Interaction between the serotoninergic and GABAergic systems in frog retina as revealed by electroretinogram

• Autorzy: Popova E. , Kupenova P.
• Języki publikacji: EN

Abstrakty

EN

Functional interactions between serotoninergic and GABAergic systems in the vertebrate retina are largely unknown. In this study, the effects of isolated or combined stimulation of the serotonin receptors (with 100 µM serotonin) and ionotropic GABAA and GABAC receptors (with 5 mM TACA) on the electroretinographic (ERG) ON (b‑wave) and OFF (d‑wave) responses were investigated in frog eyecup preparations. It was found that serotonin alone produced a significant enhancement of the b‑ and d‑wave amplitude, while TACA alone caused its marked diminution. The relative amplitude diminution, caused by the TACA treatment, was significantly smaller when TACA was applied on the background of the fully developed serotonin effect. This result suggests that the retinal serotoninergic system could diminish the effects of ionotropic GABA receptor activation on the ERG wave generator mechanisms. In order to separately evaluate the effects of the GABAC receptor activation, in a subset of experiments the effects of TACA or TACA + serotonin were tested during GABAA receptor blockade with 100 µM bicuculline. Bicuculline alone caused a marked increase of the b‑ and d‑wave amplitude. The stimulation of GABAC receptors (with TACA) during bicuculline action produced a strong diminution of the b‑ and d‑wave amplitudes. Similar relative decrease of the b‑wave amplitude was produced when TACA was applied in combination with serotonin, while the relative decrease of the d‑wave amplitude was less pronounced during treatment with serotonin + TACA than TACA alone. Our results demonstrate that there is an ON/OFF asymmetry in the receptors involved in the presumed interactions between serotoninergic and GABAergic systems. Serotonin may decrease the effects of GABAA receptor activation in the ON pathway, while it may decrease the effects of both GABAA and GABAC receptor activation in the OFF pathway.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2017
• Tom: 77
• Numer: 4
• Opis fizyczny: p.351-361,fig.,ref.

Twórcy

autor

Popova E.

• Department of physiology, Medical University of Sofia, 1431 Sofia, Bulgaria

autor

Kupenova P.

• Department of physiology, Medical University of Sofia, 1431 Sofia, Bulgaria

Bibliografia

• Berumen LC, Rodríguez A, Miledi R, García‑Alcocer G (2012) Serotonin receptors in hippocampus. Scientific World Journal 2012: 823493.
• Bijak  M, Misgeld U (1997) Effects of serotonin through serotonin1A and serotonin4 receptors on inhibition in the guinea‑pig dentate gyrus in vitro. Neurosci 78: 1017–1026.
• Bragadottir R, Kato M, Jarkman S (1997) Serotonin elevates the c‑wave of the electroretinogram of the rabbit eye by increasing the transepithelial potential. Vision Res 37: 2495–2503.
• Ciranna  L (2006) Serotonin as a  modulator of glutamate‑ and GABA‑mediated neurotransmission: implications in physiological functions and in pathology. Curr Neuropharmacol 4: 101–14.
• Dong CJ, Werblin FS (1998) Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. J Neurophysiol 79: 2171–2180.
• Eggers ED, Lukasiewicz PD (2006) GABAA, GABAC and glycine receptor‑mediated inhibition differentially affects lightevoked signalling from mouse retinal rod bipolar cells. J Physiol 572: 215–225.
• Eggers ED, Lukasiewicz PD (2011) Multiple pathways of inhibition shape bipolar cell responses in the retina. Vis Neurosci 28: 95–108.
• Ehinger B (1983) Connexions between retinal neurons with identified neurotransmitters. Vision Res 23: 1281–1289.
• Euler T, Wassle H (1998) Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. J Neurophysiol 79(3): 1384–1395.
• Feigenspan A, Bormann J (1994) Modulation of GABAC receptors in rat retinal bipolar cells by protein kinase C. J Physiol. 481(Pt 2): 325–30.
• Feng J, Cai X, Zhao J, Yan Z (2001) Serotonin receptors modulate GABA(A) receptor channels through activation of anchored protein kinase C in prefrontal cortical neurons. J Neurosci 21: 6502–6511.
• Frishman LJ (2006) Origins of the electroretinogram. In: Heckenlively JR, Arden GB, editors. Principles and Practice of Clinical Electrophysiology of Vision. 2nd ed. London: MIT Press; p.139–183.
• Frishman LJ (2013) Electrogenesis of the electroretinogram. In: Ryan SJ, Hinton DR, Sadda SR, Schachat AP, Wilkinson CP, Wiedemann P, editors. Retina. 5th ed. Elsevier Health Sciences; volume 1, p. 177–201.
• Gábriel R (2000) Calretinin is present in serotonin‑ and gamma‑aminobu‑ tyric acid‑positive amacrine cell populations in the retina of Xenopus laevis. Neurosci Lett 285: 9–12.
• Gastinger MJ, Bordt AS, Bernal MP, Marshak DW (2005) Serotonergic retinopetal axons in the monkey retina. Curr Eye Res 30: 1089–95.
• Gastinger MJ, Tian N, Horvath T, Marshak DW (2006) Retinopetal axons in mammals: emphasis on histamine and serotonin. Curr Eye Res 31: 655–67.
• Ghai K, Zelinka C, Fischer AJ (2009) Serotonin released from amacrine neurons is scavenged and degraded in bipolar neurons in the retina. J Neurochem 111: 1–14.
• Han  L, Zhong YM, Yang XL (2007) 5‑HT2A receptors are differentially expressed in bullfrog and rat retinas: a comparative study. Brain Res Bull 73: 273–277.
• Haverkamp S, Inta D, Monyer H, Wässle H (2009) Expression analysis of green fluorescent protein in retinal neurons of four transgenic mouse lines. Neurosci 160: 126–139.
• Hidaka S (2009) Serotonergic synapses modulate generation of spikes from retinal ganglion cells of teleosts. J Integr Neurosci 8: 299–322.
• Hurd LB 2nd, Eldred WD (1993) Synaptic microcircuitry of bipolar and amacrine cells with serotonin‑like immunoreactivity in the retina of the turtle, Pseudemys scripta elegans. Vis Neurosci 10: 455–471.
• Johnston GA (1996) GABAc receptors: relatively simple transmitter‑gated ion channels? Trends Pharmacol Sci 17: 319–323.
• Kupenova P, Popova E, Vitanova  L (2008) GABAa and GABAc receptor mediated influences on the intensity‑response functions of the b‑ and d‑wave in the frog ERG. Vision Res 48: 882–892.
• Kusama T, Spivak CE, Whiting P, Dawson VL, Schaeffer JC, Uhl GR (1993) Pharmacology of GABA rho 1 and GABA alpha/beta receptors expressed in Xenopus oocytes and COS cells. Br J Pharmacol 109: 200–206.
• Li H, Lang B, Kang JF, Li YQ (2000) Serotonin potentiates the response of neurons of the superficial laminae of the rat spinal dorsal horn to gamma‑aminobutyric acid. Brain Res Bull 52: 559–565.
• Lima L, Urbina M (1998) Serotonergic projections to the retina of rat and goldfish. Neurochem Int. 32: 133–141.
• Mangel SC, Brunken WJ (1992) The effects of serotonin drugs on horizontal and ganglion cells in the rabbit retina. Vis Neurosci 8: 213–218.
• Marc RE, Liu WL, Scholz K, Muller JF (1988) Serotonergic and serotonin‑ac‑ cumulating neurons in the goldfish retina. J Neurosci 8: 3427–3450.
• Nakatsuka K, Hamasaki DI (1985) Destruction of the indoleamine‑accumu‑ lating amacrine cells alters the ERG of rabbits. Invest Ophthalmol Vis Sci 26: 1109–16.
• Nichols DE, Nichols CD (2008) Serotonin Receptors. Chem. Rev. 108: 1614–1641.
• Ochoa‑de la Paz LD, Estrada‑Mondragón A, Limón A, Miledi R, Martínez‑Torres A (2012) Dopamine and serotonin modulate human GABAρ1 receptors expressed in Xenopus laevis oocytes. ACS Chem Neurosci 3: 96–104.
• Olsen RW, Sieghart W (2009) GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacol 56: 141–8.
• Osborne NN, Nesselhut T, Nicholas DA, Patel S, Cuello AC (1982) Sero‑ tonin‑containing neurones in vertebrate retinas. J  Neurochem 39: 1519–28.
• Padgett CL, Slesinger PA (2010) GABAB receptor coupling to G‑proteins and ion channels. Adv Pharmacol. 58: 123–47.
• Pennesi ME, Stoddard JW, Michaels KV, Blum ED, Maricle A, Francis PJ (2012) Expression and Localization of Serotonin Receptors in the Mouse Retina. Invest Ophthalmol Vis Sci 53: 6547.
• Pootanakit K, Brunken WJ (2001) Identification of 5‑HT(3A) and 5‑HT(3B) receptor subunits in mammalian retinae: potential pre‑synaptic modulators of photoreceptors. Brain Res 896: 77–85.
• Pootanakit K, Prior KJ, Hunter DD, Brunken WJ (1999) 5‑HT2a receptors in the rabbit retina: potential presynaptic modulators. Vis Neurosci 16: 221–230.
• Popova Е (2000) Glycinergic and GABAergic control of intensity‑response function of frog ERG waves under different conditions of light stimulation. Acta Physiol Scand 170: 225–242.
• Popova E (2003) Effects of benzodiazepines on frog ERG. Comp Biochem Physiol C Toxicol Pharmacol 134: 457–64.
• Popova E (2014) Ionotropic GABA receptors and distal retinal ON and OFF responses. Scientifica (Cairo) 2014: 149187.
• Popova E, Kostov M, Kupenova P (2016) Effects of dopamine D1 receptor blockade on the ERG b‑ and d‑waves during blockade of ionotropic GABA receptors. Eye Vis (Lond) 3: 32.
• Popova E, Kupenova P (2011) Effects of dopamine D1 receptor blockade on the intensity‑response function of ERG b‑ and d‑waves under different conditions of light adaptation. Vision Res 51: 1627–1636.
• Porciatti  V, Alesci R, Bagnoli P, Signorini G, Raffaelli A (1989) Serotonin depletion modifies the pigeon electroretinogram. Doc Ophthalmol 72: 93–100.
• Schütte  M (1994) Serotonergic and serotonin‑synthesizing cells of the Xenopus retina. Int J Neurosci 78: 67–73.
• Shen H, Semba K (1994) A direct retinal projection to the dorsal raphe nucleus in the rat. Brain Res. 635: 159–168.
• Skrandies  W, Wässle H (1988) Dopamine and serotonin in cat retina: electroretinography and histology. Exp Brain Res 71: 231–40.
• Smith BJ, Côté PD, Tremblay F (2015) Dopamine modulation of rod pathway signaling by suppression of GABAC feedback to rod‑driven depolarizing bipolar cells. Eur J Neurosci 42: 2258–2270.
• Vígh J, Bánvölgyi T, Wilhelm M (2000) Amacrine cells of the anuran retina: morphology, chemical neuroanatomy, and physiology”, Microsc Res Tech 50: 373–383.
• Villar MJ, Vitale ML, Parisi MN (1987) Dorsal raphe serotonergic projection to the retina. A  combined peroxidase tracing‑neurochemical/ high‑performance liquid chromatography study in the rat. Neurosci 22: 681–686.
• Vitanova  L, Kupenova P, Haverkamp S, Popova E, Mitova  L, Wassle H (2001) Immunocytochemical and electrophysiological characterization of GABA receptors in the frog and turtle retina. Vision Res 41: 691–704.
• Wang DS, Xu TL, Li JS (1999) 5‑HT potentiates GABA‑ and glycine‑activated chloride currents on the same neurons in rat spinal cord. J Hirnforsch 39: 531–537.
• Wang H, Hu  L, Liu C, Su Z, Wang  L, Pan G, Guo Y, He J (2016) 5‑HT2 receptors mediate functional modulation of GABAa receptors and inhibitory synaptic transmissions in human iPS‑derived neurons. Sci Rep 6: 20033.
• Wilhelm  M, Zhu B, Gábriel R, Straznicky C (1993) Immunocytochemical identification of serotonin‑synthesizing neurons in the vertebrate retina: a comparative study. Exp Eye Res 56: 231–240.
• Xu TL, Pang ZP, Li JS, Akaike N (1998) 5‑HT potentiation of the GABA(A) response in the rat sacral dorsal commissural neurones. Br J Pharmacol 124: 779–787.
• Zhu B, Gabriel R, Straznicky C (1992) Serotonin synthesis and accumulation by neurons of the anuran retina. Vis Neurosci 9: 377–388.