Food restriction reduces neurogenesis in the avian hippocampal formation

The mammalian hippocampus is particularly vulnerable to chronic stress. Adult neurogenesis in the dentate gyrus is suppressed by chronic stress and by administration of glucocorticoid hormones. Post-natal and adult neurogenesis are present in the avian hippocampal formation as well, but much less is known about its sensitivity to chronic stressors. In this study, we investigate this question in a commercial bird model: the broiler breeder chicken. Commercial broiler breeders are food restricted during development to manipulate their growth curve and to avoid negative health outcomes, including obesity and poor reproductive performance. Beyond knowing that these chickens are healthier than fully-fed birds and that they have a high motivation to eat, little is known about how food restriction impacts the animals' physiology. Chickens were kept on a commercial food-restricted diet during the first 12 weeks of life, or released from this restriction by feeding them ad libitum from weeks 7–12 of life. To test the hypothesis that chronic food restriction decreases the production of new neurons (neurogenesis) in the hippocampal formation, the cell proliferation marker bromodeoxyuridine was injected one week prior to tissue collection. Corticosterone levels in blood plasma were elevated during food restriction, even though molecular markers of hypothalamic-pituitary-adrenal axis activation did not differ between the treatments. The density of new hippocampal neurons was significantly reduced in the food-restricted condition, as compared to chickens fed ad libitum, similar to findings in rats at a similar developmental stage. Food restriction did not affect hippocampal volume or the total number of neurons. These findings indicate that in birds, like in mammals, reduction in hippocampal neurogenesis is associated with chronically elevated corticosterone levels, and therefore potentially with chronic stress in general. This finding is consistent with the hypothesis that the response to stressors in the avian hippocampal formation is homologous to that of the mammalian hippocampus.

[1]  T. Smulders The Avian Hippocampal Formation and the Stress Response , 2017, Brain, Behavior and Evolution.

[2]  J. P. Andrade,et al.  Caloric restriction in young rats disturbs hippocampal neurogenesis and spatial learning , 2016, Neurobiology of Learning and Memory.

[3]  G. Striedter Evolution of the hippocampus in reptiles and birds , 2016, The Journal of comparative neurology.

[4]  C. Herold,et al.  The maturation of research into the avian hippocampal formation: Recent discoveries from one of the nature's foremost navigators , 2015, Hippocampus.

[5]  R. Sapolsky,et al.  Stress and the brain: individual variability and the inverted-U , 2015, Nature Neuroscience.

[6]  I. Dunn,et al.  Hypothalamic Agouti‐Related Peptide mRNA is Elevated During Natural and Stress‐Induced Anorexia , 2015, Journal of neuroendocrinology.

[7]  J. Wingfield,et al.  Decreases in Mineralocorticoid but not Glucocorticoid Receptor mRNA Expression During the Short Arctic Breeding Season in Free‐Living Gambel's White‐Crowned Sparrow (Zonotrichia leucophrys gambelii) , 2015, Journal of neuroendocrinology.

[8]  M. Bateson,et al.  Measuring Motivation for Appetitive Behaviour: Food-Restricted Broiler Breeder Chickens Cross a Water Barrier to Forage in an Area of Wood Shavings without Food , 2014, PloS one.

[9]  L. Medina,et al.  Combinatorial expression of Lef1, Lhx2, Lhx5, Lhx9, Lmo3, Lmo4, and Prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken , 2014, Front. Neuroanat..

[10]  R. Hen,et al.  Functional dissociation of adult‐born neurons along the dorsoventral axis of the dentate gyrus , 2014, Hippocampus.

[11]  E. Vreugdenhil,et al.  Stress, glucocorticoid receptors, and adult neurogenesis: a balance between excitation and inhibition? , 2014, Cellular and Molecular Life Sciences.

[12]  José N. Nobrega,et al.  Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects , 2014, Neuroscience & Biobehavioral Reviews.

[13]  L. Romero,et al.  Seasonal Variation in Corticosterone Receptor Binding in Brain, Hippocampus, and Gonads in House Sparrows (Passer domesticus) , 2013 .

[14]  R. D’Eath,et al.  Hypothalamic Agouti‐Related Protein Expression Is Affected by Both Acute and Chronic Experience of Food Restriction and Re‐Feeding in Chickens , 2013, Journal of neuroendocrinology.

[15]  L. Britto,et al.  Chronic unpredictable mild stress alters an anxiety-related defensive response, Fos immunoreactivity and hippocampal adult neurogenesis , 2013, Behavioural Brain Research.

[16]  Norbert J. Fortin,et al.  The evolution of episodic memory , 2013, Proceedings of the National Academy of Sciences.

[17]  M. Herkenham,et al.  Glucocorticoids Orchestrate Divergent Effects on Mood through Adult Neurogenesis , 2013, The Journal of Neuroscience.

[18]  M. Morris,et al.  The link between stress and feeding behaviour , 2012, Neuropharmacology.

[19]  L. Carruth,et al.  Distribution and subcellular localization of glucocorticoid receptor-immunoreactive neurons in the developing and adult male zebra finch brain. , 2011, General and comparative endocrinology.

[20]  N. Rattenborg,et al.  A bird-brain view of episodic memory , 2011, Behavioural Brain Research.

[21]  V. Pravosudov,et al.  Birds as a model to study adult neurogenesis: bridging evolutionary, comparative and neuroethological approaches , 2011, The European journal of neuroscience.

[22]  I. D. de Jong,et al.  Major welfare issues in broiler breeders , 2011 .

[23]  S. Meddle,et al.  Mineralocorticoid and glucocorticoid receptor mRNA expression in the brain of translocated chukar (Alectoris chukar). , 2011, General and comparative endocrinology.

[24]  Y. Ho,et al.  Adult neurogenesis is reduced in the dorsal hippocampus of rats displaying learned helplessness behavior , 2010, Neuroscience.

[25]  L. Galea,et al.  Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats , 2010, Neuroscience.

[26]  L. LaDage,et al.  Ecologically relevant spatial memory use modulates hippocampal neurogenesis , 2010, Proceedings of the Royal Society B: Biological Sciences.

[27]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[28]  T. Devoogd,et al.  Captivity reduces hippocampal volume but not survival of new cells in a food‐storing bird , 2009, Developmental neurobiology.

[29]  I. Dunn,et al.  Chronic Stress Alters Glucocorticoid Receptor and Mineralocorticoid Receptor mRNA Expression in the European Starling (Sturnus vulgaris) Brain , 2009, Journal of neuroendocrinology.

[30]  G. Chrousos Stress and disorders of the stress system , 2009, Nature Reviews Endocrinology.

[31]  Ilias Kyriazakis,et al.  ‘Freedom from hunger’ and preventing obesity: the animal welfare implications of reducing food quantity or quality , 2009, Animal Behaviour.

[32]  P. Kaiser,et al.  Effects of stress, mimicked by administration of corticosterone in drinking water, on the expression of chicken cytokine and chemokine genes in lymphocytes , 2009, Stress.

[33]  M. Furey,et al.  Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression , 2008, Brain Structure and Function.

[34]  M. Mattson,et al.  Dietary restriction enhances neurogenesis and up-regulates neurotrophin expression in the hippocampus of adult mice , 2008 .

[35]  I. Veissier,et al.  Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare , 2007, Physiology & Behavior.

[36]  Luis Puelles,et al.  The Chick Brain in Stereotaxic Coordinates: An Atlas featuring Neuromeric Subdivisions and Mammalian Homologies , 2007 .

[37]  B. McEwen Physiology and neurobiology of stress and adaptation: central role of the brain. , 2007, Physiological reviews.

[38]  B. Czéh,et al.  What causes the hippocampal volume decrease in depression? , 2007, European Archives of Psychiatry and Clinical Neuroscience.

[39]  S. Healy,et al.  Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress , 2007, Proceedings of the Royal Society B: Biological Sciences.

[40]  E. Acevedo,et al.  Modeling the anxiety–depression continuum hypothesis in domestic fowl chicks , 2006, Behavioural pharmacology.

[41]  C. Dermon,et al.  Passive avoidance training is correlated with decreased cell proliferation in the chick hippocampus , 2006, The European journal of neuroscience.

[42]  Y. Jégo,et al.  Broiler breeder paradox: a project report , 2006 .

[43]  René Hen,et al.  Hippocampal Neurogenesis: Regulation by Stress and Antidepressants , 2006, Biological Psychiatry.

[44]  F. Nottebohm,et al.  Social and spatial changes induce multiple survival regimes for new neurons in two regions of the adult brain: An anatomical representation of time? , 2006, Behavioural Brain Research.

[45]  P. Hocking Roles of body weight and feed intake in ovarian follicular dynamics in broiler breeders at the onset of lay and after a forced molt. , 2004, Poultry science.

[46]  H. Lin,et al.  Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 1. Chronic exposure. , 2004, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[47]  M A Good,et al.  Hippocampal lesions disrupt navigation based on the shape of the environment. , 2004, Behavioral neuroscience.

[48]  J. Wild,et al.  Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions , 2004, The Journal of comparative neurology.

[49]  Michael Marriott,et al.  Lower hippocampal volume in patients suffering from depression: a meta-analysis. , 2004, The American journal of psychiatry.

[50]  V. Pravosudov Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  Robert M. Sapolsky,et al.  Stress and Plasticity in the Limbic System , 2003, Neurochemical Research.

[52]  J. Ferro,et al.  Performance and hormonal profile in broiler chickens fed with different energy levels during post restriction period , 2003 .

[53]  M. Mattson,et al.  Evidence that brain‐derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice , 2002, Journal of neurochemistry.

[54]  J. P. Andrade,et al.  Restricted feeding facilitates time–place learning in adult rats , 2002, Behavioural Brain Research.

[55]  J. Mench Broiler breeders: feed restriction and welfare , 2002 .

[56]  Arturo Alvarez-Buylla,et al.  Neurogenesis in Adult Subventricular Zone , 2002, The Journal of Neuroscience.

[57]  Fred H. Gage,et al.  Neurogenesis in the Adult Brain , 2002, The Journal of Neuroscience.

[58]  Mark P Mattson,et al.  Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice , 2002, Journal of neurochemistry.

[59]  E Gould,et al.  Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone‐dependent mechanism , 2001, The Journal of comparative neurology.

[60]  S. Healy,et al.  A larger hippocampus is associated with longer-lasting spatial memory , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[61]  N. Clayton,et al.  Effects of demanding foraging conditions on cache retrieval accuracy in food-caching mountain chickadees (Poecile gambeli) , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  Elizabeth Gould,et al.  Regulation of hippocampal neurogenesis in adulthood , 2000, Biological Psychiatry.

[63]  M. Mattson,et al.  Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats , 2000, Journal of Molecular Neuroscience.

[64]  R. Sapolsky,et al.  Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. , 2000, Archives of general psychiatry.

[65]  T. Smulders,et al.  Effects of captivity and testosterone on the volumes of four brain regions in the dark-eyed junco (Junco hyemalis). , 2000, Journal of neurobiology.

[66]  P. Eriksson,et al.  Peripheral Infusion of IGF-I Selectively Induces Neurogenesis in the Adult Rat Hippocampus , 2000, The Journal of Neuroscience.

[67]  Elizabeth Gould,et al.  Stress and hippocampal neurogenesis , 1999, Biological Psychiatry.

[68]  T J Sejnowski,et al.  Running enhances neurogenesis, learning, and long-term potentiation in mice. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[69]  R. McKay,et al.  Restoring production of hippocampal neurons in old age , 1999, Nature Neuroscience.

[70]  F. Gage,et al.  Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus , 1999, Nature Neuroscience.

[71]  S. Goldman,et al.  Adult neurogenesis: from canaries to the clinic. , 1998, Journal of neurobiology.

[72]  H. Cameron,et al.  Adrenal steroids suppress granule cell death in the developing dentate gyrus through an NMDA receptor-dependent mechanism. , 1997, Brain research. Developmental brain research.

[73]  Constance Scharff,et al.  Selective Expression of Insulin-Like Growth Factor II in the Songbird Brain , 1997, The Journal of Neuroscience.

[74]  E. Gould,et al.  Neurogenesis in the Dentate Gyrus of the Adult Tree Shrew Is Regulated by Psychosocial Stress and NMDA Receptor Activation , 1997, The Journal of Neuroscience.

[75]  S. Goldman,et al.  Hu protein as an early marker of neuronal phenotypic differentiation by subependymal zone cells of the adult songbird forebrain. , 1995, Journal of neurobiology.

[76]  Michael Maes,et al.  Evidence for an immune response in major depression: A review and hypothesis , 1995, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[77]  A. Álvarez-Buylla,et al.  Contribution of neurons born during embryonic and adult life to the brain of adult canaries: Regional specificity and delayed birth of neurons in the song‐control nuclei , 1994, The Journal of comparative neurology.

[78]  H. Cameron,et al.  Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus , 1994, Neuroscience.

[79]  A. Armario,et al.  Effects of chronic stress on food intake in rats: Influence of stressor intensity and duration of daily exposure , 1994, Physiology & Behavior.

[80]  P. Hocking,et al.  Effects of body weight at sexual maturity and the degree and age of restriction during rearing on the ovarian follicular hierarchy of broiler breeder females. , 1993, British poultry science.

[81]  M. Mitchell,et al.  Welfare assessment of broiler breeder and layer females subjected to food restriction and limited access to water during rearing , 1993 .

[82]  S. Rutter,et al.  Assessment of Hunger in Growing Broiler Breeders in Relation to a Commercial Restricted Feeding Programme , 1993, Animal Welfare.

[83]  J. Wingfield,et al.  Interactions of corticosterone with feeding, activity and metabolism in passerine birds , 1992 .

[84]  Fernando Nottebohm,et al.  Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division , 1990, Neuron.

[85]  R. S. Sloviter,et al.  Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. , 1989, Science.

[86]  Fernando Nottebohm,et al.  Migration of young neurons in adult avian brain , 1988, Nature.

[87]  J G Phillips,et al.  Stress and adrenal function. , 1984, The Journal of experimental zoology.

[88]  F. Nottebohm,et al.  Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[89]  B. Christie,et al.  Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways , 2006, Hippocampus.

[90]  R. Duman,et al.  Hippocampal neurogenesis: Opposing effects of stress and antidepressant treatment , 2006, Hippocampus.

[91]  Christian Mirescu,et al.  Stress and adult neurogenesis , 2006, Hippocampus.

[92]  J. Wild,et al.  Anatomy of the Avian Hippocampal Formation , 2006, Reviews in the neurosciences.

[93]  V. Pravosudov,et al.  Dominance-related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees. , 2005, Journal of neurobiology.

[94]  V. Pravosudov,et al.  Prolonged moderate elevation of corticosterone does not affect hippocampal anatomy or cell proliferation rates in mountain chickadees (Poecile gambeli). , 2005, Journal of neurobiology.

[95]  J. Bayle,et al.  Effects of limbic stimulations or lesions on basal and stress-induced hypothalamic-pituitary-adrenocortical activity in the pigeon. , 1973, Neuroendocrinology.