Skip to main content

Working and reference memory of pigs (Sus scrofa domesticus) in a holeboard spatial discrimination task: the influence of environmental enrichment

Animal Cognition volume 16, pages 845–850 (2013)Cite this article

Abstract

Interest in cognitive research in pigs is increasing, but little is known about the impact of environmental conditions on pigs’ cognitive capabilities. The present study investigated the effect of environmental enrichment on cognitive performance of pigs in a holeboard spatial task, in which they had to discriminate four baited buckets out of 16. Pigs (n = 32) were either housed in stimulus-poor, barren pens, or in larger pens enriched with rooting substrates. Pigs were subjected to 30 holeboard trials. Both working memory (WM), that is, the ratio (baited visits/total number of (re)visits to baited buckets), and reference memory (RM), that is, the ratio ((re)visits to baited buckets/total number of visits to all buckets), improved over trials. WM scores were higher in pigs from enriched pens than in pigs from barren pens. Housing did not affect RM scores. Personality type of the pigs, as assessed early in life using a backtest, did not affect WM or RM. In conclusion, housing conditions of pigs did not affect reference memory, but environmental enrichment improved working memory of pigs in a spatial discrimination task. Based on the findings of this study, we suggest that cognitive functioning of pigs may be impaired under commonly used housing conditions.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  • Arts JWM, van der Staay FJ, Ekkel ED (2009) Working and reference memory of pigs in the spatial holeboard discrimination task. Behav Brain Res 205:303–306

    PubMed  Article  Google Scholar 

  • Beattie VE, O’Connell NE, Kilpatrick DJ, Moss BW (2000) Influence of environmental enrichment on welfare-related behavioural and physiological parameters in growing pigs. Anim Sci 70:443–450

    Google Scholar 

  • Bolhuis JE, Schouten WGP, De Jong IC, Schrama JW, Cools AR, Wiegant VM (2000) Responses to apomorphine of pigs with different coping characteristics. Psychopharmacol 152:24–30

    Article  CAS  Google Scholar 

  • Bolhuis JE, Parmentier HK, Schouten WGP, Schrama JW, Wiegant VM (2003) Effects of housing and individual coping characteristics on immune responses of pigs. Physiol Behav 9:24–30

    Google Scholar 

  • Bolhuis JE, Schouten WGP, De Leeuw JA, Schrama JW, Wiegant VM (2004) Individual coping characteristics, rearing conditions, and behavioural flexibility in pigs. Behav Brain Res 152:351–360

    PubMed  Article  Google Scholar 

  • Bolhuis JE, Schouten WGP, Schrama JW, Wiegant VM (2005) Behavioural development of pigs with different coping characteristics in barren and substrate-enriched housing conditions. Appl Anim Behav Sci 93:213–228

    Article  Google Scholar 

  • Bolhuis JE, Schouten WGP, Schrama JW, Wiegant VM (2006) Effects of rearing and housing environment on pigs with different coping characteristics. Appl Anim Behav Sci 101:68–85

    Article  Google Scholar 

  • Bolhuis JE, Van den Brand H, Staals S, Gerrits WJJ (2007) Effects of pregelatinized vs. native potato starch on intestinal weight and stomach lesions of pigs housed in barren pens or on straw bedding. Livest Sci 109:104–110

    Article  Google Scholar 

  • Conrad CD (2010) A critical review of chronic stress effects on spatial learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 34:742–755

    PubMed  Article  Google Scholar 

  • De Jong IC, Prelle IT, Van de Burgwal JA, Lambooij E, Korte SM, Blokhuis HJ, Koolhaas JM (2000) Effects of environmental enrichment on behavioral responses to novelty, learning, and memory, and the circadian rhythm to cortisol in growing pigs. Physiol Behav 68:571–578

    PubMed  Article  Google Scholar 

  • Gieling ET, Nordquist RE, van der Staay FJ (2011) Assessing learning and memory in pigs. Anim Cogn 14:151–173

    PubMed  Article  Google Scholar 

  • Gieling ET, Park SY, Nordquist RE, Van der Staay FJ (2012) Cognitive performance of low- and normal-birth-weight piglets in a spatial hole-board discrimination task. Ped Res 71:71–76

    Article  Google Scholar 

  • Held S, Mendl M, Laughlin K, Byrne RW (2002) Cognition studies with pigs: livestock cognition and its implications for production. J Anim Sci 80:E10–E17

    Google Scholar 

  • Inglis IR, Forkman B, Lazarus J (1997) Free food or earned food? A review and fuzzy model of contrafreeloading. Anim Behav 53:1171–1191

    PubMed  Article  Google Scholar 

  • Jansen J, Bolhuis JE, Schouten WGP, Spruijt BM, Wiegant VM (2009) Spatial learning in pigs: effects of environmental enrichment and individual characteristics on behaviour and performance. Anim Cogn 12:303–315

    PubMed  Article  Google Scholar 

  • Kornum BR, Knudsen GM (2011) Cognitive testing of pigs (Sus scrofa) in translational biobehavioral research. Neurosci Biobehav Rev 35:437–451

    PubMed  Article  Google Scholar 

  • Krugers HJ, Douma BRK, Andringa G, Bohus B, Korf J, Luiten PM (1997) Exposure to chronic psychosocial stress and corticosterone in the rat: effects on spatial discrimination learning and hippocampal protein kinase Cγ immunoreactivity. Hippocampus 7:427–436

    PubMed  Article  CAS  Google Scholar 

  • Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L (2005) Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 163:78–90

    PubMed  Article  Google Scholar 

  • Lind BM, Moustgaard A, Jelsing J, Vajta G, Cumming P, Hansen AK (2007) The use of pigs in neuroscience: modeling brain disorders. Neurosci Biobehav Rev 31:728–751

    PubMed  Article  CAS  Google Scholar 

  • Manikandan S, Padma MK, Srikumar R, Parthasarathy NJ, Muthuvel A, Devi SR (2006) Effects of chronic noise stress on spatial memory of rats in relation to neuronal dendritic alteration and free radical-imbalance in hippocampus and medial prefrontal cortex. Neurosci Lett 399:17–22

    PubMed  Article  CAS  Google Scholar 

  • Melotti L, Oostindjer M, Bolhuis JE, Held S, Mendl M (2011) Personality types and environmental enrichment affect aggression at weaning in pigs. Appl Anim Behav Sci 133:144–153

    Article  Google Scholar 

  • Mendl M (1999) Performing under pressure: stress and cognitive function. Appl Anim Behav Sci 65:221–244

    Article  Google Scholar 

  • Oostindjer M, Bolhuis JE, Mendl M, Held S, Gerrits W, Van den Brand H, Kemp B (2010) Effects of environmental enrichment and loose housing of lactating sows on piglet performance before and after weaning. J Anim Sci 88:3554–3562

    PubMed  Article  CAS  Google Scholar 

  • Pearce GP, Paterson AM (1993) The effect of space restriction and provision of toys during rearing on the behaviour, productivity and physiology of male pigs. Appl Anim Behav Sci 36:11–28

    Article  Google Scholar 

  • Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65

    PubMed  Article  CAS  Google Scholar 

  • Schrijver NC, Bahr HI, Weiss IC, Würbel H (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol Biochem Behav 73:209–224

    PubMed  Article  CAS  Google Scholar 

  • Sneddon IA, Beattie VE, Dunne L, Neil W (2000) The effect of environmental enrichment on learning in pigs. Anim Welf 9:373–383

    Google Scholar 

  • Spinka M, Newberry RC, Bekov M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168

    PubMed  Article  CAS  Google Scholar 

  • Staals S, Bolhuis JE, Van den Brand H, Gerrits WJJ (2007) Contribution of a straw bedding to digestible nutrient intake of pigs fed diets based on either native or pregelatinized potato starch. Livest Sci 109:104–107

    Article  Google Scholar 

  • Van der Beek EM, Bolhuis JE, Karman AG, Van Eerdenburg FJCM, Wiegant VM (2000) Housing condition affects the correlation between volume of the dentate gyrus and the cortisol response to stress in pigs. In: Society for neuroscience abstracts, vol 26, part 1. 30th Annual Meeting, New Orleans, p 998 (abstract)

  • Van der Staay FJ, Gieling ET, Pinzón NE, Nordquist RE, Ohl F (2012) The appetitively motivated “cognitive” holeboard: a family of complex spatial discrimination tasks for assessing learning and memory. Neurosci Biobehav Rev 36:379–403

    PubMed  Article  Google Scholar 

  • Yoon T, Okada J, Jung MW, Kim JJ (2008) Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learn Mem 15:97–105

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the assistance of Esther van de Hoek and the personnel of experimental farm ‘De Haar’.

Author information

Authors and Affiliations

  1. Adaptation Physiology Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands

    J. Elizabeth Bolhuis, Marije Oostindjer, Cindy W. F. Hoeks, Elske N. de Haas, Andrea C. Bartels, Monique Ooms & Bas Kemp

  2. Department of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, P.O. Box 5003, 1432, Ås, Norway

    Marije Oostindjer

Authors
  1. J. Elizabeth Bolhuis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marije Oostindjer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cindy W. F. Hoeks
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elske N. de Haas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrea C. Bartels
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Monique Ooms
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bas Kemp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Elizabeth Bolhuis.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Elizabeth Bolhuis, J., Oostindjer, M., Hoeks, C.W.F. et al. Working and reference memory of pigs (Sus scrofa domesticus) in a holeboard spatial discrimination task: the influence of environmental enrichment. Anim Cogn 16, 845–850 (2013). https://doi.org/10.1007/s10071-013-0646-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-013-0646-7

Keywords

  • Spatial learning
  • Memory
  • Chronic stress
  • Environmental enrichment
  • Pigs
  • Personality