The gall of subordination: changes in gall bladder function associated with social stress

Diverse physiological and behavioural mechanisms allow animals to effectively deal with stressors, but chronic activation of the stress axis can have severe consequences. We explored the effects of chronic social stress on agonistic behaviour and gall bladder function, a critical but widely neglected component of stress‐induced gastrointestinal dysfunction. Prolonged cohabitation with dominant individuals elicited behavioural modifications and dramatically increased bile retention in subordinate convict cichlid fish (Archocentrus nigrofasciatum). The key predictor of gall bladder hypertrophy was social subordination rather than status‐related differences in food intake or body size. Stress‐induced inhibition of gall bladder emptying could affect energy assimilation such that subordinate animals would not be able to effectively convert energy‐rich food into mass gain. These results parallel changes in gall bladder function preceding cholesterol gallstone formation in humans and other mammals. Thus, social stress may be an important diagnostic criterion in understanding pathologies associated with gall bladder dysfunction.

[1]  G. Mawe Nerves and Hormones Interact to Control Gallbladder Function. , 1998, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[2]  C. BatesonMalcolm,et al.  Gallbladder disease , 2002 .

[3]  Q. Chen,et al.  Mechanisms of gallbladder hypomotility in pregnant guinea pigs. , 1999, Gastroenterology.

[4]  A. Johnsen,et al.  Stimulation of rainbow trout gallbladder contraction by cionin, an ancestral member of the CCK/gastrin family. , 1995, General and Comparative Endocrinology.

[5]  H. Lenz,et al.  Noradrenergic inhibition of canine gallbladder contraction and murine pancreatic secretion during stress by corticotropin-releasing factor. , 1992, The Journal of clinical investigation.

[6]  H. Fox,et al.  Stress and Dominance in a Social Fish , 1997, The Journal of Neuroscience.

[7]  J. Thakore,et al.  HPA axis response to a psychological stressor in generalised social phobia , 2002, Psychoneuroendocrinology.

[8]  R. Sapolsky Individual differences and the stress response , 1994 .

[9]  H. Lenz,et al.  Regulation of canine gallbladder motility by brain peptides. , 1993, Gastroenterology.

[10]  S. Creel,et al.  Social dominance and stress hormones , 2001 .

[11]  Rui F. Oliveira,et al.  Dynamics of social interactions during group formation in male of the cichlid fish Oreochromis mossambicus , 1998 .

[12]  Robert L. Spencer,et al.  Visible burrow system as a model of chronic social stress: Behavioral and neuroendocrine correlates , 1995, Psychoneuroendocrinology.

[13]  K. Huhman,et al.  Hormonal responses to fighting in hamsters: Separation of physical and psychological causes , 1992, Physiology & Behavior.

[14]  C. Talbot,et al.  Observations on the gall bladder of juvenile Atlantic salmon Salmo salar L., in relation to feeding , 1982 .

[15]  D. Karasic,et al.  Anxiety and anxiety disorders. , 1996, Focus.

[16]  Y. Taché,et al.  Psychological stress-induced accelerated colonic transit in rats involves hypothalamic corticotropin-releasing factor. , 1993, Gastroenterology.

[17]  Y. Taché,et al.  Corticotropin-releasing factor and the brain-gut motor response to stress. , 1999, Canadian journal of gastroenterology = Journal canadien de gastroenterologie.

[18]  F. Al-Kawas,et al.  Complications of gallstone disease: mirizzi syndrome, cholecystocholedochal fistula, and gallstone ileus , 2002, American Journal of Gastroenterology.

[19]  E. Keverne,et al.  Are subordinates always stressed? a comparative analysis of rank differences in cortisol levels among primates , 2003, Hormones and Behavior.

[20]  A. Seasholtz,et al.  Corticotropin-releasing hormone-binding protein: biochemistry and function from fishes to mammals. , 2002, The Journal of endocrinology.

[21]  B. Wisenden Reproductive behaviour of free-ranging convict cichlids,Cichlasoma nigrofasciatum , 1995, Environmental Biology of Fishes.

[22]  N. Metcalfe,et al.  Plasma Cortisol Concentrations Before and After Social Stress in Rainbow Trout and Brown Trout , 2001, Physiological and Biochemical Zoology.

[23]  T. Ljungberg,et al.  A test of the sequential assessment game: fighting in the cichlid fish Nannacara anomala , 1990, Animal Behaviour.

[24]  F. Guarraci,et al.  Opioid agonists inhibit excitatory neurotransmission in ganglia and at the neuromuscular junction in Guinea pig gallbladder. , 2002, Gastroenterology.

[25]  R. Alloni,et al.  Ultrasonographic assessment of gallbladder bile exchanges in healthy subjects and in gallstone patients. , 2001, Ultrasound in medicine & biology.

[26]  P. Casanova,et al.  Effect of somatostatin and thyrotropin-releasing hormone on cholecystokinin-induced gallbladder emptying , 1986, Digestive Diseases and Sciences.

[27]  Tamara C. Grand,et al.  Spatial predictability of resources and the ideal free distribution in convict cichlids, Cichlasoma nigrofasciatum , 1994, Animal Behaviour.

[28]  G. Mawe Noradrenaline as a presynaptic inhibitory neurotransmitter in ganglia of the guinea‐pig gall‐bladder. , 1993, The Journal of physiology.

[29]  K. Lillemoe,et al.  Estrogen inhibits sphincter of Oddi motility. , 1994, The Journal of surgical research.

[30]  C. Schreck,et al.  Metabolic cost of acute physical stress in juvenile steelhead , 1987 .

[31]  M. Carey,et al.  Pathogenesis of cholesterol gallstones: a parsimonious hypothesis , 1996, European journal of clinical investigation.

[32]  M. Itzkowitz,et al.  THE BENEFITS OF DEAR ENEMY RECOGNITION IN THREE-CONTENDER CONVICT CICHLID (CICHLASOMA NIGROFASCIATUM) CONTESTS , 1999 .

[33]  C. Ko,et al.  Gallstone formation. Local factors. , 1999, Gastroenterology clinics of North America.

[34]  L. Johnson,et al.  Physiology of the gastrointestinal tract , 2012 .

[35]  J. Wingfield,et al.  The concept of allostasis in biology and biomedicine , 2003, Hormones and Behavior.

[36]  V. Plourde Stress-induced changes in the gastrointestinal motor system. , 1999, Canadian journal of gastroenterology = Journal canadien de gastroenterologie.

[37]  Francis Creed,et al.  Stress and psychiatric disorder in healthcare professionals and hospital staff , 2000, The Lancet.

[38]  L. M. Gómez-Laplaza,et al.  Laboratory studies of the effects of short‐term isolation on aggressive behaviour in fish , 2000 .

[39]  C. McKittrick,et al.  Chronic Social Stress Alters Levels of Corticotropin-Releasing Factor and Arginine Vasopressin mRNA in Rat Brain , 1997, The Journal of Neuroscience.

[40]  J. Koolhaas,et al.  Individual Differences in Plasma Catecholamine and Corticosterone Stress Responses of Wild-Type Rats: Relationship With Aggression , 1996, Physiology and Behavior.

[41]  A. Johnsen,et al.  Gastrin and cholecystokinin of the bullfrog, Rana catesbeiana, have distinct effects on gallbladder motility and gastric acid secretion in vitro. , 1998, General and comparative endocrinology.

[42]  Lisa J. Martin,et al.  Gallstones: Genetics Versus Environment , 2002, Annals of surgery.

[43]  T. Coşkun,et al.  Pathways mediating CRF-induced inhibition of gastric emptying in rats , 1997, Regulatory Peptides.

[44]  M. Miyazaki,et al.  Obstructive jaundice impairs hepatic sinusoidal endothelial cell function and renders liver susceptible to hepatic ischemia/reperfusion. , 2000, Journal of hepatology.

[45]  S. Holmgren,et al.  Intraduodenal fat and amino acids activate gallbladder motility in the rainbow trout, Oncorhynchus mykiss. , 1995, General and comparative endocrinology.

[46]  S. Sarna,et al.  Central regulation of gastric emptying of solid nutrient meals by corticotropin releasing factor , 1997, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[47]  G. Tortora,et al.  Principles of anatomy & physiology , 1975 .