An examination of early neural and cognitive alterations in hippocampal-spatial function of ghrelin receptor-deficient rats

Behavioural Brain Research

Volumn 264, Issue , 2014, Pages 105-115

  Cahill, Shaina P ^a   Hatchard, Taylor ^a   Abizaid, Alfonso ^a   Holahan, Matthew R ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

Ghrelin; Neurogenesis; Radial arm maze; Spatial memory; Spines; Water maze

Indexed keywords

DOUBLECORTIN; GHRELIN RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS; DORSAL RAPHE NUCLEUS; GENE MUTATION; HIPPOCAMPAL CA1 REGION; MALE; MEDIAN RAPHE NUCLEUS; MIDDLE AGED; MORRIS WATER MAZE TEST; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; RADIAL ARM MAZE TEST; RAT; SPATIAL LEARNING; SPATIAL MEMORY; TASK PERFORMANCE; WILD TYPE; YOUNG ADULT;

GHRELIN; NEUROGENESIS; RADIAL ARM MAZE; SPATIAL MEMORY; SPINES; WATER MAZE;

AGE FACTORS; ANIMALS; BODY WEIGHT; COGNITION DISORDERS; DENDRITIC SPINES; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GHRELIN; HIPPOCAMPUS; MALE; MAZE LEARNING; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPEPTIDES; RATS; RATS, TRANSGENIC; RECEPTORS, GHRELIN; SILVER STAINING; SPACE PERCEPTION; TIME FACTORS;

EID: 84896707708     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.02.004     Document Type: Article

References (58)

1. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999, 402:656-660.
2. Kojima M., Kangawa K. Ghrelin, an orexigenic signaling molecule from the gastrointestinal tract. Curr Opin Pharmacol 2002, 2:665-668.
3. Yoshihara F., Kojima M., Hosoda H., Nakazato M., Kangawa K. Ghrelin: a novel peptide for growth hormone release and feeding regulation. Curr Opin Clin Nutr Metab Care 2002, 5:391-395.
4. Tschop M., Smiley D.L., Heiman M.L. Ghrelin induces adiposity in rodents. Nature 2000, 407:908-913.
5. Theander-Carrillo C., Wiedmer P., Cettour-Rose P., Nogueiras R., Perez-Tilve D., Pfluger P., et al. Ghrelin action in the brain controls adipocyte metabolism. J Clin Invest 2006, 116:1983-1993.
6. Abizaid A., Horvath T.L. Brain circuits regulating energy homeostasis. Regul Pept 2008, 149:3-10.
7. Abizaid A. Ghrelin and dopamine: new insights on the peripheral regulation of appetite. J Neuroendocrinol 2009, 21:787-793.
8. Perello M., Zigman J.M. The role of ghrelin in reward-based eating. Biol Psychiatry 2012, 72:347-353.
9. Skibicka K.P., Dickson S.L. Ghrelin and food reward: the story of potential underlying substrates. Peptides 2011, 32:2265-2273.
10. Skibicka K.P., Hansson C., Alvarez-Crespo M., Friberg P.A., Dickson S.L. Ghrelin directly targets the ventral tegmental area to increase food motivation. Neuroscience 2011, 180:129-137.
11. Egecioglu E., Jerlhag E., Salome N., Skibicka K.P., Haage D., Bohlooly Y.M., et al. Ghrelin increases intake of rewarding food in rodents. Addict Biol 2010, 15:304-311.
12. Zigman J.M., Jones J.E., Lee C.E., Saper C.B., Elmquist J.K. Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol 2006, 494:528-548.
13. Diano S., Farr S.A., Benoit S.C., McNay E.C., da Silva I., Horvath B., et al. Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci 2006, 9:381-388.
14. Moon M., Kim S., Hwang L., Park S. Ghrelin regulates hippocampal neurogenesis in adult mice. Endocr J 2009, 56:525-531.
15. Berrout L., Isokawa M. Ghrelin promotes reorganization of dendritic spines in cultured rat hippocampal slices. Neurosci Lett 2012, 516:280-284.
16. Johansson I., Destefanis S., Aberg N.D., Aberg M.A., Blomgren K., Zhu C., et al. Proliferative and protective effects of growth hormone secretagogues on adult rat hippocampal progenitor cells. Endocrinology 2008, 149:2191-2199.
17. Rao M.S., Hattiangady B., Abdel-Rahman A., Stanley D.P., Shetty A.K. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 2005, 21:464-476.
18. Rao M.S., Hattiangady B., Shetty A.K. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 2006, 5:545-558.
19. Amrein I., Isler K., Lipp H.P. Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage. Eur J Neurosci 2011, 34:978-987.
20. Atcha Z., Chen W.S., Ong A.B., Wong F.K., Neo A., Browne E.R., et al. Cognitive enhancing effects of ghrelin receptor agonists. Psychopharmacology (Berl) 2009, 206:415-427.
21. Carlini V.P., Monzon M.E., Varas M.M., Cragnolini A.B., Schioth H.B., Scimonelli T.N., et al. Ghrelin increases anxiety-like behavior and memory retention in rats. Biochem Biophys Res Commun 2002, 299:739-743.
22. Carlini V.P., Varas M.M., Cragnolini A.B., Schioth H.B., Scimonelli T.N., de Barioglio S.R. Differential role of the hippocampus, amygdala, and dorsal raphe nucleus in regulating feeding, memory, and anxiety-like behavioral responses to ghrelin. Biochem Biophys Res Commun 2004, 313:635-641.
23. Carlini V.P., Perez M.F., Salde E., Schioth H.B., Ramirez O.A., de Barioglio S.R. Ghrelin induced memory facilitation implicates nitric oxide synthase activation and decrease in the threshold to promote LTP in hippocampal dentate gyrus. Physiol Behav 2010, 101:117-123.
24. Carlini V.P., Ghersi M., Schioth H.B., de Barioglio S.R. Ghrelin and memory: differential effects on acquisition and retrieval. Peptides 2010, 31:1190-1193.
25. Kenny R., Cai G., Bayliss J.A., Clarke M., Choo Y.L., Miller A.A., et al. Endogenous ghrelin's role in hippocampal neuroprotection after global cerebral ischemia: does endogenous ghrelin protect against global stroke?. Am J Physiol Regul Integr Comp Physiol 2013, 304:R980-R990.
26. Albarran-Zeckler R.G., Brantley A.F., Smith R.G. Growth hormone secretagogue receptor (GHS-R1a) knockout mice exhibit improved spatial memory and deficits in contextual memory. Behav Brain Res 2012, 232:13-19.
27. Davis J.F., Choi D.L., Clegg D.J., Benoit S.C. Signaling through the ghrelin receptor modulates hippocampal function and meal anticipation in mice. Physiol Behav 2011, 103:39-43.
28. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 2001, 36:60-90.
29. Whishaw I.Q., Tomie J. Of mice and mazes: similarities between mice and rats on dry land but not water mazes. Physiol Behav 1996, 60:1191-1197.
30. Lipp H.P., Wolfer D.P. Genetically modified mice and cognition. Curr Opin Neurobiol 1998, 8:272-280.
31. Abizaid A., Liu Z.W., Andrews Z.B., Shanabrough M., Borok E., Elsworth J.D., et al. Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest 2006, 116:3229-3239.
32. Saab B.J., Saab A.M., Roder J.C. Statistical and theoretical considerations for the platform re-location water maze. J Neurosci Methods 2011, 198:44-52.
33. Meck W.H., Church R.M., Olton D.S. Hippocampus, time, and memory. Behav Neurosci 2013, 127:655-668.
34. Vetere G., Restivo L., Cole C.J., Ross P.J., Ammassari-Teule M., Josselyn S.A., et al. Spine growth in the anterior cingulate cortex is necessary for the consolidation of contextual fear memory. PNAS 2011, 108:8456-8460.
35. Vetere G., Restivo L., Novembre G., Aceti M., Lumaca M., Ammassari-Teule M. Extinction partially reverts structural changes associated with remote fear memory. Learn Mem 2011, 18:554-557.
36. Gould E., Woolley C.S., Frankfurt M., McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 1990, 10:1286-1291.
37. Li E., Chung H., Kim Y., Kim D.H., Ryu J.H., Sato T., et al. Ghrelin directly stimulates adult hippocampal neurogenesis: implications for learning and memory. Endocr J 2013, 60:781-789.
38. Li E., Kim Y., Kim S., Park S. Ghrelin-induced hippocampal neurogenesis and enhancement of cognitive function are mediated independently of GH/IGF-1 axis: lessons from the spontaneous dwarf rats. Endocr J 2013.
39. Bizon J.L., Gallagher M. More is less: neurogenesis and age-related cognitive decline in Long-Evans rats. Sci Aging Knowledge Environ-SAGE KE 2005, 2005:re2.
40. Scharfman H.E., Hen R. Neuroscience: is more neurogenesis always better?. Science 2007, 315:336-338.
41. Hsiao S., Isaacson R.L. Learning of food and water positions by hippocampus damaged rats. Physiol Behav 1971, 6:81-83.
42. Hirsh R. The hippocampus and contextual retrieval of information from memory: a theory. Behav Biol 1974, 12:421-444.
43. Egecioglu E., Skibicka K.P., Hansson C., Alvarez-Crespo M., Friberg P.A., Jerlhag E., et al. Hedonic and incentive signals for body weight control. Rev Endocr Metab Disord 2011, 12:141-151.
44. Jerlhag E., Egecioglu E., Dickson S.L., Andersson M., Svensson L., Engel J.A. Ghrelin stimulates locomotor activity and accumbal dopamine-overflow via central cholinergic systems in mice: implications for its involvement in brain reward. Addict Biol 2006, 11:45-54.
45. Jerlhag E., Egecioglu E., Dickson S.L., Engel J.A. Ghrelin receptor antagonism attenuates cocaine- and amphetamine-induced locomotor stimulation, accumbal dopamine release, and conditioned place preference. Psychopharmacology (Berl) 2010, 211:415-422.
46. Wellman P.J., Clifford P.S., Rodriguez J.A., Hughes S., Di Francesco C., Melotto S., et al. Brain reinforcement system function is ghrelin dependent: studies in the rat using pharmacological fMRI and intracranial self-stimulation. Addict Biol 2012, 17:908-919.
47. Clifford P.S., Rodriguez J., Schul D., Hughes S., Kniffin T., Hart N., et al. Attenuation of cocaine-induced locomotor sensitization in rats sustaining genetic or pharmacologic antagonism of ghrelin receptors. Addict Biol 2012, 17:956-963.
48. Kuijpers M.H., de Jong W. Relationship between blood pressure level, renal histopathological lesions and plasma renin activity in fawn-hooded rats. Br J Exp Pathol 1987, 68:179-187.
49. Kuijpers M.H., de Jong W. Spontaneous hypertension in the fawn-hooded rat: a cardiovascular disease model. J Hypertens Suppl 1986, 4:S41-S44.
50. Kuijpers M.H., Gruys E. Spontaneous hypertension and hypertensive renal disease in the fawn-hooded rat. Br J Exp Pathol 1984, 65:181-190.
51. Kuijpers M.H., Provoost A.P., de Jong W. Development of hypertension and proteinuria with age in fawn-hooded rats. Clin Exp Pharmacol Physiol 1986, 13:201-209.
52. Chung H., Kim E., Lee D.H., Seo S., Ju S., Lee D., et al. Ghrelin inhibits apoptosis in hypothalamic neuronal cells during oxygen-glucose deprivation. Endocrinology 2007, 148:148-159.
53. Moon M., Kim H.G., Hwang L., Seo J.H., Kim S., Hwang S., et al. Neuroprotective effect of ghrelin in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease by blocking microglial activation. Neurotox Res 2009, 15:332-347.
54. Brown E.S., Rush A.J., McEwen B.S. Hippocampal remodeling and damage by corticosteroids: implications for mood disorders. Neuropsychopharmacology 1999, 21:474-484.
55. McEwen B.S. Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann NY Acad Sci 2001, 933:265-277.
56. Sapolsky R.M., Armanini M.P., Packan D.R., Sutton S.W., Plotsky P.M. Glucocorticoid feedback inhibition of adrenocorticotropic hormone secretagogue release. Relationship to corticosteroid receptor occupancy in various limbic sites. Neuroendocrinology 1990, 51:328-336.
57. McEwen B.S. Brain on stress: how the social environment gets under the skin. PNAS 2012, 109(Suppl 2):17180-17185.
58. Patterson Z.R., Ducharme R., Anisman H., Abizaid A. Altered metabolic and neurochemical responses to chronic unpredictable stressors in ghrelin receptor-deficient mice. Eur J Neurosci 2010, 32:632-639.