Diversity of neuron-specific K+-Cl- cotransporter expression and inhibitory postsynaptic potential depression in rat motoneurons.
Motoneurons receive a robust recurrent synaptic inhibition by gamma-aminobutyric acid and glycine, which activate Cl(-) channels. Thus, Cl(-) homeostasis determines the efficacy of synaptic inhibition in the motoneurons. In situ hybridization reveals that the neuronal K(+)-Cl(-) cotransporter isoform 2 (KCC2), a major mechanism in maintaining a low Cl(-) concentration in neurons, is abundantly expressed in the facial, hypoglossal (XII), and spinal motoneurons innervating striated muscle, whereas the dorsal vagal motoneurons (DMVs) controlling smooth muscle exhibited little expression of KCC2. This raises a general interest in the correlation between KCC2 expression and inhibitory postsynaptic potential (IPSP) performance in the native circuits. Intracellular and whole-cell patch recordings revealed that an activity-dependent depression of IPSPs and positive shift of IPSP reversal potentials were more prominent in the DMV than in the XII. Cl(-) influx through Cl(-) channels was extruded more potently in the XII than in the DMV, suggesting that differences in Cl(-) extrusion account for these dynamic differences of IPSP. Cl(-) extrusion was inhibited by either furosemide or an increase in extracellular potassium concentrations. Thus, the rigid maintenance of IPSP and rapid Cl(-) extrusion in the XII reflects an intense expression of KCC2. KCC2 expression may strongly influence the IPSP depression and functional properties of the motoneurons innervating striated muscles.
Ueno
Tsuyoshi
T
Department of Cellular and System Physiology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan.
Okabe
Akihito
A
Akaike
Norio
N
Fukuda
Atsuo
A
Nabekura
Junichi
J
D000818:Animals; D001692:Biological Transport; D002713:Chlorine / Q000494:pharmacology; D004232:Diuretics / Q000494:pharmacology; D004594:Electrophysiology; D005665:Furosemide / Q000494:pharmacology; D006706:Homeostasis; D017403:In Situ Hybridization; D008969:Molecular Sequence Data; D018482:Muscle, Skeletal / Q000294:innervation*; D009474:Neurons / Q000378:metabolism*; D011188:Potassium / Q000494:pharmacology; D020033:Protein Isoforms; D016372:RNA, Antisense / Q000378:metabolism; D012333:RNA, Messenger / Q000378:metabolism; D051381:Rats; D017208:Rats, Wistar; D027981:Symporters / Q000096:biosynthesis* / Q000502:physiology*; D013569:Synapses / Q000378:metabolism*; D013997:Time Factors; D005680:gamma-Aminobutyric Acid / Q000378:metabolism; D000096922:K Cl- Cotransporters
D002713:Chlorine; D004232:Diuretics; D005665:Furosemide; D011188:Potassium; D020033:Protein Isoforms; D016372:RNA, Antisense; D012333:RNA, Messenger; D027981:Symporters; D005680:gamma-Aminobutyric Acid; D000096922:K Cl- Cotransporters