Regulation of Burst Activity through Presynaptic and Postsynaptic GABA_B Receptors in Mouse Superior Colliculus

Abstract

Katsuyuki Kaneda,^1,2 Penphimon Phongphanphanee,^1,2 Tomoko Katoh,¹ Kaoru Isa,^1,3 Yuchio Yanagawa,⁴ Kunihiko Obata,⁵ and Tadashi Isa.^1,2,3 Regulation of Burst Activity through Presynaptic and Postsynaptic GABA_B Receptors in Mouse Superior Colliculus. The Journal of Neuroscience, 23 Jan 2008; 28 (4) 816-827

1. Department of Developmental Physiology, National Institute for Physiological Sciences
2. The Graduate University for Advanced Studies
3. Core Research for Evolutional Science and Technology, Japan Science and Technology Agency
4. Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine
5. Neuronal Circuit Mechanisms Research Group, RIKEN Brain Science Institute

In slice preparations, electrical stimulation of the superficial gray layer (SGS) of the superior colliculus (SC) induces EPSC bursts in neurons in the intermediate gray layer (SGI) when GABA_A receptor (GABA_AR)-mediated inhibition is reduced. This preparation has been used as a model system to study signal processing involved in execution of short-latency orienting responses to visual stimuli such as saccadic eye movements. In the present study, we investigated the role of GABA_B receptors (GABA_BRs) in modulating signal transmission in the above pathway with whole-cell patch-clamp recordings in SC slices obtained from GAD67-GFP knock-in mice. Perfusion of the slice with the GABA_BR antagonist CGP52432 (CGP) greatly prolonged the duration of the EPSC bursts. Local application of CGP to the SGS but not to the SGI produced similar effects. Because SGS stimulation elicited bursts in GABAergic neurons in the SGS when GABA_ARs were blocked, these results suggest that GABA released after bursts activates GABA_BRs in the SGS, leading to reduced burst duration. We found both postsynaptic and presynaptic actions of GABA_BRs in the SGS; activation of postsynaptic GABA_BRs induced outward currents in narrow-field vertical cells, whereas it caused shunting inhibition in distal dendrites in wide-field vertical cells. On the other hand, activation of presynaptic GABA_BRs suppressed excitatory synaptic transmissions to non-GABAergic neurons in the SGS. These results indicate that synaptically released GABA can activate both presynaptic and postsynaptic GABA_BRs in the SGS and limit the duration of burst responses in the SC local circuit.
 

1. Department of Developmental Physiology, National Institute for Physiological Sciences
2. The Graduate University for Advanced Studies
3. Core Research for Evolutional Science and Technology, Japan Science and Technology Agency
4. Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine
5. Neuronal Circuit Mechanisms Research Group, RIKEN Brain Science Institute

Figure

Schematic of local circuit underlying GABA_BR-mediated regulation of bursts in the SC. Postsynaptic GABA_BRs expressed both in NFV and WFV cells and presynaptic GABA_BRs located on glutamatergic synaptic terminals in the SGS are activated by synaptically released GABA during bursts of SGS GABAergic neurons. Hyperpolarization in NFV cells, shunting inhibition in WFV cells, and reduction of glutamate release may contribute to the limitation of burst duration. When GABA_BRs are blocked, burst duration in the SGS may be prolonged in an NMDAR-dependent manner, and then, the prolonged burst may spread to the SGI. Thus the burst duration of the SGI may also be prolonged. Note that the localization of the receptors and synaptic connections essential to explain the present results are depicted and other components such as AMPA ⁄ Kainate receptors and GABA_ARs are not drawn for clarity.