Elsevier

Behavioural Brain Research

Volume 321, 15 March 2017, Pages 50-60
Behavioural Brain Research

Research report
Young pigs exhibit differential exploratory behavior during novelty preference tasks in response to age, sex, and delay

https://doi.org/10.1016/j.bbr.2016.12.027Get rights and content

Abstract

Novelty preference paradigms have been widely used to study recognition memory and its neural substrates. The piglet model continues to advance the study of neurodevelopment, and as such, tasks that use novelty preference will serve especially useful due to their translatable nature to humans. However, there has been little use of this behavioral paradigm in the pig, and previous studies using the novel object recognition paradigm in piglets have yielded inconsistent results. The current study was conducted to determine if piglets were capable of displaying a novelty preference. Herein a series of experiments were conducted using novel object recognition or location in 3- and 4-week-old piglets. In the novel object recognition task, piglets were able to discriminate between novel and sample objects after delays of 2 min, 1 h, 1 day, and 2 days (all P < 0.039) at both ages. Performance was sex-dependent, as females could perform both 1- and 2-day delays (P < 0.036) and males could perform the 2-day delay (P = 0.008) but not the 1-day delay (P = 0.347). Furthermore, 4-week-old piglets and females tended to exhibit greater exploratory behavior compared with males. Such performance did not extend to novel location recognition tasks, as piglets were only able to discriminate between novel and sample locations after a short delay (P > 0.046). In conclusion, this study determined that piglets are able to perform the novel object and location recognition tasks at 3-to-4 weeks of age, however performance was dependent on sex, age, and delay.

Introduction

The piglet is increasingly being used as an animal model to investigate brain trauma [1], [2], [3], neuroscience [4], [5], animal welfare [6], pediatric nutrition [7], [8], [9], and toxicology [10]. The piglet is much larger than the rodent, and large sample sizes require relatively greater effort to acquire data compared with rodents. As such, there is a need to develop behavioral tests that are accurate, timely, and require relatively little labor. Novelty preference paradigms have been widely used in humans as well as primate and rodent models to assess recognition memory, spatial memory, discrimination, and other cognitive domains [11], [12], [13], [14], [15]. Specifically, these paradigms have been extensively used in infant research to assess development of memory and perceptual abilities in infants [16], [17], [18], [19], [20]. Thus, the use of such paradigms in animals imparts greater translational value to infant models than most operant based maze training tasks, which are the predominant tasks used. The novel object recognition (NOR) and novel location recognition (NLR) tasks require no operant training and can be used repeatedly on the same experimental unit, making them efficient behavioral tasks to assess recognition memory [14]. Robustly establishing replicable methods to use these tasks will become increasingly necessary as the piglet model gains greater acceptance within the field of neuroscience.

Although there has been some investigation into piglets’ spontaneous preference for novel or familiar objects [21], using novel objects as enrichment [22], or exploration of novel objects [23], [24], to our knowledge, only three experiments have formally investigated NOR in piglets [25], [26], [27], and no experiments have investigated NLR. Research using 12–14-month-old Göttingen minipig boars (i.e., mature, intact male pigs) suggested pigs can remember objects for short delays of 10 min or 1 h, but were unable to do so at a longer delay of 24 h [25], [27]. However, 5-week-old domestic pigs were shown to be capable of remembering objects for longer delays of 3 h or 5 days, but not for a shorter delay of 1 h [26]. Such differences may be accounted for by a range of different genetics, rearing conditions, and testing methodology. These conflicting results have led to the belief that the task may be unsuitable for the pig, and a recent review states that the NOR task “has not yet indisputably proven its relevance in pigs” [28]. Understanding the basic ability of the piglet to perform novelty preference tasks will be crucial in advancing both the field of piglet behavior and cognition, and additionally those fields seeking to use the piglet as a model for investigation.

The present study involves compilation of three individual experiments designed to test the hypothesis that young pigs are capable of displaying a novelty preference at a range of short and long delays in an NOR task, and that performance is modulated by sex and age. Additionally, we tested the hypothesis that piglets are capable of displaying a novelty preference in the NLR task as previous literature has suggested piglets can complete spatial tasks such as the associative 8-arm radial maze and a spatial T-maze [29], [30].

Section snippets

Methods

All animal care and experimental procedures were in compliance with National Research Council Guide for the Care and Use of Laboratory Animal Care and Use Committee and approved by the University of Illinois Urbana-Champaign Institutional Animal Care and Use Committee.

Control trials

One-tailed t-tests revealed that recognition indices for object pairs 1, 2, 4, and 5 were not different from a null preference of 0.50 (object pair 1: n = 14, mean = 0.446 ± 0.0552, P = 0.345; object pair 2: n = 14, mean = 0.424 ± 0.0587, P = 0.217; object pair 4: n = 13, mean = 0.524 ± 0.0523, P = 0.658; object pair 5: n = 14, mean = 0.491 ± 0.0446, P = 0.847) and a Sign test indicated object pair 3 was different from a null preference of 0.50 (object pair 3: n = 12, mean = 0.734 ± 0.0548, P = 0.006) (Fig. 3A). The Friedman test

Discussion

Novelty preference tasks will be pivotal for investigating piglet behavior due to the ease of execution and ability to modulate the design to the experimenters needs. Currently, there have only been three formal investigations into the piglets ability to complete the NOR task, and these have yielded inconsistent results, partly due to differences in animals tested and methodology [25], [26], [27]. The purpose of the present experiments was to identify the delays at which young piglets are

Conclusions

As established, previous research has yielded conflicting results using the NOR task in pigs [25], [26], [27]. The aim of the present experiments was to replicate results from previous work, and elucidate the effects of sex and age on performance of young pigs in the NOR task. Our data suggest that piglets were able to discriminate between novel and sample objects after delays of 2 min, 1 h, 24 h, and 48 h, but recognition of the novel object was dependent on sex. Females were able to display

Funding

This project was supported by Mead Johnson Nutrition and the American Egg Board.

Acknowledgments

The authors would like to thank Dr. Mark Stanton and Dr. Brian Berg for their assistance and advice on experimental design. They would also like to thank Kristen Karkiewicz, Laura Knight, Rachel Clark, and Maryam Bassiri for their assistance with behavioral testing and analysis.

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