Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Neurophysiological assessment of animal welfare

A. J. Tilbrook A B C and C. R. Ralph A
+ Author Affiliations
- Author Affiliations

A Animal Welfare Science Centre, South Australian Research and Development Institute, Roseworthy, SA 5371, Australia.

B Present address: Centre for Animal Science, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, Qld 4072, Australia.

C Corresponding author. Email: a.tilbrook@uq.edu.au

Animal Production Science 57(12) 2370-2375 https://doi.org/10.1071/AN17312
Submitted: 12 May 2017  Accepted: 31 July 2017   Published: 20 November 2017

Abstract

Livestock industries such as the pork industry are striving to continuously improve the welfare of animals. Inherent to the success of this is the ability to rigorously assess the welfare of animals in the field. While much progress has been made towards the development of methodology to assess the welfare of animals, there have been major challenges to establishing practical and definitive procedures to assess the welfare of animals. These include, but are not limited to, establishing a universally accepted definition of animal welfare and the choice of measures that are taken from the animal to assess its welfare. Measures of biological functioning and affective (emotional) state of the animal have been common, but there have been many limitations in terms of practical application. Some of the reasons for this include the choice of physiological measures, which are often restrictive in providing information about welfare, affective measures being restricted to specific behavioural measures and the biological-functioning and affective-states approaches being undertaken in isolation. Biological and affective functioning are integrated and controlled by the brain. Many of the regions of the brain involved in the regulation of biological and emotional functioning have been identified. Furthermore, there is considerable knowledge about the roles and interactions among the neurophysiological systems in these brain regions. We propose a strategy to use this knowledge to develop procedures to assess animal welfare. The initial phase is to identify the neural pathways that regulate the physiological and emotional processes that allow animals to adapt and cope. The next phase is to determine the activity of these pathways in conscious animals in the field. This requires the identification of biomarkers of specific neuronal activity that can be measured in the conscious animal in the field. Emerging technologies are offering promise in the identification of such biomarkers and some of these are already applicable to the pig. There is now the opportunity to apply this strategy within the pork industry to assess the welfare of pigs throughout the value chain.


References

Balakathiresan NS, Chandran R, Bhomia M, Jia M, Li H, Maheshwari RK (2014) Serum and amygdala microRNA signatures of posttraumatic stress: fear correlation and biomarker potential. Journal of Psychiatric Research 57, 65–73.
Serum and amygdala microRNA signatures of posttraumatic stress: fear correlation and biomarker potential.Crossref | GoogleScholarGoogle Scholar |

Barnett JL, Hemsworth PH (2009) Welfare monitoring schemes: using research to safeguard welfare of animals on the farm. Journal of Applied Animal Welfare Science 12, 114–131.
Welfare monitoring schemes: using research to safeguard welfare of animals on the farm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKqu7o%3D&md5=f7ca3d48772b3c44bf1d20676c7dab82CAS |

Basak I, Patil KS, Alves G, Larsen JP, Møller SG (2016) MicroRNAs as neuroregulators, biomarkers and therapeutic agents in neurodegenerative diseases. Cellular and Molecular Life Sciences 73, 811–827.
MicroRNAs as neuroregulators, biomarkers and therapeutic agents in neurodegenerative diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFamu7vO&md5=cc4e0a94a6fe74400e99b1ec73ed2ed1CAS |

Baudry A, Mouillet-Richard S, Schneider B, Launay JM, Kellermann O (2010) MiR-16 targets the serotonin transporter: a new facet for adaptive responses to antidepressants. Science 329, 1537–1541.
MiR-16 targets the serotonin transporter: a new facet for adaptive responses to antidepressants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFGjtLrP&md5=bf965feb28f358ad40bbe18bc6210493CAS |

Beaudoin-Gobert M, Sgambato-Faure V (2014) Serotonergic pharmacology in animal models: from behavioral disorders to dyskinesia. Neuropharmacology 81, 15–30.
Serotonergic pharmacology in animal models: from behavioral disorders to dyskinesia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmt1ahtb8%3D&md5=0f51a36d4896f0781fb7975f804b577bCAS |

Beausoleil NJ, Mellor DJ (2015a) Advantages and limitations of the five domains model for assessing welfare impacts associated with vertebrate pest control. New Zealand Veterinary Journal 63, 37–43.
Advantages and limitations of the five domains model for assessing welfare impacts associated with vertebrate pest control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVKrt7bM&md5=5395e9f2d54b9054f339966f84c25671CAS |

Beausoleil NJ, Mellor DJ (2015b) Introducing breathlessness as a significant animal welfare issue. New Zealand Veterinary Journal 63, 44–51.
Introducing breathlessness as a significant animal welfare issue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cbgsV2jsA%3D%3D&md5=81b7bd61acc4a7063b07b81bb9b72609CAS |

Benarroch EE (2012) Endogenous opioid systems: current concepts and clinical correlations. Neurology 79, 807–814.
Endogenous opioid systems: current concepts and clinical correlations.Crossref | GoogleScholarGoogle Scholar |

Bergholm AM, Henning C, Holm SE (1984) Static and dynamic properties of tissue cage fluid in rabbits. European Journal of Clinical Microbiology 3, 126–130.
Static and dynamic properties of tissue cage fluid in rabbits.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c3gsl2ltw%3D%3D&md5=2d075b026a5da8fe2ae1778b9bd5567dCAS |

Berridge KC, Kringelbach ML (2013) Neuroscience of affect: brain mechanisms of pleasure and displeasure. Current Opinion in Neurobiology 23, 294–303.
Neuroscience of affect: brain mechanisms of pleasure and displeasure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCitrw%3D&md5=97822acb86b3318fa1e154e384a194ffCAS |

Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J, Bakken M, Veissier I, Aubert A (2007) Assessment of positive emotions in animals to improve their welfare. Physiology & Behavior 92, 375–397.
Assessment of positive emotions in animals to improve their welfare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2htr7K&md5=9fa07443e6d3ae1098f72e1e6fbcd605CAS |

Chan T, Kyere K, Davis BR, Shemyakin A, Kabitzke PA, Shair HN, Barr GA, Wiedenmayer CP (2011) The role of the medial prefrontal cortex in innate fear regulation in infants, juveniles, and adolescents. The Journal of Neuroscience 31, 4991–4999.
The role of the medial prefrontal cortex in innate fear regulation in infants, juveniles, and adolescents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkslSltbs%3D&md5=d28bf1f214f3d48aba66696101740e70CAS |

Codocedo JF, Inestrosa NC (2016) Environmental control of microRNAs in the nervous system: implications in plasticity and behavior. Neuroscience and Biobehavioral Reviews 60, 121–138.
Environmental control of microRNAs in the nervous system: implications in plasticity and behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFems7%2FK&md5=50766e1ac7b4cd4db810b5952e0180a6CAS |

Courtin J, Bienvenu TCM, Einarsson EÖ, Herry C (2013) Medial prefrontal cortex neuronal circuits in fear behavior. Neuroscience 240, 219–242.
Medial prefrontal cortex neuronal circuits in fear behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmsVCqur0%3D&md5=09f4c86e8695d5fc807568b29832e62cCAS |

Davis M (1997) Neurobiology of fear responses: the role of the amygdala. The Journal of Neuropsychiatry and Clinical Neurosciences 9, 382–402.
Neurobiology of fear responses: the role of the amygdala.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtVGgsLc%3D&md5=e195ee4f496280d781660d87aa0f5729CAS |

Dawkins MS (2008) The science of animal suffering. Ethology 114, 937–945.
The science of animal suffering.Crossref | GoogleScholarGoogle Scholar |

Dawkins MS (2017) Animal welfare and efficient farming: is conflict inevitable? Animal Production Science 57, 201–208.

Dunn JD, Whitener J (1986) Plasma corticosterone responses to electrical stimulation of the amygdaloid complex: cytoarchitectural specificity. Neuroendocrinology 42, 211–217.
Plasma corticosterone responses to electrical stimulation of the amygdaloid complex: cytoarchitectural specificity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xmt1emsQ%3D%3D&md5=a04b20591b47f85798262d385ac71d1cCAS |

Ferris CF, Febo M, Luo F, Schmidt K, Brevard M, Harder JA, Kulkarni P, Messenger T, King JA (2006) Functional magnetic resonance imaging in conscious animals: a new tool in behavioural neuroscience research. Journal of Neuroendocrinology 18, 307–318.
Functional magnetic resonance imaging in conscious animals: a new tool in behavioural neuroscience research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkslaqt78%3D&md5=12911a180504a1b4ec6c4bcdc7bf7603CAS |

Ferris CF, Stolberg T, Kulkarni P, Murugavel M, Blanchard R, Caroline CD, Febo M, Brevard M, Simon NG (2008) Imaging the neural circuitry and chemical control of aggressive motivation. BMC Neuroscience 9, 111
Imaging the neural circuitry and chemical control of aggressive motivation.Crossref | GoogleScholarGoogle Scholar |

Fraser D, Nicol CJ (2011) Preference and motivation research. In ‘Animal welfare’. (Eds MC Appleby, JA Mench, I Olsson, BO Hughes) pp. 183–199. (CAB International: Oxon, UK)

Fraser D, Duncan IJH, Edwards SA, Grandin T, Gregory NG, Guyonnet V, Hemsworth PH, Huertas SM, Huzzey JM, Mellor DJ, Mench JA, Spinka M, Whay HR (2013) General principles for the welfare of animals in production systems: the underlying science and its application. Veterinary Journal 198, 19–27.
General principles for the welfare of animals in production systems: the underlying science and its application.Crossref | GoogleScholarGoogle Scholar |

Green TC, Mellor DJ (2011) Extending ideas about animal welfare assessment to include ‘quality of life’ and related concepts. New Zealand Veterinary Journal 59, 263–271.
Extending ideas about animal welfare assessment to include ‘quality of life’ and related concepts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbltlOltQ%3D%3D&md5=653a3a9ced69f8e9a1e3fa476d9d8d15CAS |

Hartley CA, Phelps EA (2010) Changing fear: the neurocircuitry of emotion regulation. Neuropsychopharmacology 35, 136–146.
Changing fear: the neurocircuitry of emotion regulation.Crossref | GoogleScholarGoogle Scholar |

Hazel S, White P, Lomax S, Fisher AD, Hutchinson MR (2015) A systematic review of novel approaches for the measurement of pain in animals. Final report for Australian Pork Limited 2014/442.

Hemsworth PH, Mellor DJ, Cronin GM, Tilbrook AJ (2015) Scientific assessment of animal welfare. New Zealand Veterinary Journal 63, 24–30.
Scientific assessment of animal welfare.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M7lt1Cntg%3D%3D&md5=0109e2f0d79eff7df2ecaac616283d9bCAS |

Issler O, Chen A (2015) Determining the role of microRNAs in psychiatric disorders. Nature Reviews. Neuroscience 16, 201–212.
Determining the role of microRNAs in psychiatric disorders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvVKrtr8%3D&md5=685ca747ef45c2c2c17d805affb0617fCAS |

Issler O, Haramati S, Paul ED, Maeno H, Navon I, Zwang R, Gil S, Mayberg HS, Dunlop BW, Menke A, Awatramani R, Binder EB, Deneris ES, Lowry CA, Chen A (2014) MicroRNA 135 is essential for chronic stress resiliency, antidepressant efficacy, and intact serotonergic activity. Neuron 83, 344–360.
MicroRNA 135 is essential for chronic stress resiliency, antidepressant efficacy, and intact serotonergic activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVCjur7J&md5=23602cd1ca67860b3f826dd154ef84efCAS |

Kocerha J, Dwivedi Y, Brennand KJ (2015) Noncoding RNAs and neurobehavioral mechanisms in psychiatric disease. Molecular Psychiatry 20, 677–684.
Noncoding RNAs and neurobehavioral mechanisms in psychiatric disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlsFektbs%3D&md5=d42058445161dbe8c7c49adfdde1632cCAS |

Kolber BJ, Roberts MS, Howell MP, Wozniak DF, Sands MS, Muglia LJ (2008) Central amygdala glucocorticoid receptor action promotes fear-associated CRH activation and conditioning. Proceedings of the National Academy of Sciences, USA 105, 12004–12009.
Central amygdala glucocorticoid receptor action promotes fear-associated CRH activation and conditioning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVChur3I&md5=ff0607b2acd33644865812dbb22a6160CAS |

Li M, Xia Y, Gu Y, Zhang K, Lang Q, Chen L, Guan J, Luo Z, Chen H, Li Y, Li Q, Li X, Jiang A-a, Shuai S, Wang J, Zhu Q, Zhou X, Gao X, Li X (2010) MicroRNAome of porcine pre- and postnatal development. PLoS One 5, e11541
MicroRNAome of porcine pre- and postnatal development.Crossref | GoogleScholarGoogle Scholar |

Mason JW (1959) Plasma 17-hydroxycorticosteroid levels during electrical stimulation of the amygdaloid complex in conscious monkeys. The American Journal of Physiology 196, 44–48.

Mellor DJ (2012) Animal emotions, behaviour and the promotion of positive welfare states. New Zealand Veterinary Journal 60, 1–8.
Animal emotions, behaviour and the promotion of positive welfare states.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38%2Fot1Wgug%3D%3D&md5=eda4271f5e82e5a3d2cc88b23dbd3cc5CAS |

Mellor DJ (2015a) Enhancing animal welfare by creating opportunities for positive affective engagement. New Zealand Veterinary Journal 63, 3–8.
Enhancing animal welfare by creating opportunities for positive affective engagement.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cjntFyjsA%3D%3D&md5=c8cecdf89c9162c93b84a12cad176670CAS |

Mellor DJ (2015b) Positive animal welfare states and reference standards for welfare assessment. New Zealand Veterinary Journal 63, 17–23.
Positive animal welfare states and reference standards for welfare assessment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cjntFOgsA%3D%3D&md5=a04b5b2523df5b1ffa9bb707717a3d05CAS |

Mellor DJ (2016) Updating animal welfare thinking: moving beyond the ‘five freedoms’ towards ‘a life worth living’. Animals 6, 21
Updating animal welfare thinking: moving beyond the ‘five freedoms’ towards ‘a life worth living’.Crossref | GoogleScholarGoogle Scholar |

Mellor DJ, Reid CWS (1994) Concepts of animal well-being and predicting the impact of procedures on experimental animals. In ‘Improving the well-being of animals in the research environment’. pp. 3–18. (The Australian and New Zealand Council for the Care of Animals in Research and Teaching: Adelaide, SA)

Mellor DJ, Patterson-Kane E, Stafford KJ (2009) ‘The sciencs of animal welfare.’ (Wiley-Blackwell Publishing: Oxford, UK)

Mendl M, Burman OHP, Parker RMA, Paul ES (2009) Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Applied Animal Behaviour Science 118, 161–181.
Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms.Crossref | GoogleScholarGoogle Scholar |

Panksepp J (2005) Affective consciousness: core emotional feelings in animals and humans. Consciousness and Cognition 14, 30–80.
Affective consciousness: core emotional feelings in animals and humans.Crossref | GoogleScholarGoogle Scholar |

Perentos N, Nicol AU, Martins AQ, Stewart JE, Taylor P, Morton AJ (2017) Techniques for chronic monitoring of brain activity in freely moving sheep using wireless EEG recording. Journal of Neuroscience Methods 279, 87–100.
Techniques for chronic monitoring of brain activity in freely moving sheep using wireless EEG recording.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sjjt1Sgtg%3D%3D&md5=c1a689771e7aebb0e9e000ca7d2b023eCAS |

Podolska A, Kaczkowski B, Busk PK, Søkilde R, Litman T, Fredholm M, Cirera S (2011) MicroRNA expression profiling of the porcine developing brain. PloS One 6, e14494
MicroRNA expression profiling of the porcine developing brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosVyhsQ%3D%3D&md5=df8de3eec6f075c7da25484a10ee32a0CAS |

Ralph CR, Tilbrook AJ (2016) INVITED REVIEW: the usefulness of measuring glucocorticoids for assessing animal welfare. Journal of Animal Science 94, 457–470.
INVITED REVIEW: the usefulness of measuring glucocorticoids for assessing animal welfare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtVymu73J&md5=8df20a3f1cc021418809f78b784a365eCAS |

Roozendaal B, Brunson KL, Holloway BL, McGaugh JL, Baram TZ (2002) Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proceedings of the National Academy of Sciences, USA 99, 13908–13913.
Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVKmurg%3D&md5=4f13043ba6224fae0a9fa9fe3478b56eCAS |

Shepard JD, Barron KW, Myers DA (2000) Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior. Brain Research 861, 288–295.
Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1Wht78%3D&md5=c89a25fd84724a1328ae16dc08fb1249CAS |

Spruijt BM, Van den Bos R, 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, 145–171.
A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems.Crossref | GoogleScholarGoogle Scholar |

Taber KH, Black DN, Porrino LJ, Hurley RA (2012) Neuroanatomy of dopamine: reward and addiction. The Journal of Neuropsychiatry and Clinical Neurosciences 24, 1–4.
Neuroanatomy of dopamine: reward and addiction.Crossref | GoogleScholarGoogle Scholar |

Tilbrook AJ, Ralph CR (2017) Hormones, stress and the welfare of animals. Animal Production Science
Hormones, stress and the welfare of animals.Crossref | GoogleScholarGoogle Scholar |

Tovote P, Fadok JP, Luthi A (2015) Neuronal circuits for fear and anxiety. Nature Reviews. Neuroscience 16, 317–331.
Neuronal circuits for fear and anxiety.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFeit73E&md5=7f5c73d7c86741cdb0726cc5a3dbbaa0CAS |

Wang H, Wang J, Sun S, Wang Y, Guo J, Ning C, Yang K, Liu JF (2015) Identification of reference microRNAs for quantitative expression analysis in porcine peripheral blood mononuclear cells treated with polyinosinic-polycytidylic acid. International Journal of Immunogenetics 42, 217–225.
Identification of reference microRNAs for quantitative expression analysis in porcine peripheral blood mononuclear cells treated with polyinosinic-polycytidylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotVCqurg%3D&md5=0955893623dc0a8b4da4c3b55fc67462CAS |

Wemelsfelder F, Mullan S (2014) Applying ethological and health indicators to practical animal welfare assessment. Revue Scientifique et Technique (International Office of Epizootics) 33, 111–120.
Applying ethological and health indicators to practical animal welfare assessment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cbgt1SmtQ%3D%3D&md5=c5680dc9ba1994ff202ca7d0de5c3aaaCAS |