Research reportYoung pigs exhibit differential exploratory behavior during novelty preference tasks in response to age, sex, 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.
References (41)
- et al.
Gait analysis in a pre- and post-ischemic stroke biomedical pig model
Physiol. Behav.
(2014) - et al.
The use of pigs in neuroscience: modeling brain disorders
Neurosci. Biobehav. Rev.
(2007) - et al.
Early life iron deficiency impairs spatial cognition in neonatal piglets
J. Nutr. Cogn.
(2012) - et al.
The seeking of novelty and its relation to play
Anim. Behav.
(1991) - et al.
A systematic approach towards developing environmental enrichment for pigs
Appl. Anim. Behav. Sci.
(2003) - et al.
Behavioral responses of domestic pigs and cattle to humans and novel stimuli
Appl. Anim. Behav. Sci.
(1996) - et al.
Objects as enrichment: effects of object exposure time and delay interval on object recognition memory of the domestic pig
Appl. Anim. Behav. Sci.
(2007) - et al.
The effect of the inter-phase delay interval in the spontaneous object recognition test for pigs
Behav. Brain Res.
(2007) - et al.
Behavioral assessment of cognitive function using a translational neonatal piglet model
Brain Behav. Immun.
(2010) - et al.
c-Fos expression correlates with performance on novel object and novel place recognition tests
Brain Res. Bull.
(2015)
Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions
Behav. Brain Res.
Rats and mice share common ethologically relevant parameters of exploratory behavior
Behav. Brain Res.
Effects of pre-weaning exposure to a maze on stress responses in pigs at weaning and on subsequent performance in spatial and fear-related tests
Appl. Anim. Behav. Sci.
Neurotoxic lesions of the perirhinal cortex do not mimic the behavioral effects of fornix transection in the rat
Behav. Brain Res.
Improved behavior, motor, and cognition assessments in neonatal piglets
J. Neurotrauma
Mild traumatic brain injury and diffuse axonal injury in swine
J. Neurotrauma
The pig as a model animal for studying cognition and neurobehavioral disorders
Mol. Funct. Models Neuropsychiatry
The Welfare of Pigs
Early supplementation of phospholipids and gangliosides affects brain and cognitive development in neonatal piglets
J. Nutr.
Moderate perinatal choline deficiency elicits altered physiology and metabolomic profiles in the piglet
PLoS One
Cited by (36)
Pediatric Nutrition: Implications for the Developing Microbiota–Gut–Brain Axis
2024, The Gut-Brain Axis, Second EditionImpaired neurogenesis with reactive astrocytosis in the hippocampus in a porcine model of acquired hydrocephalus
2023, Experimental NeurologyFactors of potential influence on different behavioural tests in fattening pigs
2020, Applied Animal Behaviour ScienceCitation Excerpt :This assumption was supported by Forkman et al (2007): during aging, pigs became less anxious and fearful. Furthermore, older pigs showed more exploratory behaviour than younger ones (Fleming and Dilger, 2017). However, the results of the NOT and HART in this study showed lower latencies and a higher percentage of animals reacting to the object or human positively in younger animals.