Journal of Neurophysiology, Vol 71, Issue 1 280-293, Copyright © 1994 by APS

ARTICLES

Spatiotemporally differential inhibition of pyramidal cells in the cat motor cortex

Y. Kang, T. Kaneko, H. Ohishi, K. Endo and T. Araki
Department of Physiology, Faculty of Medicine, Kyoto University, Japan.

1. The spatiotemporal pattern of inhibition in the cat motor cortex was studied in in vitro slice preparations in the presence of 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and 2-amino-5-phosphonovaleric acid (APV). 2. After intracortical microstimulation (0.5-6 microA), fast and slow inhibitory postsynaptic potentials (IPSPs) were produced in layers II-VI pyramidal cells and selectively reduced with bicuculline methiodide and phaclofen, respectively. 3. Fast IPSPs were maximally produced by stimulation of the same layer where their cell bodies were located, and they decreased in amplitude as the more superficial layer was stimulated. In contrast, slow IPSPs were maximally produced by stimulation of layer II regardless of the location of the recorded pyramidal cell and decreased in amplitude as the deeper layer was stimulated. 4. The reduction of amplitude of fast IPSPs, in response to a vertical shift of the stimulation site toward more superficial layers, was always correlated with an increase in rise time and with a shift of the reversal potential to a more hyperpolarized level. 5. When the stimulation site was moved horizontally to the more lateral site, fast IPSPs increased in latency and decreased in amplitude gradually without appreciable changes in rise time. Fast IPSPs could be evoked from horizontally remote sites of up to 800-1,200 microns. 6. Inhibitory interneurons, which are responsible for evoking fast IPSPs, appear to be distributed through almost all layers to send horizontally spreading parallel axons making synaptic contacts at different electrotonic distances along apical dendrites of single pyramidal cells. 7. Horizontal spreads were much less in slow IPSPs (< 340-680 microns). The time-to-peak of slow IPSPs produced in layer V pyramidal cells (159.5 +/- 6.8 ms, mean +/- SD, n = 10) was significantly (P < 0.0001) longer than that in layers II and III pyramidal cells (128.5 +/- 7.5 ms, n = 7). Asymmetric reversal properties of slow IPSPs were seen, suggesting the spatial dispersion of synaptic inputs along apical dendrites of pyramidal cells. 8. In layer V pyramidal cells, the time-to-peak of slow IPSPs decreased with increasing membrane hyperpolarization, indicating that the later portion of slow IPSPs was more sensitive to the membrane-potential change than the early portion. This further indicates that the late portion of slow IPSPs is generated at synapses on the more proximal dendrite of pyramidal cells than the early portion, contrary to that expected from the Rall's model of passive dendrite under the condition of synchronous inputs.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				Z. J Daskalakis, B. K Christensen, P. B Fitzgerald, B. Moller, S. I Fountain, and R. Chen Increased cortical inhibition in persons with schizophrenia treated with clozapine J Psychopharmacol, March 1, 2008; 22(2): 203 - 209. [Abstract] [PDF]

				R.A.B. Badawy, J. M. Curatolo, M. Newton, S. F. Berkovic, and R. A.L. Macdonell Sleep deprivation increases cortical excitability in epilepsy: Syndrome-specific effects. Neurology, September 26, 2006; 67(6): 1018 - 1022. [Abstract] [Full Text] [PDF]

				S. K. Esser, S. L. Hill, and G. Tononi Modeling the Effects of Transcranial Magnetic Stimulation on Cortical Circuits J Neurophysiol, July 1, 2005; 94(1): 622 - 639. [Abstract] [Full Text] [PDF]

				S. Hill and G. Tononi Modeling Sleep and Wakefulness in the Thalamocortical System J Neurophysiol, March 1, 2005; 93(3): 1671 - 1698. [Abstract] [Full Text] [PDF]

				K. Rosenkranz and J. C Rothwell Differential effect of muscle vibration on intracortical inhibitory circuits in humans J. Physiol., September 1, 2003; 551(2): 649 - 660. [Abstract] [Full Text] [PDF]

				A. Sailer, G. F Molnar, D. I Cunic, and R. Chen Effects of peripheral sensory input on cortical inhibition in humans J. Physiol., October 15, 2002; 544(2): 617 - 629. [Abstract] [Full Text] [PDF]

				H. Ojima and K. Murakami Intracellular Characterization of Suppressive Responses in Supragranular Pyramidal Neurons of Cat Primary Auditory Cortex In Vivo Cereb Cortex, October 1, 2002; 12(10): 1079 - 1091. [Abstract] [Full Text] [PDF]

				S. C. Gandevia Spinal and Supraspinal Factors in Human Muscle Fatigue Physiol Rev, October 1, 2001; 81(4): 1725 - 1789. [Abstract] [Full Text] [PDF]

				T. D Sanger, R. R Garg, and R. Chen Interactions between two different inhibitory systems in the human motor cortex J. Physiol., January 15, 2001; 530(2): 307 - 317. [Abstract] [Full Text] [PDF]

				H. Tokuno and A. Nambu Organization of Nonprimary Motor Cortical Inputs on Pyramidal and Nonpyramidal Tract Neurons of Primary Motor Cortex: An Electrophysiological Study in the Macaque Monkey Cereb Cortex, January 1, 2000; 10(1): 58 - 68. [Abstract] [Full Text] [PDF]

				Z. Shao and A. Burkhalter Role of GABAB Receptor-Mediated Inhibition in Reciprocal Interareal Pathways of Rat Visual Cortex J Neurophysiol, March 1, 1999; 81(3): 1014 - 1024. [Abstract] [Full Text] [PDF]

				H. R. Siebner, J. M. Tormos, A. O. C. Baumann, C. Auer, M. D. Catala, B. Conrad, and A. Pascual-Leone Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer's cramp Neurology, February 1, 1999; 52(3): 529 - 529. [Abstract] [Full Text] [PDF]

				Y. Kang, K. Endo, T. Araki, and T. Kaneko Trans-synaptically Induced Bursts in Regular Spiking Non-pyramidal Cells in Deep Layers of the Cat Motor Cortex Cereb Cortex, January 1, 1999; 9(1): 77 - 89. [Abstract] [Full Text] [PDF]

				T. K. Hensch, M. Fagiolini, N. Mataga, M. P. Stryker, S. Baekkeskov, and S. F. Kash Local GABA Circuit Control of Experience-Dependent Plasticity in Developing Visual Cortex Science, November 20, 1998; 282(5393): 1504 - 1508. [Abstract] [Full Text]

				A. Kapur, R. A. Pearce, W. W. Lytton, and L. B. Haberly GABAA-Mediated IPSCs in Piriform Cortex Have Fast and Slow Components With Different Properties and Locations on Pyramidal Cells J Neurophysiol, November 1, 1997; 78(5): 2531 - 2545. [Abstract] [Full Text] [PDF]

				D. Contreras, N. Durmuller, and M. Steriade Absence of a Prevalent Laminar Distribution of IPSPs in Association Cortical Neurons of Cat J Neurophysiol, November 1, 1997; 78(5): 2742 - 2753. [Abstract] [Full Text] [PDF]

				R. Cerne and W. J. Spain GABAA Mediated Afterdepolarization in Pyramidal Neurons From Rat Neocortex J Neurophysiol, February 1, 1997; 77(2): 1039 - 1045. [Abstract] [Full Text] [PDF]