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The Journal of Neuroscience, January 23, 2008, 28(4):816-827; doi:10.1523/JNEUROSCI.4666-07.2008

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

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

¹Department of Developmental Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan, ²The Graduate University for Advanced Studies, Hayama, Kanagawa 240-0193, Japan, ³Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan, ⁴Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Maebashi 371-8511, Japan, and ⁵Neuronal Circuit Mechanisms Research Group, RIKEN Brain Science Institute, Wako 351-0198, Japan

Correspondence should be addressed to Dr. Katsusyuki Kaneda, Department of Developmental Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan. Email: kaneda{at}nips.ac.jp

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.

Key words: superior colliculus; GABA_B receptors; bursts; GAD67-GFP knock-in mouse; saccadic eye movement; patch clamp

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Received Oct. 14, 2007; revised Dec. 4, 2007; accepted Dec. 4, 2007.

Correspondence should be addressed to Dr. Katsusyuki Kaneda, Department of Developmental Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan. Email: kaneda{at}nips.ac.jp

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