers the important roles of tactile cues and hippocampal CA1 during repeated OFTs in mice.
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Testing experience and environmental enrichment potentiated open-field habituation and grooming behaviour in rats

Highlights

Section snippets

Animals

Experiment 1: EE Potentiated Habituation in the OFT and Increased Type 3 Grooming

Discussion

Acknowledgments

Behavioural Brain Research

Animal Behaviour

Neurobiology of Learning and Memory

Neuroscience & Biobehavioral Reviews

Neuropharmacology

Neuroscience Letters

Behavioural Brain Research

Hormones and Behavior

Animal Behaviour

Behavioural Brain Research

Behavioural Brain Research

Developmental Brain Research

Animal Behaviour

Pharmacology, Biochemistry, and Behavior

Hormones and Behavior

Cell

Pharmacology, Biochemistry, and Behavior

Brain Research Bulletin

Behavioral and Neural Biology

Journal of Neuroscience Methods

Neuroscience & Biobehavioral Reviews

Brain Research

Pharmacology, Biochemistry, and Behavior

Behavioural Brain Research

Behavioural Brain Research

Animal Behaviour

Animal Behaviour

Neurobiology of Learning and Memory

Animal Behaviour

Developmental Brain Research

Behavioural Brain Research

Neuroscience

Brain Research

Neuroscience & Biobehavioral Reviews

Physiology & Behavior

Physiology & Behavior

Pharmacology, Biochemistry, and Behavior

Behavioural Brain Research

Neuroscience

Animal Behaviour

Progress in Neurobiology

Biological Psychiatry