Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-18T19:53:42.673Z Has data issue: false hasContentIssue false
  • English
  • Français

Pig cognitive bias affects the conversion of muscle into meat by antioxidant and autophagy mechanisms

Published online by Cambridge University Press:  18 April 2017

Y. Potes ,
M. Oliván ,
A. Rubio-González ,
B. de Luxán-Delgado ,
F. Díaz ,
V. Sierra ,
L. Arroyo ,
R. Peña ,
A. Bassols  and
J. González
...Show all authors
Y. Potes
Affiliation:
Departamento de Morfología y Biología Celular, Universidad de Oviedo, Av Julián Clavería s/n, 33006 Oviedo, Asturias, Spain
M. Oliván
Affiliation:
Servicio Regional de Investigación y Desarrollo Agroalimentario (SERIDA), Apdo 13, 33300 Villaviciosa, Asturias, Spain
A. Rubio-González
Affiliation:
Departamento de Morfología y Biología Celular, Universidad de Oviedo, Av Julián Clavería s/n, 33006 Oviedo, Asturias, Spain
B. de Luxán-Delgado
Affiliation:
Departamento de Morfología y Biología Celular, Universidad de Oviedo, Av Julián Clavería s/n, 33006 Oviedo, Asturias, Spain
F. Díaz
Affiliation:
Servicio Regional de Investigación y Desarrollo Agroalimentario (SERIDA), Apdo 13, 33300 Villaviciosa, Asturias, Spain
V. Sierra
Affiliation:
Departamento de Morfología y Biología Celular, Universidad de Oviedo, Av Julián Clavería s/n, 33006 Oviedo, Asturias, Spain Servicio Regional de Investigación y Desarrollo Agroalimentario (SERIDA), Apdo 13, 33300 Villaviciosa, Asturias, Spain
L. Arroyo
Affiliation:
Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain
R. Peña
Affiliation:
Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain
A. Bassols
Affiliation:
Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain
J. González
Affiliation:
Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Finca Camps i Armet s/n, 17121 Monells, Gerona, Spain
R. Carreras
Affiliation:
Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Finca Camps i Armet s/n, 17121 Monells, Gerona, Spain
A. Velarde
Affiliation:
Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Finca Camps i Armet s/n, 17121 Monells, Gerona, Spain
M. Muñoz-Torres
Affiliation:
Hospital Universitario San Cecilio, Instituto de Investigación Biosanitaria de Granada, C/Dr. Azpitarte, 4, 18012 Granada, Spain
A. Coto-Montes*
Affiliation:
Departamento de Morfología y Biología Celular, Universidad de Oviedo, Av Julián Clavería s/n, 33006 Oviedo, Asturias, Spain
*
†E-mail: acoto@uniovi.es
Get access

Abstract

Slaughter is a crucial step in the meat production chain that could induce psychological stress on each animal, resulting in a physiological response that can differ among individuals. The aim of this study was to investigate the relationship between an animal’s emotional state, the subsequent psychological stress at slaughter and the cellular damage as an effect. In all, 36 entire male pigs were reared at an experimental farm and a cognitive bias test was used to classify them into positive bias (PB) or negative bias (NB) groups depending on their decision-making capabilities. Half of the animals, slaughtered in the same batch, were used for a complete study of biomarkers of stress, including brain neurotransmitters and some muscle biomarkers of oxidative stress. After slaughter, specific brain areas were excised and the levels of catecholamines (noradrenaline (NA) and dopamine (DA)) and indoleamines (5-hydroxyindoleacetic acid and serotonin (5HT)) were analyzed. In addition, muscle proteasome activity (20S), antioxidant defence (total antioxidant activity (TAA)), oxidative damage (lipid peroxidation (LPO)) and autophagy biomarkers (Beclin-1, microtubule-associated protein I light chain 3 (LC3-I) and LC3-II) were monitored during early postmortem maturation (0 to 24 h). Compared with PB animals, NB pigs were more susceptible to stress, showing higher 5HT levels (P<0.01) in the hippocampus and lower DA (P<0.001) in the pre-frontal cortex. Furthermore, NB pigs had more intense proteolytic processes and triggered primary muscle cell survival mechanisms immediately after slaughter (0 h postmortem), thus showing higher TAA (P<0.001) and earlier proteasome activity (P<0.001) and autophagy (Beclin-1, P<0.05; LC3-II/LC3-I, P<0.001) than PB pigs, in order to counteract the induced increase in oxidative stress, that was significantly higher in the muscle of NB pigs at 0 h postmortem (LPO, P<0.001). Our study is the first to demonstrate that pig’s cognitive bias influences the animal’s susceptibility to stress and has important effects on the postmortem muscle metabolism, particularly on the cell antioxidant defences and the autophagy onset. These results expand the current knowledge regarding biomarkers of animal welfare and highlight the potential use of biomarkers of the proteasome, the autophagy (Beclin-1, LC3-II/LC3-I ratio) and the muscle antioxidant defence (TAA, LPO) for detection of peri-slaughter stress.

Keywords

pigscognitive biasdecision makingoxidative stressautophagy
Type
Research Article
Information
animal , Volume 11 , Issue 11 , November 2017 , pp. 2027 - 2035
Copyright
© The Animal Consortium 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Members of Research team: cellular Response to Oxidative Stress (cROS).

References

Adeola, O, Ball, RO, House, JD and O’Brien, PJ 1993. Regional brain neurotransmitter concentrations in stress-susceptible pigs. Journal of Animal Science 71, 968–974.CrossRefGoogle ScholarPubMed
Arnao, MB, Cano, A and Acosta, M 2001. The hydrophilic and lipophilic contribution to total antioxidant activity. Food Chemistry 73, 239–244.CrossRefGoogle Scholar
Arroyo, L, Carreras, R, Valent, D, Pena, R, Mainau, E, Velarde, A, Sabria, J and Bassols, A 2016. Effect of handling on neurotransmitter profile in pig brain according to fear related behaviour. Physiology & Behavior 167, 374–381.CrossRefGoogle ScholarPubMed
Bauer, EP 2015. Serotonin in fear conditioning processes. Behavioural Brain Research 277, 68–77.CrossRefGoogle ScholarPubMed
Berridge, CW and Waterhouse, BD 2003. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Research Reviews 42, 33–84.CrossRefGoogle ScholarPubMed
Bradford, MM 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Caballero, B, Sierra, V, Oliván, M, Vega-Naredo, I, Tomás-Zapico, C, Álvarez-García, O, Tolivia, D, Hardeland, R, Rodríguez-Colunga, MJ and Coto-Montes, A 2007. Activity of cathepsins during beef aging related to mutations in the myostatin gene. Journal of the Science of Food and Agriculture 87, 192–199.CrossRefGoogle Scholar
Caballero, B, Tomas-Zapico, C, Vega-Naredo, I, Sierra, V, Tolivia, D, Hardeland, R, Rodriguez-Colunga, MJ, Joel, A, Nevo, E, Avivi, A and Coto-Montes, A 2006. Antioxidant activity in Spalax ehrenbergi: a possible adaptation to underground stress. Journal of Comparative Physiology 192, 753–759.CrossRefGoogle ScholarPubMed
Carreras, R, Mainau, E, Rodríguez, P, Dalmau, A, Manteca, X and Velarde, A 2015. Cognitive bias in pigs: individual classification and consistency over time. Journal of Veterinary Behavior 10, 577–581.CrossRefGoogle Scholar
Conus, S and Simon, H-U 2008. Review: cathepsins: key modulators of cell death and inflammatory responses. Biochemical Pharmacology 76, 1374–1382.CrossRefGoogle ScholarPubMed
Coto-Montes, A, Boga, JA, Rosales-Corral, S, Fuentes-Broto, L, Tan, DX and Reiter, RJ 2012. Role of melatonin in the regulation of autophagy and mitophagy: a review. Molecular and Cellular Endocrinology 361, 12–23.CrossRefGoogle ScholarPubMed
de Gonzalo-Calvo, D, Neitzert, K, Fernandez, M, Vega-Naredo, I, Caballero, B, Garcia-Macia, M, Suarez, FM, Rodriguez-Colunga, MJ, Solano, JJ and Coto-Montes, A 2010. Differential inflammatory responses in aging and disease: TNF-alpha and IL-6 as possible biomarkers. Free Radical Biology & Medicine 49, 733–737.CrossRefGoogle ScholarPubMed
European Union 2007. Amendments to the treaty on European Union and to the treaty stablishing the European community. Official Journal of the European Communities 50, 1–271.Google Scholar
European Union 2010. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Official Journal of the European Communities L276, 33–79.Google Scholar
Garcia-Macia, M, Sierra, V, Palanca, A, Vega-Naredo, I, de Gonzalo-Calvo, D, Rodriguez-Gonzalez, S, Olivan, M and Coto-Montes, A 2014. Autophagy during beef aging. Autophagy 10, 137–143.CrossRefGoogle ScholarPubMed
Houbak, MB, Ertbjerg, P and Therkildsen, M 2008. In vitro study to evaluate the degradation of bovine muscle proteins post-mortem by proteasome and mu-calpain. Meat Science 79, 77–85.CrossRefGoogle ScholarPubMed
Jorgensen, A 2013. Oxidatively generated DNA/RNA damage in psychological stress states. Danish Medical Journal 60, B4685.Google ScholarPubMed
Lana, A and Zolla, L 2015. Apoptosis or autophagy, that is the question: two ways for muscle sacrifice towards meat. Trends in Food Science & Technology 46, 231–241.CrossRefGoogle Scholar
Landsheer, J and van den Wittenboer, G 2015. Unbalanced 2 x 2 factorial designs and the interaction effect: a troublesome combination. PLoS ONE 10, e0121412.CrossRefGoogle ScholarPubMed
Li, Q, Zhang, M, Chen, YJ, Wang, YJ, Huang, F and Liu, J 2011. Oxidative damage and HSP70 expression in masseter muscle induced by psychological stress in rats. Physiology & Behavior 104, 365–372.CrossRefGoogle ScholarPubMed
Logue, SF and Gould, TJ 2013. The neural and genetic basis of executive function: attention, cognitive flexibility, and response inhibition. Pharmacology Biochemistry and Behavior 123, 45–54.CrossRefGoogle ScholarPubMed
Maribo, H, EWrtbjerg, P, Andersson, M, Barton-Gade, P and Mùller, AJ 1999. Electrical stimulation of pigs- effect on pH fall, meat quality and Cathepsin B+L activity. Meat Science 52, 179–187.CrossRefGoogle ScholarPubMed
Mendl, M, Burman, OHP, Parker, RMA and 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.CrossRefGoogle Scholar
Mora, F, Segovia, G, Del Arco, A, de Blas, M and Garrido, P 2012. Stress, neurotransmitters, corticosterone and body-brain integration. Brain Research 1476, 71–85.CrossRefGoogle ScholarPubMed
Nakhaee, A, Shahabizadeh, F and Erfani, M 2013. Protein and lipid oxidative damage in healthy students during and after exam stress. Physiology & Behavior 118, 118–121.CrossRefGoogle ScholarPubMed
Ouali, A, Gagaoua, M, Boudida, Y, Becila, S, Boudjellal, A, Herrera-Mendez, CH and Sentandreu, MA 2013. Review: biomarkers of meat tenderness: present knowledge and perspectives in regards to our current understanding of the mechanisms involved. Meat Science 95, 854–870.CrossRefGoogle ScholarPubMed
Phillips, AG, Vacca, G and Ahn, S 2008. A top-down perspective on dopamine, motivation and memory. Pharmacology Biochemistry and Behavior 90, 236–249.CrossRefGoogle ScholarPubMed
Piekarzewska, A, Sadowski, B and Rosochacki, SJ 1999. Alterations of brain monoamine levels in pigs exposed to acute immobilization stress. Zentralbl Veterinarmed A 46, 197–207.CrossRefGoogle ScholarPubMed
Poletto, R, Cheng, HW, Meisel, RL, Garner, JP, Richert, BT and Marchant-Forde, JN 2010. Aggressiveness and brain amine concentration in dominant and subordinate finishing pigs fed the beta-adrenoreceptor agonist ractopamine. Journal of Animal Science 88, 3107–3120.CrossRefGoogle ScholarPubMed
Poletto, R, Cheng, HW, Meisel, RL, Richert, BT and Marchant-Forde, JN 2011. Gene expression of serotonin and dopamine receptors and monoamine oxidase-A in the brain of dominant and subordinate pubertal domestic pigs (Sus scrofa) fed a beta-adrenoreceptor agonist. Brain Research 1381, 11–20.CrossRefGoogle ScholarPubMed
Rubio-Gonzalez, A, Potes, Y, Illan-Rodriguez, D, Vega-Naredo, I, Sierra, V, Caballero, B, Fabrega, E, Velarde, A, Dalmau, A, Olivan, M and Coto-Montes, A 2015. Effect of animal mixing as a stressor on biomarkers of autophagy and oxidative stress during pig muscle maturation. Animal 9, 1188–1194.CrossRefGoogle ScholarPubMed
Sabria, J, Torres, D, Pasto, M, Peralba, JM, Allali-Hassani, A and Pares, X 2003. Release of neurotransmitters from rat brain nerve terminals after chronic ethanol ingestion: differential effects in cortex and hippocampus. Addiction Biology 8, 287–294.CrossRefGoogle ScholarPubMed
Salim, S 2014. Oxidative stress and psychological disorders. Current Neuropharmacology 12, 140–147.CrossRefGoogle ScholarPubMed
Yeates, JW and Main, DC 2008. Assessment of positive welfare: a review. Veterinary Journal 175, 293–300.CrossRefGoogle ScholarPubMed
Supplementary material: File

Potes supplementary material

Figures S1-S2

Download Potes supplementary material(File)
File 4.1 MB