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The Journal of Neuroscience, October 21, 2009, 29(42):13401-13409; doi:10.1523/JNEUROSCI.2628-09.2009

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Behavioral/Systems/Cognitive
Evidence against AMPA Receptor-Lacking Glutamatergic Synapses in the Superficial Dorsal Horn of the Rat Spinal Cord

Toshiharu Yasaka,¹ David I. Hughes,¹ Erika Polgár,¹ Gergely G. Nagy,¹ Masahiko Watanabe,² John S. Riddell,¹ and Andrew J. Todd¹

¹Neuroscience and Molecular Pharmacology, Faculty of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom, and ²Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan

Correspondence should be addressed to Prof. Andrew J. Todd, Spinal Cord Group, West Medical Building, University of Glasgow, University Avenue, Glasgow G12 8QQ, UK. Email: a.todd{at}bio.gla.ac.uk

Pure NMDA receptor (NMDAr)-mediated EPSCs, thought to correspond to "silent" glutamatergic synapses that lack AMPA receptors (AMPArs), have been observed in superficial spinal dorsal horn of neonatal but not adult rats. Recent anatomical studies suggest that AMPArs are present at virtually all glutamatergic synapses in this region in adults. We used antigen retrieval to examine colocalization of AMPArs and PSD-95 (a marker for glutamatergic synapses) in laminae I–II of neonatal and adult rats. We found a high degree of colocalization in all cases, which suggests that AMPArs are present in the great majority of glutamatergic synapses even in neonatal animals. We therefore reexamined evidence for silent synapses by performing blind whole-cell recordings from superficial dorsal horn neurons in slices from neonatal or adult rats, with focal stimulation to activate glutamatergic synapses. On some occasions in both neonatal (10 of 109, 9%) and adult (9 of 77, 12%) slices, NMDAr-mediated EPSCs were observed when the holding potential was raised to +50 mV at a stimulus strength that had failed to evoke AMPAr-mediated EPSCs. However, in all cases tested, AMPAr-mediated EPSCs were then observed when the cell was returned to –70 mV; this and other properties of the EPSCs suggest that they do not represent genuine silent synapses. When compared with previous findings, our results indicate that the appearance of silent synapses depends on experimental protocol. This suggests that pure NMDAr-mediated EPSCs seen in previous studies do not correspond to AMPAr-lacking synapses but result from another mechanism, for example, loss of labile AMPArs from recently formed synapses.

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Received June 5, 2009; revised Sept. 9, 2009; accepted Sept. 15, 2009.

Correspondence should be addressed to Prof. Andrew J. Todd, Spinal Cord Group, West Medical Building, University of Glasgow, University Avenue, Glasgow G12 8QQ, UK. Email: a.todd{at}bio.gla.ac.uk

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