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The Journal of Neuroscience, August 19, 2009, 29(33):10387-10395; doi:10.1523/JNEUROSCI.1978-09.2009

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Behavioral/Systems/Cognitive
Serotonergic Modulation of Locomotion in Zebrafish—Endogenous Release and Synaptic Mechanisms

Jens Peter Gabriel,^1 * Riyadh Mahmood,^1 * Alexandros Kyriakatos,¹ Iris Söll,^2,3 Giselbert Hauptmann,^2,3 Ronald L. Calabrese,⁴ and Abdeljabbar El Manira¹

¹Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden, ²School of Life Sciences, Södertörns Högskola, SE-141 89 Huddinge, Sweden, ³Department of Biosciences and Nutrition, Novum, Karolinska Institutet, SE-141 57 Huddinge, Sweden, and ⁴Department of Biology, Emory University, Atlanta, Georgia 30322

Corresponding author: Abdel El Manira, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden. Email: Abdel.ElManira{at}ki.se

Serotonin (5-HT) plays an important role in shaping the activity of the spinal networks underlying locomotion in many vertebrate preparations. At larval stages in zebrafish, 5-HT does not change the frequency of spontaneous swimming; and it only decreases the quiescent period between consecutive swimming episodes. However, it is not known whether 5-HT exerts similar actions on the locomotor network at later developmental stages. For this, the effect of 5-HT on the fictive locomotor pattern of juvenile and adult zebrafish was analyzed. Bath-application of 5-HT (1–20 µM) reduced the frequency of the NMDA-induced locomotor rhythm. Blocking removal from the synaptic cleft with the reuptake inhibitor citalopram had similar effects, suggesting that endogenous serotonin is modulating the locomotor pattern. One target for this modulation was the mid-cycle inhibition during locomotion because the IPSPs recorded in spinal neurons during the hyperpolarized phase were increased both in amplitude and occurrence by 5-HT. Similar results were obtained for IPSCs recorded in spinal neurons clamped at the reversal potential of excitatory currents (0 mV). 5-HT also slows down the rising phase of the excitatory drive recorded in spinal cord neurons when glycinergic inhibition is blocked. These results suggest that the decrease in the locomotor burst frequency induced by 5-HT is mediated by a potentiation of mid-cycle inhibition combined with a delayed onset of the subsequent depolarization.

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Received April 27, 2009; revised July 2, 2009; accepted July 8, 2009.

Corresponding author: Abdel El Manira, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden. Email: Abdel.ElManira{at}ki.se

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