The Journal of Neuroscience, October 22, 2008, 28(43):11071-11078; doi:10.1523/JNEUROSCI.3263-08.2008
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Behavioral/Systems/Cognitive
Nigral Inhibition of GABAergic Neurons in Mouse Superior Colliculus
Katsuyuki Kaneda,1,2
Kaoru Isa,1,3
Yuchio Yanagawa,4 and
Tadashi Isa1,2,3
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, and 4Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Maebashi, 371-8511, Japan
Correspondence should be addressed to Katsuyuki Kaneda, Department of Developmental Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan. Email: kaneda{at}nips.ac.jp
The current dominant concept for the control of saccadic eye movements by the basal ganglia is that release from tonic GABAergic inhibition by the substantia nigra pars reticulata (SNr) triggers burst firings of intermediate gray layer (SGI) neurons in the superior colliculus (SC) to allow saccade initiation. This hypothesis is based on the assumption that SNr cells inhibit excitatory projection neurons in the SGI. Here we show that nigrotectal fibers are connected to local GABAergic neurons in the SGI with a similar frequency to non-GABAergic neurons. This was accomplished by applying neuroanatomical tracing and slice electrophysiological experiments in GAD67–green fluorescent protein (GFP) knock-in mice, in which GABAergic neurons specifically express GFP. We also found that GABAA, but not GABAB, receptors subserve nigrotectal transmission. The present results revealed a novel aspect on the role of the basal ganglia in the control of saccades, e.g., the SNr not only regulates burst initiation but also modulates the spatiotemporal properties of premotor neurons via connections to local GABAergic neurons in the SC.
Key words: superior colliculus; saccade; basal ganglia; substantia nigra pars reticulata; disinhibition; burst
Received July 12, 2008;
revised Aug. 20, 2008;
accepted Sept. 9, 2008.
Correspondence should be addressed to Katsuyuki 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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T. Isa and W. C. Hall
Exploring the Superior Colliculus In Vitro
J Neurophysiol,
November 1, 2009;
102(5):
2581 - 2593.
[Abstract]
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