Somatostatinergic systems: An update on brain functions in normal and pathological aging

Frontiers in Endocrinology

Volumn 3, Issue DEC, 2012, Pages

  Martel, Guillaume ^a   Dutar, Patrick ^a   Epelbaum, Jacques ^a   Viollet, Cécile ^a  

^a INSERM   (France)

Author keywords

Alzheimer's disease; Cortistatin; GPCR; Interneurons; Long range; SRIF; Sst

Indexed keywords

EID: 84874443445     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2012.00154     Document Type: Review

References (198)

1. Allen, J.P., Hathway, G.J., Clarke, N.J., Jowett, M.I., Topps, S., Kendrick, K. M., et al. (2003).Somatostatin receptor 2 knockout/lacZ knockin mice show impaired motor coordination and revealsites of somatostatin action with in the striatum. Eur. J. Neurosci. 17, 1881-1895.
2. Andrews-Zwilling, Y., Bien-Ly, N., Xu, Q., Li, G., Bernardo, A., Yoon, S.Y., et al. (2010). Apolipoprotein E4 causesage-and Tau-dependent impairment of GABAergic interneurons, leading to learning and memory deficits in mice. J. Neurosci. 30, 13707-13717.
3. 2 receptors. Neuropharmacol-ogy 61, 1327-1333.
4. Bakhit, C., and Swerdlow, N. (1986). Behavioral changes following central injection of cysteamine in rats. Brain Res. 365, 159-163.
5. Baraban, S. C., and Tallent, M. K. (2004). Interneuron Diversity Series: interneuronal neuropeptides -endogenous regulators of neuronal excitability. Trends Neurosci. 27, 135-142.
6. 2+ signaling in mouse dentate gyrus. J. Neurophysiol. 88, 3078-3086.
7. Beal, M. F., Mazurek, M. F., Tran, V. T., Chattha, G., Bird, E. D., and Martin, J. B. (1985). Reduced numbers of somatostatin receptors in the cerebral cortex in Alzheimer's disease. Science 229, 289-291.
8. Beneyto, M., Morris, H. M., Roven-sky, K. C., and Lewis, D. A. (2012). Lamina- and cell-specific alterations in cortical somatostatin receptor 2 mRNA expression in schizophrenia. Neuropharmacology 62, 1598-1605.
9. Bergstrom, L., Garlind, A., Nilsson, L., Alafuzoff, I., Fowler, C. J., Winblad, B., et al. (1991). Regional distribution of somatostatin receptor binding and modulation of adenylyl cyclase activity in Alzheimer's disease brain. J. Neurol Sci. 105, 225-233.
10. Boehm, S., and Betz, H. (1997). Somatostatin inhibits excitatory transmission at rat hippocampal synapses via presynaptic receptors. J. Neurosci. 17, 4066-4075.
11. Bollok, I., Vecsei, L., and Telegdy, G. (1983). The effects of interaction between propranolol and somatostatin on the active avoidance behavior, open-field activity and electroconvulsive shock-induced amnesia of rats. Neuropeptides 3, 263-270.
12. Bousquet, C., Lasfargues, C., Chalabi, M., Billah, S. M., Susini, C., Vezzosi, D., et al. (2012). Clinical review: current scientific rationale for the use of somatostatin analogs and mTOR inhibitors in neuroendocrine tumor therapy. J. Clin. Endocrinol. Metab. 97, 727-737.
13. Bouvier, J., Thoby-Brisson, M., Renier, N., Dubreuil, V., Ericson, J., Cham-pagnat, J., et al. (2010). Hindbrain interneurons and axon guidance signaling critical for breathing. Nat. Neurosci. 13, 1066-1074.
14. Brazeau, P., Vale, W., Burgus, R., Ling, N., Butcher, M., Rivier, J., et al. (1973). Hypothalamic polypep-tide that inhibits the secretion of immunoreactive pituitary growth hormone. Science 179, 77-79.
15. Brecht, W. J., Harris, E M., Chang, S., Tesseur, I., Yu, G. Q., Xu, Q., et al. (2004). Neuron-specific apolipoprotein e4 proteolysis is associated with increased tau phosphory-lation in brains of transgenic mice. J. Neurosci. 24, 2527-2534.
16. Brunjes, P. C., Kay, R. B., and Arrivil-laga, J. P. (2011). The mouse olfactory peduncle. J. Comp. Neurol. 519, 2870-2886.
17. Buckmaster, P. S., Otero-Corchon, V., Rubinstein, M., and Low, M. J. (2002). Heightened seizure severity in somatostatin knockout mice. Epilepsy Res. 48, 43-56.
18. Butler, R. K., White, L. C., Frederick-Duus, D., Kaigler, K. F., Fadel, J. R., and Wilson, M. A. (2012). Comparison of the activation of somatostatin- and neuropeptide Y-containing neuronal populations of the rat amygdala following two different anxiogenic stressors. Exp. Neurol. 238, 52-63.
19. Cammalleri, M., Cervia, D., Dal Monte, M., Martini, D., Langenegger, D., Fehlmann, D., et al. (2006). Compensatory changes in the hippocampus of somatostatin knockout mice: upregulation of somatostatin receptor 2 and its function in the control of bursting activity and synaptic transmission. Eur. J. Neurosci. 23, 2404-2422.
20. Cammalleri, M., Cervia, D., Langenegger, D., Liu, Y., Dal Monte, M., Hoyer, D., et al. (2004). Somatostatin receptors differentially affect spontaneous epileptiform activity in mouse hippocampal slices. Eur. J. Neurosci. 20, 2711-2721.
21. Cammalleri, M., Martini, D., Timperio, A. M., and Bagnoli, P. (2009). Functional effects of somatostatin receptor 1 activation on synaptic transmission in the mouse hippocampus. J. Neurochem. 111, 1466-1477.
22. Casini, G., Catalani, E., Dal Monte, M., and Bagnoli, P. (2005). Functional aspects of the somatostatinergic system in the retina and the potential therapeutic role of somatostatin in retinal disease. Histol. Histopathol. 20, 615-632.
23. Cervia, D., and Bagnoli, P. (2007). An update on somatostatin receptor signaling in native systems and new insights on their patho-physiology. Pharmacol. Ther. 116, 322-341.
24. Cervia, D., Casini, G., and Bagnoli, P. (2008). Physiology and pathology of somatostatin in the mammalian retina: a current view. Mol. Cell. Endocrinol. 286, 112-122.
25. Choi, Y. S., Lin, S. L., Lee, B., Kurup, P., Cho, H.Y., Naegele, J. R., et al. (2007). Status epilepticus-induced somatostatinergic hilar interneuron degeneration is regulated by striatal enriched protein tyrosine phosphatase. J. Neurosci. 27, 2999-3009.
26. Córdoba-Chacón, J., Gahete, M. D., Durán-Prado, M., Luque, R. M., and Castaño, J. P. (2011). Truncated somatostatin receptors as new players in somatostatin-cortistatin patho-physiology. Ann. N. Y.Acad. Sci. 1220, 6-15.
27. Cossart, R., Dinocourt, C., Hirsch, J. C., Merchan-Perez, A., De Felipe, J., Ben-Ari, Y., et al. (2001). Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 4, 52-62.
28. Csaba, Z., Peineau, S., and Dournaud, P. (2012). Molecular mechanisms of somatostatin receptor trafficking. J. Mol. Endocrinol. 48, R1-R12.
29. Dal Monte, M., Cammalleri, M., Martini, D., Casini, G., and Bagnoli, P. (2007). Antiangiogenic role of somatostatin receptor 2 in a model of hypoxia-induced neovascularization in the retina: results from transgenic mice. Invest. Ophthalmol. Vis. Sci. 48, 3480-3489.
30. Dal Monte, M., Ristori, C., Cammalleri, M., and Bagnoli, P. (2009). Effects of somatostatin analogues on retinal angiogenesis in a mouse model of oxygen-induced retinopa-thy: involvement of the somatostatin receptor subtype 2. Invest. Ophthalmol. Vis. Sci. 50, 3596-3606.
31. Davies, P., Katzman, R., and Terry, R. D. (1980). Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa. Nature 288, 279-280.
32. de Bundel, D., Aourz, N., Kiagiadaki, F., Clinckers, R., Hoyer, D., Kastellakis, A., et al. (2010). Hippocampal sst(1) receptors are autoreceptors and do not affect seizures in rats. Neuroreport 21, 254-258.
33. de Lanerolle, N. C., Kim, J. H., Rob-bins, R. J., and Spencer, D. D. (1989). Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 495, 387-395.
34. de Lecea, L. (2008). Cortistatin - functions in the central nervous system. Mol. Cell. Endocrinol. 286, 88-95.
35. De Lecea, L., Criado, J. R., Prospero-Garcia, O., Gautvik, K. M., Schweitzer, P., Danielson, P. E., et al. (1996). A cortical neuropeptide with neuronal depressant and sleep-modulating properties. Nature 381, 242-245.
36. DeNoble, V. J., Hepler, D. J., and Barto, R. A. (1989). Cysteamine-induced depletion of somatostatin produces differential cognitive deficits in rats. Brain Res. 482, 42-48.
37. Dournaud, P., Delaere, P., Hauw, J. J., and Epelbaum, J. (1995). Differential correlation between neurochemical deficits, neuropathology, and cognitive status in Alzheimer's disease. Neurobiol. Aging 16, 817-823.
38. Dutar, P., Vaillend, C., Viollet, C., Bil-lard, J. M., Potier, B., Carlo, A. S., et al. (2002). Spatial learning and synaptic hippocampal plasticity in type 2 somatostatin receptor knock-out mice. Neuroscience 112, 455-466.
39. Einstein, E. B., Patterson, C. A., Hon, B. J., Regan, K. A., Reddi, J., Melnikoff, D. E., et al. (2010). Somatostatin signaling in neuronal cilia is critical for object recognition memory. J. Neurosci. 30, 4306-4314.
40. Engin, E., Stellbrink, J., Treit, D., and Dickson, C. (2008a). Anx-iolytic and antidepressant effects of intracerebroventricularly administered somatostatin: behavioral and neurophysiological evidence. Neuroscience 157, 666-676.
41. Engin, E., Stellbrink, J., Treit, D., and Dickson, C. T. (2008b). Anx-iolytic and antidepressant effects of intracerebroventricularly administered somatostatin: behavioral and neurophysiological evidence. Neuroscience 157, 666-676.
42. 3 receptors. Psychopharmacology (Berl.) 206, 281-289.
43. Epelbaum, J. (1986). Somatostatin in the central nervous system: physiology and pathological modifications. Prog. Neurobiol. 27, 63-100.
44. Epelbaum, J., Agid, F., Agid, Y., Beaudet, A., Bertrand, P., Enjalbert, A., et al. (1989). Somatostatin receptors in brain and pituitary. Horm. Res. 31, 45-50.
45. Epelbaum, J., Guillou, J. L., Gastambide, F., Hoyer, D., Duron, E., and Viollet, C. (2009). Somatostatin, Alzheimer's disease and cognition: an old story coming of age? Prog. Neurobiol. 89, 153-161.
46. Eyre, M. D., Kerti, K., and Nusser, Z. (2009). Molecular diversity of deep short-axon cells of the rat main olfactory bulb. Eur. J. Neurosci. 29, 1397-1407.
47. Ferrier, I. N., Roberts, G. W., Crow, T. J., Johnstone, E. C., Owens, D. G., Lee, Y. C., et al. (1983). Reduced cholecystokinin-like and somatostatin-like immunoreactivity in limbic lobe is associated with nega tive symptoms in schizophrenia. Life Sci. 33, 475-482.
48. Fillman, S. G., Cloonan, N., Catts, V S., Miller, L. C., Wong, J., Mccrossin, T., et al. (2012). Increased inflammatory markers identified in the dorsolateral prefrontal cortex of individuals with schizophrenia. Mol. Psychiatry. doi: 10.1038/mp.2012.110 [Epub ahead of print].
49. Fino, E., andYuste, R. (2011). Dense inhibitory connectivity in neocortex. Neuron 69, 1188-1203.
50. Florio, P., Abella, R., Marinoni, E., Di Iorio, R., Letizia, C., Meli, M., et al. (2008). Adrenomedullin blood concentrations in infants subjected to cardiopulmonary bypass: correlation with monitoring parameters and prediction of poor neurological outcome. Clin. Chem. 54, 202-206.
51. Gahete, M. D., Rubio, A., Duran-Prado, M., Avila, J., Luque, R. M., and Castano, J. P. (2010). Expression of Somatostatin, cortistatin, and their receptors, as well as dopamine receptors, but not of neprilysin, are reduced in the temporal lobe of Alzheimer's disease patients. J. Alzheimers Dis. 20, 465-475.
52. Galarraga, E., Vilchis, C., Tkatch, T., Salgado, H., Tecuapetla, F., Perez-Rosello, T., et al. (2007). Somatostatinergic modulation of firing pattern and calcium-activated potassium currents in medium spiny neostriatal neurons. Neuroscience 146, 537-554.
53. Gastambide, F., Lepousez, G., Viollet, C., Loudes, C., Epelbaum, J., and Guillou, J. L. (2010). Cooperation between hippocampal somatostatin receptor subtypes 4 and 2: functional relevance in interactive memory systems. Hippocampus 20, 745-757.
54. Gastambide, F., Viollet, C., Lepousez, G., Epelbaum, J., and Guillou, J. L. (2009). Hippocampal SSTR4 somatostatin receptors control the selection of memory strategies. Psychopharmacology (Berl.) 202, 153-163.
55. Genin, E., Hannequin, D., Wallon, D., Sleegers, K., Hiltunen, M., Com-barros, O., et al. (2011). APOE and Alzheimer disease: a major gene with semi-dominant inheritance. Mol. Psychiatry 16, 903-907.
56. Gentet, L. J., Kremer, Y., Taniguchi, H., Huang, Z. J., Staiger, J. F., and Petersen, C. C. (2012). Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607-612.
57. Gleichmann, M., Zhang, Y., Wood, W. H. III, Becker, K. G., Mughal, M. R., Pazin, M. J., et al. (2012). Molecular changes in brain aging and Alzheimer's disease are mirrored in experimentally silenced cortical neuron networks. Neurobiol. Aging 33, 205.e201-205.e218.
58. Glorioso, C., Oh, S., Douillard, G. G., and Sibille, E. (2011). Brain molecular aging, promotion of neurological disease and modulation by sirtuin 5 longevity gene polymorphism. Neurobiol. Dis. 41, 279-290.
59. Goldberg, J. H., Lacefield, C. O., and Yuste, R. (2004). Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting.J. Physiol. 558, 465-478.
60. Goldin, M., Epsztein, J., Jorquera, I., Represa, A., Ben-Ari, Y., Crepel, V., et al. (2007). Synaptic kainate receptors tune oriens-lacunosum molecu-lare interneurons to operate at theta frequency. J. Neurosci. 27, 9560-9572.
61. Gonchar, Y., Wang, Q., and Burkhal-ter, A. (2007). Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front. Neuroanat. 1, 1-11.
62. Gray, P. A., Hayes, J. A., Ling, G. Y., Llona, I., Tupal, S., Picardo, M. C. D., et al. (2010). Developmental origin of preBötzinger complex respiratory neurons. J. Neurosci. 30, 14883-14895.
63. 2 receptors linked to the adenylyl cyclase-protein kinase A pathway. Neuropharmacology 46, 388-396.
64. Grouselle, D., Winsky-Sommerer, R., David, J. P., Delacourte, A., Dour-naud, P., and Epelbaum, J. (1998). Loss of somatostatin-like immunore-activity in the frontal cortex of Alzheimer patients carrying the apolipoprotein epsilon 4 allele. Neurosci. Lett. 255, 21-24.
65. Guillou, J. L., Micheau, J., and Jaffard, R. (1993). Effects of intrahippocam-pal injections of somatostatin and cysteamine on spatial discrimination learning in mice. Psychobiology 21, 265-271.
66. Guillou, J. L., Micheau, J., and Jaffard, R. (1998). The opposite effects of cysteamine on the acquisition of two different tasks in mice are associated with bidirectional testing-induced changes in hippocampal adenylyl cyclase activity. Behav. Neurosci. 112, 900-908.
67. Guilloux, J. P., Douillard-Guilloux, G., Kota, R., Wang, X., Gardier, A. M., Martinowich, K., et al. (2011). Molecular evidence for BDNF- and GABA-related dysfunctions in the amygdala of female subjects with major depression. Mol. Psychiatry 17, 1130-1142.
68. Hannon, J.P., Petrucci, C., Fehlmann, D., Viollet, C.,Epelbaum, J.,and Hoyer, D.(2002). Somatostatinsst2 receptor knock-outmice:localisation of sst1-5 receptor mRNA and binding in mouse brain by semi-quantitative RT-PCR, in situ hybridisation his-tochemistry and receptor autora-diography. Neuropharmacology 42, 396-413.
69. Haroutunian, V., Kanof, P. D., and Davis, K. L. (1989). Interactions of forebrain cholinergic and somatostatinergic systems in the rat. Brain Res. 496, 98-104.
70. Haroutunian, V., Mantin, R., Campbell, G. A., Tsuboyama, G. K., and Davis, K. L. (1987). Cysteamine-induced depletion of central somatostatin-like immunoactivity: effects on behavior, learning, memory and brain neuro-chemistry. Brain Res. 403, 234-242.
71. Harris, E M., Brecht, W J., Xu, Q., Tesseur, I., Kekonius, L., Wyss-Coray, T., et al. (2003). Carboxyl-terminal-truncated apolipoprotein E4 causes Alzheimer's disease-like neuro degeneration and behavioral deficits in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 100, 10966-10971.
72. Hashimoto, T., Arion, D., Unger, T., Maldonado-Aviles, J. G., Morris, H. M., Volk, D. W., et al. (2008). Alterations in GABA-related transcrip-tome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol. Psychiatry 13, 147-161.
73. Hathway, G. J., Humphrey, P. P., and Kendrick, K. M. (2004). Somatostatin induces striatal dopamine release and contralateral turning behaviour in the mouse. Neurosci. Lett. 358, 127-131.
74. Havlicek, V., Rezek, M., and Friesen, H. (1976). Somatostatin and thy-rotropin releasing hormone: central effect on sleep and motor system. Pharmacol. Biochem. Behav. 4, 455-459.
75. Horgan, J., Miguel-Hidalgo, J. J., Thrasher, M., and Bissette, G. (2007). Longitudinal brain corticotropin releasing factor and somatostatin in a transgenic mouse (TG2576) model of Alzheimer's disease. J. Alzheimers Dis. 12, 115-127.
76. Hu, H., Ma, Y., and Agmon, A. (2011). Submillisecond firing synchrony between different subtypes of cortical interneurons connected chemically but not electrically. J. Neurosci. 31, 3351-3361.
77. Huang, Y., Liu, X. Q., Wyss-Coray, T., Brecht, W J., Sanan, D. A., and Mahley, R.W (2001). Apolipoprotein E fragments present in Alzheimer's disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons. Proc. Natl. Acad. Sci. U.S.A. 98, 8838-8843.
78. Hwang, I. K., Lee, J. C., Park, S.-K., An, S.-J., Lee, H. Y., Lee, Y.-B., et al. (2004). Age-related change of somatostatin-immunoreactive neurones in the main olfactory bulb of the rat. Anat. Histol. Embryol. 33, 59-63.
79. Ishibashi, H., and Akaike, N. (1995). Somatostatin modulates high-voltage-activated Ca2+ channels in freshly dissociated rat hippocampal neurons. J. Neurophysiol. 74, 1028-1036.
80. Iwata, N., Higuchi, M., and Saido, T. C. (2005). Metabolism of amyloid-beta peptide and Alzheimer's disease. Pharmacol. Ther. 108, 129-148.
81. Jeneson, A., and Squire, L. R. (2012). Working memory, long-term memory, and medial temporal lobe function. Learn. Mem. 19, 15-25.
82. Jiang, N., Furue, H., Katafuchi, T., and Yoshimura, M. (2003). Somatostatin directly inhibits substantia gelatinosa neurons in adult rat spinal dorsal horn in vitro. Neurosci. Res. 47, 97-107.
83. Jinno, S., Klausberger, T., Marton, L. F., Dalezios, Y., Roberts, J. D., Fuentealba, P., et al. (2007). Neuronal diversity in GABAergic long-range projections from the hippocampus. J. Neurosci. 27, 8790-8804.
84. Jolkkonen, J., Kahkonen, K., and Pitkanen, A. (1997). Cholinergic deafferentation exacerbates seizure-induced loss of somatostatin-immunoreactive neurons in the rat hippocampus. Neuroscience 80, 401-411.
85. Kapfer, C., Glickfeld, L. L., Atallah, B. V., and Scanziani, M. (2007). Supra-linear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat. Neurosci. 10, 743-753.
86. Kawaguchi, Y., and Kubota, Y. (1998). Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85, 677-701.
87. Kiagiadaki, F., Savvaki, M., and Thermos, K. (2010). Activation of somatostatin receptor (sst 5) protects the rat retina from AMPA-induced neu-rotoxicity. Neuropharmacology 58, 297-303.
88. 2 analogs on AMPA-induced neurotoxicity in rat retina. Invest. Ophthalmol. Vis. Sci. 49, 3080-3089.
89. Kokona, D., Mastrodimou, N., Pedi-aditakis, I., Charalampopoulos, I., Schmid, H. A., and Thermos, K. (2012). Pasireotide (SOM230) protects the retina in animal models of ischemia induced retinopathies. Exp. Eye Res. 103, 90-98.
90. Konradi, C., Yang, C. K., Zimmerman, E. I., Lohmann, K. M., Gresch, P., Pantazopoulos, H., et al. (2011). Hip-pocampal interneurons are abnormal in schizophrenia. Schizophr. Res. 131, 165-173.
91. Kosaka, K., and Kosaka, T. (2007). Chemical properties of type 1 and type 2 periglomerular cells in the mouse olfactory bulb are different from those in the rat olfactory bulb. Brain Res. 1167, 42-55.
92. Krantic, S., Robitaille, Y., and Quirion, R. (1992). Deficits in the somatostatin SS1 receptor sub-type in frontal and temporal cortices in Alzheimer's disease. Brain Res. 573, 299-304.
93. Kumar, U. (2005). Expression of somatostatin receptor subtypes (SSTR1-5) in Alzheimer's disease brain: an immunohistochemical analysis. Neuroscience 134, 525-538.
94. Lahlou, H., Guillermet, J., Hortala, M., Vernejoul, F., Pyronnet, S., Bousquet, C., et al. (2004). Molecular signaling of somatostatin receptors. Ann. N. Y. Acad.Sci. 1014, 121-131.
95. Lamirault, L., Guillou, J. L., Micheau, J., and Jaffard, R. (2001). Intrahip-pocampal injections of somatostatin dissociate acquisition from the flexible use of place responses. Eur. J. Neurosci. 14, 567-570.
96. Lavezzi, A. M., and Matturri, L. (2008). Functional neuroanatomy of the human pre-Bötzinger complex with particular reference to sudden unexplained perinatal and infant death. Neuropathology 28, 10-16.
97. Lepousez, G., Csaba, Z., Bernard, V., Loudes, C., Videau, C., Lacombe, J., et al. (2010a). Somatostatin interneurons delineate the inner part of the external plexiform layer in the mouse main olfactory bulb. J. Comp. Neurol. 518, 1976-1994.
98. Lepousez, G., Mouret, A., Loudes, C., Epelbaum, J., and Viollet, C. (2010b). Somatostatin contributes to in vivo gamma oscillation modulation and odor discrimination in the olfactory bulb. J. Neurosci. 30, 870-875.
99. Leresche, N., Asprodini, E., Emri, Z., Cope, D. W., and Crunelli, V. (2000). Somatostatin inhibits GABAergic transmission in the sensory thalamus via presynaptic receptors. Neuroscience 98, 513-522.
100. Levinson, A. J., Fitzgerald, P. B., Favalli, G., Blumberger, D. M., Daigle, M., andDaskalakis, Z. J. (2010). Evidence of cortical inhibitory deficits in major depressive disorder. Biol. Psychiatry 67, 458-464.
101. Llona, I., and Eugenín, J. (2005). Central actions of somatostatin in the generation and control of breathing. Biol. Res. 38, 347-352.
102. Lopez-Huerta, V. G., Blanco-Hernandez, E., Bargas, J., and Galarraga, E. (2012). Presynaptic modulation by somatostatin in the rat neostriatum is altered in a model of Parkinsonism. J. Neurophysiol. 108, 1032-1043.
103. Lopez-Huerta, V. G., Tecuapetla, F., Guzman, J. N., Bargas, J., and Galarraga, E. (2008). Presynaptic modulation by somatostatin in the neostriatum. Neurochem. Res. 33, 1452-1458.
104. Ma, Y., Hu, H., Berrebi, A. S., Mathers, P. H., and Agmon, A. (2006). Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26, 5069-5082.
105. Mastrodimou, N., Lambrou, G. N., and Thermos, K. (2005). Effect of somatostatin analogues on chemically induced ischaemia in the rat retina. Naunyn Schmiedebergs Arch. Pharmacol. 371, 44-53.
106. McCarthy, A. D., Owens, I. J., Bansal, A. T., Mctighe, S. M., Bussey, T. J., and Saksida, L. M. (2011). FK962 and donepezil act synergistically to improve cognition in rats: potential as an add-on therapy for Alzheimer's disease. Pharmacol. Biochem. Behav. 98, 76-80.
107. McDonald, A. J., Mascagni, F., and Zaric, V. (2012). Subpopulations of somatostatin-immunoreactive non-pyramidal neurons in the amygdala and adjacent external capsule project to the basal forebrain: evidence for the existence of GABAergic projection neurons in the cortical nuclei and basolateral nuclear complex. Front. Neural Circuits 6:46. doi: 10.3389/fncir.2012.00046
108. McGarry, L. M., Packer, A. M., Fino, E., Nikolenko, V., Sippy, T., and Yuste, R. (2010). Quantitative classification of somatostatin-positive neocortical interneurons identifies three interneuron subtypes. Front. Neural Circuits 4:12. doi: 10.3389/fncir.2011.00012
109. Melzer, S., Michael, M., Caputi, A., Eliava, M., Fuchs, E. C., Whitting-ton, M. A., et al. (2012). Long-range-projecting GABAergic neurons modulate inhibition in hippocampus and entorhinal cortex. Science 335, 1506-1510.
110. Mendez-Diaz, M., Irwin, L., Gomez-Chavarin, M., Jimenez-Anguiano, A., Cabeza, R., Murillo-Rodriguez, E., et al. (2005). Cortistatin modulates memory evocation in rats. Eur. J. Pharmacol. 507, 21-28.
111. Momiyama, T., and Zaborszky, L. (2006). Somatostatin presynaptically inhibits both GABA and gluta-mate release onto rat basal forebrain cholinergic neurons. J. Neurophysiol. 96, 686-694.
112. Moneta, D., Richichi, C., Aliprandi, M., Dournaud, P., Dutar, P., Billard, J. M., et al. (2002). Somatostatin receptor subtypes 2 and 4 affect seizure susceptibility and hippocampal excitatory neurotransmission in mice. Eur. J. Neurosci. 16, 843-849.
113. Moore, S. D., Madamba, S. G., Joels, M., and Siggins, G. R. (1988). Somatostatin augments the M-current in hippocampal neurons. Science 239, 278-280.
114. Nanda, S. A., Qi, C., Roseboom, P. H., and Kalin, N. H. (2008). Predator stress induces behavioral inhibition and amygdala somatostatin receptor 2 gene expression. Genes Brain Behav. 7, 639-648.
115. Nilsson, A., Falth, M., Zhang, X., Kul-tima, K., Skold, K., Svenningsson, P., et al. (2009). Striatal alterations of secretogranin-1, somatostatin, pro-dynorphin, and cholecystokinin pep-tides in an experimental mouse model of Parkinson disease. Mol. Cell. Proteomics 8, 1094-1104.
116. Olias, G., Viollet, C., Kusserow, H., Epelbaum, J., and Meyerhof, W. (2004). Regulation and function of somatostatin receptors. J. Neurochem. 89, 1057-1091.
117. Oliva, A. A. Jr., Jiang, M., Lam, T., Smith, K. L., and Swann, J. W. (2000). Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J. Neurosci. 20, 3354-3368.
118. Pantaleo, T., Mutolo, D., Cinelli, E., and Bongianni, F. (2011). Respiratory responses to somatostatin microin-jections into the Bötzinger complex and the pre-Bötzinger complex of the rabbit. Neurosci. Lett. 498, 26-30.
119. 2 somatostatin receptor interaction in rat hypothalamus requires activation of NMDA and/or metabotropic glu-tamate receptors and depends on intracellular calcium. J. Physiol. 546, 101-117.
120. Perez-Santiago, J., Diez-Alarcia, R., Callado, L. F., Zhang, J. X., Chana, G., White, C. H., et al. (2012). A combined analysis of microar-ray gene expression studies of the human prefrontal cortex identifies genes implicated in schizophrenia. J. Psychiatr. Res. 46, 1464-1474.
121. Perrenoud, Q., Rossier, J., Geoffroy, H., Vitalis, T., and Gallopin, T. (2012). Diversity of GABAergic interneurons in layer VIa and VIb of mouse barrel cortex. Cereb. Cortex. doi: 10.1093/cercor/bhs032 [Epub ahead of print].
122. Picardo, M. A., Guigue, P., Bonifazi, P., Batista-Brito, R., Allene, C., Ribas, A., et al. (2011). Pioneer GABA cells comprise a subpopulation of hub neurons in the developing hippocampus. Neuron 71, 695-709.
123. Pinter, E., Helyes, Z., and Szolcsanyi, J. (2006). Inhibitory effect of somatostatin on inflammation and nocicep-tion. Pharmacol. Ther. 112, 440-456.
124. Qiu, C., Zeyda, T., Johnson, B., Hochgeschwender, U., De Lecea, L., and Tallent, M. K. (2008). Somatostatin receptor subtype 4 couples to the M-current to regulate seizures. J. Neurosci. 28, 3567-3576.
125. Radojevic, V., Hanusek, C., Setz, C., Brand, Y., Kapfhammer, J. P., and Bodmer, D. (2011). The somatostatinergic system in the mammalian cochlea. BMC Neurosci. 12: doi: 10.1186/1471-2202-12-89
126. Ramírez-Jarquín, J. O., Lara-Hernández, S., López-Guerrero, J. J., Aguileta, M. A., Rivera-Angulo, A. J., Sampieri, A., et al. (2012). Somatostatin modulates generation of inspiratory rhythms and determines asphyxia survival. Peptides 34, 360-372.
127. Ramos, B., Baglietto-Vargas, D., Del Rio, J. C., Moreno-Gonzalez, I., Santa-Maria, C., Jimenez, S., et al. (2006). Early neuropathology of somato-statin/NPY GABAergic cells in the hippocampus of a PS1xAPP transgenic model of Alzheimer's disease. Neurobiol. Aging 27, 1658-1672.
128. Rat, D., Schmitt, U., Tippmann, F., Dewachter, I., Theunis, C., Wiecz-erzak, E., et al. (2011). Neuropeptide pituitary adenylate cyclase-activating polypeptide (PACAP) slows down Alzheimer's disease-like pathology in amyloid precursor protein-transgenic mice. FASEB J. 25, 3208-3218.
129. Raynor, K., Lucki, I., and Reisine, T. (1993). Somatostatin receptors in the nucleus accumbens selectively mediate the stimulatory effect of somatostatin on locomotor activity in rats. J. Pharmacol. Exp. Ther. 265, 67-73.
130. Robbins, R. J., Brines, M. L., Kim, J. H., Adrian, T., De Lanerolle, N., Welsh, S., et al. (1991). A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy. Ann. Neurol. 29, 325-332.
131. Roberts, G. W., Ferrier, I. N., Lee, Y., Crow, T. J., Johnstone, E. C., Owens, D. G., et al. (1983). Peptides, the lim-bic lobe and schizophrenia. Brain Res. 288, 199-211.
132. Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., et al. (2012). Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 15, 769-775.
133. Rubio, A., Perez, M., De Lecea, L., and Avila, J. (2008). Effect of cortistatin on tau phosphorylation at Ser262 site. J. Neurosci. Res. 86, 2462-2475.
134. Rubio, A., Sanchez-Mut, J. V., Garcia, E., Velasquez, Z. D., Oliver, J., Esteller, M., et al. (2012). Epigenetic control of somatostatin and cortistatin expression by beta amyloid peptide. J. Neurosci. Res. 90, 13-20.
135. Rudy, B., Fishell, G., Lee, S., and Hjerling-Leffler, J. (2011). Three groups of interneurons account for nearly 100% of neocortical GABAer-gic neurons. Dev. Neurobiol. 71, 45-61.
136. Saito, T., Iwata, N., Tsubuki, S., Takaki, Y., Takano, J., Huang, S. M., et al. (2005). Somatostatin regulates brain amyloid beta peptide Abeta42 through modulation of proteolytic degradation. Nat. Med. 11, 434-439.
137. Saiz-Sanchez, D., Ubeda-Banon, I., De La Rosa-Prieto, C., Argandona-Palacios, L., Garcia-Munozguren, S., Insausti, R., et al. (2010). Somatostatin, tau, and beta-amyloid within the anterior olfactory nucleus in Alzheimer disease. Exp. Neurol. 223, 347-350.
138. Saiz-Sanchez, D., Ubeda-Banon, I., De La Rosa-Prieto, C., and Martinez-Marcos, A. (2012). Differential expression of interneuron populations and correlation with amyloid-beta deposition in the olfactory cortex of an AbetaPP/PS1 transgenic mouse model of Alzheimer's disease. J. Alzheimers Dis. 31, 113-129.
139. Samson, W. K., Zhang, J. V., Avsian-Kretchmer, O., Cui, K., Yosten, G. L., Klein, C., et al. (2008). Neurono-statin encoded by the somatostatin gene regulates neuronal, cardiovascular, and metabolic functions. J. Biol. Chem. 283, 31949-31959.
140. Sanchez-Alavez, M., Gomez-Chavarin, M., Navarro, L., Jimenez-Anguiano, A., Murillo-Rodriguez, E., Prado-Alcala, R. A., et al. (2000). Cortistatin modulates memory processes in rats. Brain Res. 858, 78-83.
141. Sandoval, K. E., Farr, S. A., Banks, W. A., Niehoff, M. L., Morley, J. E., Crider, A. M., et al. (2011). Chronic peripheral administration of somatostatin receptor subtype-4 agonist NNC 26-9100 enhances learning and memory in SAMP8 mice. Eur. J. Pharmacol. 654, 53-59.
142. Savonenko, A., Xu, G. M., Melnikova, T., Morton, J. L., Gonzales, V., Wong, M. P., et al. (2005). Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis. 18, 602-617.
143. Schettini, G., Florio, T., Magri, G., Grimaldi, M., Meucci, O., Lan-dolfi, E., et al. (1988). Somatostatin and SMS 201-995 reverse the impairment of cognitive functions induced by cysteamine depletion of brain somatostatin. Eur. J. Pharmacol. 151, 399-407.
144. Schumann, C. M., Bauman, M. D., and Amaral, D. G. (2011). Abnormal structure or function of the amygdala is a common component of neurodevelopmental disorders. Neu-ropsychologia 49, 745-759.
145. Schwarzacher, S. W., Rüb, U., and Deller, T. (2011). Neuroanatomical characteristics of the human pre-Bötzinger complex and its involvement in neu-rodegenerative brainstem diseases. Brain 134, 24-35.
146. Schweitzer, P., Madamba, S. G., and Siggins, G. R. (1998). Somatostatin increases a voltage-insensitive K+ conductance in rat CA1 hippocampal neurons. J. Neurophysiol. 79, 1230-1238.
147. Shipley, M. T., and Ennis, M. (1996). Functional organization of olfactory system. J. Neurobiol. 30, 123-176.
148. Sibille, E., Morris, H. M., Kota, R. S., and Lewis, D. A. (2011). GABA-related transcripts in the dorsolateral prefrontal cortex in mood disorders. Int. J. Neuropsychopharmacol. 14, 721-734.
149. Siehler, S., Nunn, C., Hannon, J., Feuer-bach, D., and Hoyer, D. (2008). Pharmacological profile of somatostatin and cortistatin receptors. Mol Cell. Endocrinol. 286, 26-34.
150. Silberberg, G., and Markram, H. (2007). Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735-746.
151. Sousa, V. H., Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., and Fishell, G. (2009). Characterization of Nkx6-2-derived neocortical interneuron lineages. Cereb. Cortex 19(Suppl. 1), i1-i10.
152. 5 in areas of the rat medulla oblongata involved in autonomic regulation. J. Chem. Neuroanat. 35, 49-66.
153. Stanic, D., Malmgren, H., He, H., Scott, L., Aperia, A., and Hökfelt, T. (2008). Developmental changes in frequency of the ciliary somatostatin receptor 3 protein. Brain Res. 1249, 101-112.
154. Stanley, E. M., Fadel, J. R., and Mott, D. D. (2012). Interneuron loss reduces dendritic inhibition and GABA release in hippocampus of aged rats. Neurobiol. Aging 33, 431.e1-13.
155. Stornetta, R. L., Rosin, D. L., Wang, H., Sevigny, C. P., Weston, M. C., and Guyenet, P. G. (2003). A group of glutamatergic interneurons expressing high levels of both neurokinin-1 receptors and somatostatin identifies the region of the pre-Bötzinger complex. J. Comp. Neurol. 455, 499-512.
156. Stumm, R. K., Zhou, C., Schulz, S., Endres, M., Kronenberg, G., Allen, J. P., et al. (2004). Somatostatin receptor 2 is activated in cortical neurons and contributes to neurodegenera-tion after focal ischemia. J. Neurosci. 24, 11404-11415.
157. Suzuki, N., and Bekkers, J. M. (2010). Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piri-form cortex. Cereb. Cortex 20, 2971-2984.
158. Szabo, S., and Reichlin, S. (1981). Somatostatin in rat tissues is depleted by cysteamine administration. Endocrinology 109, 2255-2257.
159. Tahvildari, B., Wölfel, M., Duque, A., and Mccormick, D. A. (2012). Selective functional interactions between excitatory and inhibitory cortical neurons and differential contribution to persistent activity of the slow oscillation. J. Neurosci. 32, 12165-12179.
160. Tallent, M. K., Fabre, V., Qiu, C., Cal-bet, M., Lamp, T., Baratta, M. V., et al. (2005). Cortistatin overexpression in transgenic mice produces deficits in synaptic plasticity and learning. Mol. Cell. Neurosci. 30, 465-475.
161. Tallent, M. K., and Qiu, C. (2008). Somatostatin: an endogenous antiepileptic. Mol. Cell. Endocrinol. 286, 96-103.
162. Tallent, M. K., and Siggins, G. R. (1997). Somatostatin depresses excitatory but not inhibitory neurotransmission in rat CA1 hippocampus. J. Neurophysiol. 78, 3008-3018.
163. Tamminga, C. A., Foster, N. L., Fedio, P., Bird, E. D., and Chase, T. N. (1987). Alzheimer's disease: low cerebral somatostatin levels correlate with impaired cognitive function and cortical metabolism. Neurology 37, 161-165.
164. Tan, W, Lanczewski, W A., Yang, P., Shao, X. M., Callaway, E. M., and Feldman, J. L. (2008). Silencing preBötzinger Complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nat. Neurosci. 11, 538-540.
165. Tan, W., Pagliardini, S., Yang, P., Janczewski, W. A., and Feldman, J. L. (2010). Projections of preBötzinger complex neurons in adult rats. J. Comp. Neurol. 518, 1862-1878.
166. Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., et al. (2011). A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995-1013.
167. Tashev, R., Belcheva, S., Milenov, K., and Belcheva, I. (2001). Behavioral effects of somatostatin microinjected into caudate putamen. Neuropeptides 35, 271-275.
168. Thermos, K. (2003). Functional mapping of somatostatin receptors in the retina: a review. Vision Res. 43, 1805-1815.
169. 1 receptor: an autoreceptor for somatostatin in brain and retina? Pharmacol. Ther. 110, 455-464.
170. Tomioka, R., Okamoto, K., Furuta, T., Fujiyama, F., Iwasato, T., Yanagawa, Y., et al. (2005). Demonstration of long-range GABAergic connections distributed throughout the mouse neocortex. Eur. J. Neurosci. 21, 1587-1600.
171. Tripp, A., Kota, R. S., Lewis, D. A., and Sibille, E. (2011). Reduced somatostatin in subgenual anterior cingulate cortex in major depression. Neurobiol. Dis. 42, 116-124.
172. Vanetti, M., Kouba, M., Wang, X., Vogt, G., and Höllt, V. (1992). Cloning and expression of a novel mouse somatostatin receptor (SSTR2B). FEBS Lett. 311, 290-294.
173. Vecsei, L., Alling, C., and Widerlov, E. (1990). Comparative studies of intracerebroventricularly administered cysteamine and pantethine in different behavioral tests and on brain catecholamines in rats. Arch. Int. Pharmacodyn. Ther. 305, 140-151.
174. Vecsei, L., Bollok, I., and Telegdy, G. (1983). Intracerebroventricular somatostatin attenuates electrocon-vulsive shock-induced amnesia in rats. Peptides 4, 293-295.
175. Vecsei, L., Kiraly, C., Bollok, I., Nagy, A., Varga, J., Penke, B., et al. (1984). Comparative studies with somatostatin and cysteamine in different behavioral tests on rats. Pharmacol. Biochem. Behav. 21, 833-837.
176. Vecsei, L., and Widerlov, E. (1988). Effects of intracerebroventricularly administered somatostatin on passive avoidance, shuttle-boxbehaviour and open-field activity in rats. Neu-ropeptides 12, 237-242.
177. Vepsalainen, S., Helisalmi, S., Koivisto, A. M., Tapaninen, T., Hiltunen, M., and Soininen, H. (2007). Somato-statin genetic variants modify the risk for Alzheimer's disease among Finnish patients. J. Neurol. 254, 1504-1508.
178. Vezzani, A., andHoyer, D. (1999). Brain somatostatin: a candidate inhibitory role in seizures and epileptogenesis. Eur. I Neurosci. 11, 3767-3776.
179. Villette, V., Poindessous-Jazat, F., Bel-lessort, B., Roullot, E., Peterschmitt, Y., Epelbaum, J., et al. (2012). A new neuronal target for beta-amyloid peptide in the rat hippocampus. Neu-robiol. Aging 33, 1126.e1121-1114.
180. Villette, V., Poindessous-Jazat, F., Simon, A., Lena, C., Roullot, E., Bel-lessort, B., et al. (2010). Decreased rhythmic GABAergic septal activity and memory-associated theta oscillations after hippocampal amyloid-beta pathology in the rat. J. Neurosci. 30, 10991-11003.
181. Viollet, C., Lepousez, G., Loudes, C., Videau, C., Simon, A., and Epelbaum, J. (2008). Somatostatinergic systems in brain: networks and functions. Mol. Cell. Endocrinol. 286, 75-87.
182. 2 somatostatin receptor in locomotor, exploratory activity and emotional reactivity in mice. Eur. J. Neurosci. 12, 3761-3770.
183. Wang, J. Z., Grundke-Iqbal, I., and Iqbal, K. (2007). Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur. J. Neurosci. 25, 59-68.
184. Wei, X.-Y., Zhao, Y., Wong-Riley, M. T. T., Ju, G., and Liu, Y.-Y. (2012). Synaptic relationship between somatostatin- and neurokinin-1 receptor-immunoreactive neurons in the pre-Bötzinger complex of rats. J. Neurochem. 122, 923-933.
185. Wilson, N. R., Runyan, C. A., Wang, E L, and Sur, M. (2012). Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488, 343-348.
186. Wilson, R. S., Arnold, S. E., Schneider, J. A., Boyle, P. A., Buchman, A. S., and Bennett, D. A. (2009). Olfactory impairment in presymptomatic Alzheimer's disease. Ann. N. Y. Acad. Sci. 1170, 730-735.
187. Xu, X., Roby, K. D., and Callaway, E. M. (2006). Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J. Comp. Neurol. 499, 144-160.
188. Xu, X., Roby, K. D., and Callaway, E. M. (2010). Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J. Comp. Neurol. 518, 389-404.
189. Xue, S., Jia, L., and Jia, J. (2009). Association between somatostatin gene polymorphisms and sporadic Alzheimer's disease in Chinese population. Neurosci. Lett. 465, 181-183.
190. Yang, A. M., Ge, W W., Lu, S. S., Yang, S. B., Su, S. F., Mi, Z. Y., et al. (2011a). Central administration of neuronostatin induces antinocicep-tion in mice. Peptides 32, 1893-1901.
191. Yang, A. M., Ji, Y. K., Su, S. F., Yang, S. B., Lu, S. S., Mi, Z. Y., et al. (2011b). Intracerebroven-tricular administration of neuronostatin induces depression-like effect in forced swim test of mice. Peptides 32, 1948-1952.
192. Yang, S. B., Yang, A. M., Su, S. F., Wang, H. H., Wang, N. B., and Chen, Q. (2012). Neuronostatin induces hyperalgesia in formalin test in mice. Neurosci. Lett. 506, 126-130.
193. 2 antagonist PRL2903. Pharmacol. Biochem. Behav. 101, 88-92.
194. Yosten, G. L., Pate, A. T., and Samson, W K. (2011). Neuronostatin acts in brain to biphasically increase mean arterial pressure through sympatho-activation followed by vasopressin secretion: the role of melanocortin receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1194-R1199.
195. Young, A., and Sun, Q.-Q. (2009). GABAergic inhibitory interneurons in the posterior piriform cortex of the GAD67-GFP mouse. Cereb. Cortex 19, 3011-3029.
196. Zafar, R., King, M. A., and Carney, P. R. (2012). Adeno associated viral vector-mediated expression of somatostatin in rat hippocampus suppresses seizure development. Neurosci. Lett. 509, 87-91.
197. Zeyda, T., Diehl, N., Paylor, R., Bren-nan, M. B., and Hochgeschwen-der, U. (2001). Impairment in motor learning of somatostatin null mutant mice. Brain Res. 906, 107-114.
198. Zhang, Z. J., Lappi, D. A., Wrenn, C. C., Milner, T. A., and Wiley, R. G. (1998). Selective lesion of the cholinergic basal forebrain causes a loss of cortical neuropeptide Y and somatostatin neurons. Brain Res. 800, 198-206.