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From operant learning to cognitive enrichment in farm animal housing: bases and applicability

Published online by Cambridge University Press:  01 January 2023

G Manteuffel*
Affiliation:
Research Institute for the Biology of Farm Animals (FBN), Unit Behavioural Physiology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
J Langbein
Affiliation:
Research Institute for the Biology of Farm Animals (FBN), Unit Behavioural Physiology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
B Puppe
Affiliation:
Research Institute for the Biology of Farm Animals (FBN), Unit Behavioural Physiology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
*
* Contact for correspondence and requests for reprints: manteuff@fbn-dummerstorf.de

Abstract

This study has its basis in recent findings by our own and other laboratories and proposes a type of rewarded operant learning that seeks the detection of discriminatory cues as a cognitive enrichment in intensive husbandry systems. This type of cognitive enrichment has the ability to activate the intrinsically-rewarding mesolimbic brain axis when an animal acquires successful strategies to cope with environmental demands. It provides animals with the opportunity to develop positive affects through control of their environment and the anticipation of consummatory reward. If true animal welfare is considered more than simply the absence of stress and harm, provoking better affective conditions may be a suitable way of increasing the well-being of intensively-housed animals. Recent research with elaborated operant learning equipment, under experimental and quasi-commercial conditions, revealed better health, reduced boredom and less maladaptive behaviour as potentially practical advantages. A number of the issues regarding the transfer of this suggested form of cognitive enrichment to large scale, commercial farming are discussed.

Type
Research Article
Copyright
© 2009 Universities Federation for Animal Welfare

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References

Bassett, L and Buchanan-Smith, HM 2007 Effects of predictability on the welfare of captive animals. Applied Animal Behaviour Science 102: 223245CrossRefGoogle Scholar
Bateson, M and Matheson, SM 2007 Performance on a categorisation task suggests that removal of environmental enrichment induces ‘pessimism’ in captive European starlings (Sturnus vulgaris). Animal Welfare 16: S33S36Google Scholar
Baymann, U, Langbein, J, Siebert, K, Nürnberg, G, Manteuffel, G and Mohr, E 2007 Kognitive Verhaltensanreicherung bei landwirtschaftlichen Nutztieren - zum Einfluss des sozialen Ranges und der sozialen Umwelt auf das Lernverhalten von Zwergziegen. Berlin Münchner Tierärztliche Wochenschrift 120: 8997. [Title translation: Cognitive enrichment in farm animals: the impact of social rank and social environment on learning behaviour of dwarf goats]Google Scholar
Bloomsmith, MA and Lambeth, SP 1995 Effects of predictable versus unpredictable feeding schedules on chimpanzee behaviour. Applied Animal Behaviour Science 44: 6574Google Scholar
Boissy, A, Manteuffel, G, Bak Jensen, M, Oppermann Moe, R, Spruijt, BM, Keeling, LJ, Winckler, C, Forkman, B, Dimitrov, I, Langbein, J, Bakken, M, Veissier, I and Aubert, A 2007 Assessment of positive emotions in animals to improve their welfare. Physiology & Behavior 92: 375397CrossRefGoogle ScholarPubMed
Burgdorf, J and Panksepp, J 2006 The neurobiology of positive emotions. Neuroscience & Biobehavoral Reviews 30: 173187CrossRefGoogle ScholarPubMed
Carelli, RM and Deadwyler, SA 1994 A comparison of nucleus accumbens neuronal firing patterns during cocaine self-administration and water reinforcement in rats. Journal of Neuroscience 14: 77357746CrossRefGoogle ScholarPubMed
Carlstead, K 1986 Predictability of feeding: its effects on agonistic behaviour and growth in grower pigs. Applied Animal Behaviour Science 16: 2538CrossRefGoogle Scholar
Carlstead, K and Shepherdson, DJ 2000 Alleviating stress in zoo animals with environmental enrichment. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress pp 337354. CABI Publishing: Oxon, UKGoogle Scholar
Chang, JY, Zhang, L, Janak, PH and Woodward, DJ 1997 Neuronal responses in prefrontal cortex and nucleus accumbens during heroin self-administration in freely moving rats. Brain Research 754: 1220CrossRefGoogle ScholarPubMed
Cooper, JJ, McDonald, L and Mills, DS 2000 The effect of increasing visual horizons on stereotypic weaving: implications for the social housing of stable horses. Applied Animal Behaviour Science 69: 6783CrossRefGoogle ScholarPubMed
Croney, CC, Adams, KM, Washington, CG and Stricklin, WR 2003 A note on visual, olfactory and spatial cue use in foraging behavior of pigs: indirectly assessing cognitive abilities. Applied Animal Behaviour Science 83: 303308CrossRefGoogle Scholar
Della Chiesa, A, Speranza, M, Tommasi, L and Vallortigara, G 2006 Spatial cognition based on geometry and landmarks in the domestic chick (Gallus gallus). Behavioural Brain Research 175: 119127CrossRefGoogle Scholar
Désiré, L, Boissy, A and Veissier, I 2002 Emotions in farm animals: a new approach to animal welfare in applied ethology. Behavioural Processes 60: 165180CrossRefGoogle ScholarPubMed
Désiré, L, Veissier, I, Despres, G and Boissy, A 2004 On the way to assess emotions in animals: Do lambs (Ovis aries) evaluate an event through its suddenness, novelty, or unpredictability? Journal of Comparative Psychology 118: 363374CrossRefGoogle ScholarPubMed
Désiré, L, Veissier, I, Despres, G, Delval, E, Toporenko, G and Boissy, A 2006 Appraisal process in sheep (Ovis aries): Interactive effect of suddenness and unfamiliarity on cardiac and behavioral responses. Journal of Comparative Psychology 120: 280287CrossRefGoogle ScholarPubMed
Dudink, S, Simonse, H, Marks, I, de Jonge, FH and Spruijt, BM 2006 Announcing the arrival of enrichment increases play behaviour and reduces weaning-stress-induced behaviours of piglets directly after weaning. Applied Animal Behaviour Science 101: 86101CrossRefGoogle Scholar
Edwards, JR and Cooper, CL 1988 The impacts of positive psychological states on physical health: a review and theoretical framework. Social Science & Medicine 27: 14471459CrossRefGoogle ScholarPubMed
Ernst, K, Puppe, B, Schön, PC and Manteuffel, G 2005 A complex feeding system for pigs aimed to induce succesful behavioural coping by cognitive adaptation. Applied Animal Behaviour Science 91: 205218CrossRefGoogle Scholar
Ernst, K, Tuchscherer, M, Kanitz, E, Puppe, B and Manteuffel, G 2006 Effects of attention and rewarded activity on immune parameters and wound healing in pigs. Physiology & Behavior 89: 448456CrossRefGoogle ScholarPubMed
Esch, T and Stefano, GB 2004 The neurobiology of pleasure, reward processes, addiction and their health implications. Neuroendocrinology Letters 25: 235251Google ScholarPubMed
Fiedler, I, Küchenmeister, U, Ender, K, Haider, W, Ernst, K, Puppe, B and Manteuffel, G 2005 Reaktion der Muskulatur auf eine stimulierende Haltung - Befunde am Kotelettmuskel (M. Longissimus) von Landrasse-Schweinen. Deutsche Tierärztliche Wochenschrift 112: 363368. [Title translation: Reaction of muscles to stimulation environment - effects on the loin muscle (M. Longissimus) of Landrace pigs]Google Scholar
Fiorino, DF, Coury, A, Fibiger, HC and Phillips, AG 1993 Electrical stimulation of reward sites in the ventral tegumental area increase dopamine transmission in the nucleus accumbens of the rat. Behavioural Brain Research 55: 131141CrossRefGoogle Scholar
Garlace, EM, Crombag, HS and Holland, PC 2007 Reinforcer-specificity of appetitive and consummatory behavior of rats after Pavlovian conditioning with food reinforcers. Physiology & Behavior 91: 95105Google Scholar
Ginane, C, Dumont, B and Petit, A 2002 Short-term choices of cattle vary with relative quality and accessibility of two hays according to an energy gain maximisation hypothesis. Applied Animal Behaviour Science 75: 269279CrossRefGoogle Scholar
Hagen, K and Broom, DR 2004 Emotional reactions to learning in cattle. Applied Animal Behaviour Science 85: 203213CrossRefGoogle Scholar
Hanggi, EB 2003 Discrimination learning based on relative size concepts in horses (Equus caballus). Applied Animal Behaviour Science 83: 201213CrossRefGoogle Scholar
Harding, EJ, Paul, ES and Mendl, M 2004 Animal behaviour: cognitive bias and affective state. Nature 427: 312CrossRefGoogle ScholarPubMed
Hemby, SE, Co, C, Koves, TR, Smith, JE and Dworkin, SI 1997 Differences in extracellular dopamine concentrations in the nucleus accumbens during response-dependent and response-independent cocaine administration in the rat. Psychopharmacology 133: 716CrossRefGoogle ScholarPubMed
Hiby, EF, Rooney, NJ and Bradshaw, JWS 2004 Dog training methods: their use, effectiveness and interaction with behaviour and welfare. Animal Welfare 13: 6369Google Scholar
Hughes, BO and Duncan, IJH 1988 The notion of ethological ‘need’, models of motivation and animal welfare. Animal Behaviour 36: 16961707CrossRefGoogle Scholar
Inglis, IR and Shepherd, DS 1994 Rats work for food they then reject: support for the information primacy approach to learned industriousness. Ethology 98: 154164CrossRefGoogle Scholar
Inglis, IR, Langton, S, Forkman, B and Lazarus, J 2001 A information primacy model of exploratory and foraging behaviour. Animal Behaviour 62: 543557CrossRefGoogle Scholar
Jones, RB 2001 Does occasional movement make pecking devices more attractive to domestic chicks? British Poultry Science 42: 4350CrossRefGoogle ScholarPubMed
Kilgour, R, Foster, TM, Temple, W, Matthews, LR and Bremner, KJ 1991 Operant technology applied to solving farm animal problems: an assessment. Applied Animal Behaviour Science 30: 141166CrossRefGoogle Scholar
Kuehn, BM 2002 Zoo animal welfare boosted by environmental enrichment, positive reinforcement training. Journal of the American Veterinary Medical Association 221: 15281529Google Scholar
Langbein, J, Nürnberg, G and Manteuffel, G 2004 Visual discrimination learning in dwarf goats and associated changes in heart rate and heart rate variability. Physiology & Behavior 82: 601609CrossRefGoogle ScholarPubMed
Langbein, J, Nürnberg, G, Puppe, B and Manteuffel, G 2006 Self-controlled visual discrimination learning of group-housed dwarf goats (Capra hircus): behavioral strategies and effects of relocation on learning and memory. Journal of Comparative Psychology 120: 5866CrossRefGoogle ScholarPubMed
Langbein, J, Siebert, K, Nürnberg, G and Manteuffel, G 2007 Learning to learn during visual discrimination in group housed dwarf goats (Capra hircus). Journal of Comparative Psychology 121: 447456CrossRefGoogle Scholar
Laule, G and Desmond, T 1998 Positive reinforcement training as an enrichment strategy. In: Shepherdson, D, Mellen, JD and Hutchins, M (eds) Second Nature: Environmental Enrichment for Captive Animals pp 302313. Smithsonian Institution Press: Washington DC, USAGoogle Scholar
Laule, GE, Bloomsmith, MA and Schapiro, SJ 2003 The use of positive reinforcement training techniques to enhance the care, management, and welfare of primates in the laboratory. Journal of Applied Animal Welfare Science 6: 163173CrossRefGoogle ScholarPubMed
Matheson, SM, Asher, L and Bateson, M 2008 Larger, enriched cages are associated with ‘optimistic’ response biases in captive European starlings (Sturnus vulgaris). Applied Animal Behaviour Science 109: 374383CrossRefGoogle Scholar
Matthews, LR and Ladewig, J 1994 Environment requirements of pigs measured by behavioural demand functions. Animal Behaviour 47: 713719CrossRefGoogle Scholar
McSweeney, FK, Hinson, JB and Cannon, CB 1996 Sensitization-habituation may occur during operant conditioning. Psychological Bulletin 120: 256271CrossRefGoogle Scholar
Meehan, CL and Mench, JA 2007 The challenge of challenge: can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science 102: 246261CrossRefGoogle Scholar
Melville, CL, Rue, HC, Rybinski, LR and Weatherly, JN 1997 Altering reinforcer variety or intensity changes the within session decrease in responding. Learning & Motivation 28: 609621CrossRefGoogle Scholar
Mench, JA, Morrow-Tesch, J and Chu, L 1998 Environmental enrichment for farm animals. Laboratory Animal 27: 3236Google Scholar
Mendl, M and Paul, ES 2004 Consciousness, emotion and animal welfare: insights from cognitive science. Animal Welfare 13: S17S25Google Scholar
Meredith, GE and Totterdell, S 1999 Microcircuits in nucleus accumbens’ shell and core involved in cognition and reward. Psychobiology 27: 165186CrossRefGoogle Scholar
Milgram, NW 2003 Cognitive experience and its effects on age-dependent cognitive decline in beagle dogs. Neurochemical Reviews 28: 16771682CrossRefGoogle Scholar
Montaudouin, S and Le Pape, G 2005 Comparison between 28 zoological parks: stereotypic and social behaviours of captive brown bears (Ursus arctos). Applied Animal Behaviour Science 92: 129141CrossRefGoogle Scholar
Neuringer, AJ 1969 Animals respond for food in the presence of free food. Science 166: 399401Google ScholarPubMed
Nicol, CJ 1996 Farm animal cognition. Animal Science 62: 375391CrossRefGoogle Scholar
Nicol, CJ 2005 Learning abilities in the horse. In: Mills, DS and McDonnell, SM (eds) The Domestic Horse: The Evolution, Development and Management of its Behaviour pp 169183. Cambridge University Press: Cambridge, UKGoogle Scholar
Niv, Y, Joel, D and Dayan, P 2006 A normative perspective on motivation. Trends in Cognitive Sciences 10: 375381CrossRefGoogle ScholarPubMed
Paul, ES, Harding, EJ and Mendl, M 2005 Measuring emotional processes in animals: the utility of a cognitive approach. Neuroscience & Biobehavioural Reviews 29: 469491CrossRefGoogle ScholarPubMed
Phillips, AG, Ahn, S and Howland, JG 2003 Amygdalar control of the mesocorticolimbic dopamine system: parallel pathways to motivated behaviour. Neuroscience & Biobehavioural Reviews 27: 543554CrossRefGoogle Scholar
Platt, DM and Novak, MA 1997 Videostimulation as enrichment for captive rhesus monkeys (Macaca mulatta). Applied Animal Behaviour Science 52: 139155Google Scholar
Puppe, B, Ernst, K, Schön, PC and Manteuffel, G 2007 Cognitive enrichment affects behavioural reactivity in domestic pigs. Applied Animal Behaviour Science 105: 7586CrossRefGoogle Scholar
Reinhardt, V 2003 Working with rather than against macaques during blood collection. Journal of Applied Animal Welfare Science 6: 189197CrossRefGoogle ScholarPubMed
Robinson, S, Sandstrom, SM, Denenberg, VH and Palmiter, RD 2005 Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards. Behavioral Neuroscience 119: 515CrossRefGoogle ScholarPubMed
Salamone, JD, Cousins, MS, McCullough, LD, Carriero, DL and Berkowitz, RJ 1994 Nucleus accumbens dopamine release increases during instrumental lever pressing for food but not free food consumption. Pharmacology Biochemistry and Behavior 49: 2531CrossRefGoogle Scholar
Sambrook, TD and Buchanan-Smith, HM 1997 Control and complexity in novel object enrichment. Animal Welfare 6: 207216Google Scholar
Schmidt, MJ and Markowitz, H 1977 Behavioral engineering as an aid in maintenance of healthy zoo animals. Journal of the American Veterinary Medical Association 171: 966969Google ScholarPubMed
Schultz, W 2001 Reward signaling by dopamine neurons. Neuroscientist 7: 293302CrossRefGoogle ScholarPubMed
Schütz, KE, Forkman, B and Jensen, P 2001 Domestication effects on foraging strategy, social behaviour and different fear responses: a comparison between red junglefowl (Gallus gallus) and a modern layer strain. Applied Animal Behaviour Science 74: 114CrossRefGoogle Scholar
Scott, L 1990 Training Non-Human Primates: Meeting Their Behavioural Needs. Universities Federation for Animal Welfare: Wheathampstead, Herts, UKGoogle Scholar
Shepherdson, DJ, Carlstead, K, Mellen, JD and Seidensticker, J 1993 Influence of food presentation on the behaviour of small cats in confined environments. Zoo Biology 12: 203216CrossRefGoogle Scholar
Shettleworth, SJ 2001 Animal cognition and animal behaviour. Animal Behaviour 61: 277286CrossRefGoogle Scholar
Solomon, RL and Corbit, JD 1974 An opponent-process theory of motivation I. Temporal dynamics of the affect. Psychological Review 81: 119145CrossRefGoogle ScholarPubMed
Spruijt, BM, van den Bos, R and Pijlman, FTA 2001 A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems. Applied Animal Behaviour Science 72: 145171CrossRefGoogle ScholarPubMed
Tarou, RL and Bashaw, MJ 2007 Maximizing the effects of environmental enrichment: Suggestions from the experimental analysis of behaviour. Applied Animal Behaviour Science 102: 189204CrossRefGoogle Scholar
von Borell, E, Langbein, J, Després, G, Hansen, S, Leterrier, C, Marchant-Forde, J, Marchant-Forde, R, Minero, M, Mohr, E, Prunier, A, Valance, D and Veissier, I 2007 Heart-rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals: A review. Physiology & Behavior 92: 293316CrossRefGoogle ScholarPubMed
Waitt, C and Buchanan-Smith, HM 2001 What time is feeding? How delays and anticipation of feeding schedules affect stump-tailed macaque behaviour. Applied Animal Behaviour Science 75: 7585CrossRefGoogle Scholar
Webster, AJF 1998 What use is science to animal welfare? Naturwissenschaften 85: 262269CrossRefGoogle ScholarPubMed
Wechsler, B and Lea, SEG 2007 Adaptation by learning: Its significance for farm animal husbandry. Applied Animal Behaviour Science 108: 197214CrossRefGoogle Scholar
Wells, DL 2004 The influence of toys on the behaviour and welfare of kennelled dogs. Animal Welfare 13: 367373Google Scholar
Wredle, E, Munksgaard, L and Spörndly, E 2006 Training cows to approach the milking unit in response to acoustic signals in an automatic milking system during the grazing season. Applied Animal Behaviour Science 101: 2739CrossRefGoogle Scholar
Young, RJ, Carruthers, J and Lawrence, AB 1994 The effect of a foraging device (The ‘Edinburgh Foodball’) on the behaviour of pigs. Applied Animal Behaviour Science 39: 237247CrossRefGoogle Scholar
Young, RJ 2003 Do domestic pigs in controlled environments contra-freeload? Journal of Applied Animal Welfare Science 6: 309318CrossRefGoogle Scholar