Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-26T07:35:08.342Z Has data issue: false hasContentIssue false
  • English
  • Français

Cysteamine-induced depletion of somatostatinergic systems alters potentials evoked from the rat visual cortex

Published online by Cambridge University Press:  02 June 2009

Gigliola Fontanesi ,
Rosita Siciliano ,
Vittorio Porciatti  and
Paola Bagnoli
Gigliola Fontanesi
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56123 Pisa, Italy
Rosita Siciliano
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56123 Pisa, Italy
Vittorio Porciatti
Affiliation:
Institute of Neurophysiology, Italian Research Council, 56123 Pisa, Italy
Paola Bagnoli
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56123 Pisa, Italy
Get access Rights & Permissions [Opens in a new window]

Abstract

This study was performed in order to establish whether selective depletion of somatostatin (SS) in the rat primary visual cortex obtained by cysteamine (CSH) administration results in changes of visual evoked potentials (VEPs). VEPs in response to a contrast reversal (0.5 Hz) of an optimal sinusoidal grating (0.1 cycle/deg, contrast 90%, mean luminance 15 cd/m2) were recorded from different layers of the binocular portion of the primary visual cortex of anesthetized rats with saline injection as well as before and after CSH treatment (90 mg/kg, s.c). VEPs of CSH treated rats, as compared to those obtained either in saline-injected animals or before drug administration, are reduced in amplitude at intermediate cortical layers whereas they are increased at deeper layers. VEP changes depend on CSH treatment and not on the extended anesthesia since no alterations in the VEP profile can be observed in saline-injected animals maintained in the same experimental condition. Forty-eight hours following CSH treatment, the VEP profile is comparable to that of saline-injected animals. Immunocytochemical analysis of the visual cortex of rats recorded 7 h after CSH treatment shows a 20–30% reduction in the number of SS-containing cortical cells. The highest reduction can be observed in cortical layer 5 although a significant decrease is also found in layers 2–3. In contrast, the pattern of SS immunoreactivity of the visual cortex of rats recorded 48 h after CSH administration is similar to that obtained in control conditions. These results indicate that a selective toxin for somatostatinergic systems induces a transient decrease of SS-containing cell number in selected cortical layers. Accordingly, CSH can serve as a useful pharmacological tool for the study of somatostatinergic function in the rat visual cortex since changes in VEPs can be related to a reduction of somatostatinergic neurons associated to CSH treatment. In particular, the present results suggest that one of the possible actions of somatostatinergic neurons in the rat visual cortex is to modulate the excitatory-inhibitory balance.

Keywords

Somatostatin immunoreactivityNeurotoxicityPrimary visual cortexContrast stimulusVisual evoked potentialsRat
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 327 - 334
Copyright
Copyright © Cambridge University Press 1996

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.)

References

REFERENCES

Bagnoli, P., Fontanesi, C., Alesci, R. & Erichsen, J.T. (1992). Distribution of neuropeptide Y, substance P., and choline acetyltransferase in the developing visual system of the pigeon and effects of unilateral retina removal. Journal of Comparative Neurology 318, 392–414.Google ScholarPubMed
Beal, M.F., Mazurek, M.F., Tran, V.T., Chatta, G., Bird, E.D. & Martin, J.B. (1985). Reduced numbers of somatostatin receptors in the cerebral cortex in Alzheimer's disease. Science 229, 289–291.CrossRefGoogle ScholarPubMed
Buchan, A.M.J., Sikora, L.K.J., Levy, J.G., McIntosh, C.H.S., Dyck, I. & Brown, J.C. (1985). An immunocytochemical investigation with monoclonal antibodies to somatostatin. Histochemistry 83, 175–180.CrossRefGoogle ScholarPubMed
Davies, P., Katzman, R. & Terry, R.D. (1980). Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer's disease and Alzheimer senile dementia. Nature 288, 279–280.CrossRefGoogle Scholar
Delfs, J. & Dichter, M. (1983). Effects of somatostatin on mammalian cortical neurons in culture: Physiological actions and unusual dose response characteristics. Journal of Neuroscience 3, 1176–1188.CrossRefGoogle ScholarPubMed
Di Liberto, E.J., Di Stefano, V. & Smith, J.C. (1973). Mechanism and kinetics of the inhibition of dopamine-β-hydroxylase by 2-mercaptoethylguanidine. Biochemical Pharmacology 22, 2961–2972.CrossRefGoogle Scholar
Domenici, L., Berardi, N., Carmignoto, G., Vantini, G. & Maffei, L. (1991). Nerve growth factor prevents the amblyopic effects of monocular deprivation. Proceedings of the National Academy of Sciences of the U.S.A. 88, 8811–8815.CrossRefGoogle ScholarPubMed
Epelbaum, J. (1986). Somatostatin in the central nervous system: Physiology and pathological modifications. Progress in Neurobiology 27, 63–100.CrossRefGoogle ScholarPubMed
Erichsen, J.T., Ciocchetti, A., Fontanesi, G. & Bagnoli, P. (1994). Neuroactive substances in the developing dorsomedial telencephalon of the pigeon (Columba livia): Differential distribution and time course of maturation. Journal of Comparative Neurology 345, 537–561.CrossRefGoogle ScholarPubMed
Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. (1994). Functional postnatal development of the rat primary visual cortex and role of visual experience: Dark rearing and monocular deprivation. Vision Research 34, 709–720.CrossRefGoogle ScholarPubMed
Fontanesi, G., Traina, G. & Bagnoli, P. (1993). Somatostatin-like immunoreactivity in the pigeon visual system: Developmental expression and effects of retina removal. Visual Neuroscience 10, 271–285.CrossRefGoogle ScholarPubMed
Hancock, M.B. (1984). Visualization of peptide-immunoreactive processes of serotonin immunoreactive cells using two color immunoperoxidase staining. Journal of Histochemistry and Cytochemistry 37, 311–314.CrossRefGoogle Scholar
Haroutunian, V., Mantin, R., Campbell, G.A., Tsuboyama, G.K. & Davis, K.L. (1987). Cysteamine-induced depletion of central somatostatin-like immunoreactivity: Effects on behavior, learning, memory and brain neurochemistry. Brain Research 403, 234–242.CrossRefGoogle ScholarPubMed
Hughes, H.C. (1977). Anatomical and neurobehavioural investigations concerning the thalamo-cortical organization of the rat's visual system. Journal of Comparative Neurology 175, 311–336.CrossRefGoogle ScholarPubMed
Inque, M. & Yoshii, M. (1992). Modulation of ion channels by somatostatin and acetylcholine. Progress in Neurobiology 38, 203–230.Google Scholar
Laemle, L.K. & Feldman, S.C. (1985). Somatostatin (SRlF)-like immunoreactivity in subcortical and cortical visual centers of the rat. Journal of Comparative Neurology 233, 452–462.CrossRefGoogle Scholar
Lin, C.S., Lu, S.M. & Schmechel, D.E. (1986). Glutamic acid decarboxylase and somatostatin immunoreactivities in rat visual cortex. Journal of Comparative Neurology 244, 369–383.CrossRefGoogle ScholarPubMed
McDonald, J.K., Parnavelas, J.G., Karamanlidis, A.N., Brecha, N. & Koenig, J.I. (1982). The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. I. Somatostatin, Journal of Neurocytology 11, 809–824.CrossRefGoogle ScholarPubMed
Mitzdorf, U. (1985). Current source-density method and application in the cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiological Reviews 65, 37–100.CrossRefGoogle ScholarPubMed
Mitzdorf, U. (1986). The physiological causes of VEPs. Current source-density analysis of electrically and visually evoked potentials. In Evoked Potentials, ed. Cracco, R.Q. & Wollner, I.B., pp. 141–156. New York: Alan R. Liss Inc.Google Scholar
Mizukawa, K., McGeer, P.L., Vincent, S.R. & McGeer, E.G. (1987). The distribution of somatostatin-immunoreactive neurons and fibers in the rat cerebral cortex: Light and electron microscopic studies. Brain Research 426, 28–36.CrossRefGoogle ScholarPubMed
Morrison, J.H., Benoit, R., Magistretti, P.J. & Bloom, F.E. (1983). Immunohistochemical distribution of pro-somatostatin-related peptides in cerebral cortex. Brain Research 262, 344–351.Google ScholarPubMed
Naus, C.C.G., Miller, F.D., Morrison, J.H. & Bloom, F.E. (1988). Immunohistochemical and in situ hybridization analysis of the development of the rat somatostatin-containing neocortical neuronal systems. Journal of Comparative Neurology 269, 448–463.CrossRefGoogle Scholar
Nicholson, C. & Freeman, J.A. (1975). Theory of current source-density analysis and determination of conductivity tensor for Anuran cerebellum. Journal of Neurophysiology 38, 356–368.CrossRefGoogle ScholarPubMed
Olney, J.W., Ho, O.L. & Rhee, V. (1971). Cytotoxic effects of acidiv and sulphur containing amino acids on the infant mouse central nervous system. Experimental Brain Research 14, 61–76.CrossRefGoogle Scholar
Palkovits, M., Brownstein, M.J., Eiden, L.E., Beinfeld, L.C., Russel, J., Arimura, A. & Szabo, S. (1982). Selective depletion of somatostatin in rat brain by cysteamine. Brain Research 240, 178–180.CrossRefGoogle ScholarPubMed
Parnavelas, J.G., Burne, R.A. & Lin, C.S. (1981). Receptive field properties of neurons in the visual cortex of the rat. Neuroscience Letters 27, 291–296.Google ScholarPubMed
Patel, Y.C. & Pierzchala, I. (1985). Cysteamine induces a loss of tissue somatostatin-28 when measured as somatostatin-28(15–28) like immunoreactivity but not when assessed as somatostatin 28(1–14) like immunoreactivity: Evidence for the importance of the disulfide bond for cysteamine action. Endocrinology 116, 1699–1702.CrossRefGoogle Scholar
Paxinos, G. & Watson, C. (1982). The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.Google Scholar
Pizzorusso, T., Fagiolini, M., Porciatti, V. & Maffei, L. (1995). Temporal aspects of contrast VEPs in the rat: effect of dark rearing. Vision Research, in press.Google Scholar
Pradayrol, L., Jorvall, H., Mutt, V. & Ribet, A. (1980). N-terminally extended somatostatin: The primary structure of somatostatin-28. FEBS Letters 109, 55–58.CrossRefGoogle ScholarPubMed
Raynor, K., Coy, D.C. & Reisine, T. (1992). Analogues of somatostatin bind selectively to brain somatostatin receptor subtypes. Journal of Neurochemistry 59, 1241–1250.CrossRefGoogle ScholarPubMed
Roberts, G.W., & Crow, J. & Polak, J.M. (1985). Location of neuronal tangles in somatostatin neurones in Alzheimer's disease. Nature 324, 92–94.Google Scholar
Rossor, M.N., Emson, P.C., Mountjoy, C.Q., Roth, M. & Iversen, L.L. (1980). Reduced amounts of immunoreactive somatostatin in the temporal cortex in senile dementia of Alzheimer's type. Neuroscience Letters 20, 373–377.CrossRefGoogle Scholar
Sagar, S.M., Landry, D., Millard, W.S., Badger, T.M., Arnold, M.A. & Martin, J.B. (1982). Depletion of somatostatin-like immunoreactivity in the rat central nervous system by cysteamine. Journal of Neuroscience 2, 225–231.CrossRefGoogle ScholarPubMed
Schmechel, D.E., Vickrey, B.G., Fitzpatrick, D. & Elde, R.P. (1984). GABAergic neurons of mammalian cerebral cortex: Widespread subclass defined by somatostatin content. Neuroscience Letters 47, 227–232.CrossRefGoogle ScholarPubMed
Schroeder, C.E., Tenke, C.E., Givre, S.J., Arezzo, J.C. & Vaughan, H.G. Jr. (1990). Laminar analysis of bicuculline-induced epileptiform activity in area 17 of the awake macaque. Brain Research 515, 326–330.CrossRefGoogle ScholarPubMed
Somogy, P., Hodgson, A., Smith, A.D., Nunzi, M.G., Gorio, A. & Wu, J. (1984). Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecytokinin-immunoreactive material. Journal of Neuroscience 4, 2590–2603.CrossRefGoogle Scholar
Szabo, S. & Reichlin, S. (1981). Somatostatin in rat tissues in depleted by cysteamine administration. Endocrinology 109, 2255–2257.CrossRefGoogle ScholarPubMed
Theveniau, M.A., Yasuda, K., Bell, G.I. & Reisine, T. (1994). Immunological detection of isoforms of the somatostatin receptor subtype, SSTR2. Journal of Neurochemistry 63, 447–455.CrossRefGoogle ScholarPubMed
Vincent, S.R., McIntosh, C.H.S., Buchan, A.M.J. & Brown, J.C. (1985). Central somatostatin system revealed with monoclonal antibodies. Journal of Comparative Neurology 238, 169–186.CrossRefGoogle ScholarPubMed
White, C.A., Chalupa, L.M., Johnson, D. & Brecha, N. (1990). Somatostatin-immunoreactive cells in the adult cat retina. Journal of Comparative Neurology 293, 134–150.CrossRefGoogle ScholarPubMed
Zalutsky, R.A. & Miller, R.F. (1990). The physiology of somatostatin in the rabbit retina. Journal of Neuroscience 10, 383–393.CrossRefGoogle ScholarPubMed