Journal of Neurophysiology, Vol 65, Issue 5 1055-1066, Copyright © 1991 by APS

ARTICLES

Osmotic effects on the CA1 neuronal population in hippocampal slices with special reference to glucose

B. A. Ballyk, S. J. Quackenbush and R. D. Andrew
Department of Anatomy, Queen's University, Kingston, Ontario, Canada.

1. Lowered osmolality promotes epileptiform activity both clinically and in the hippocampal slice preparation, but it is unclear how neurons are excited. We studied the effects of altered osmolality on the electrophysiological properties of CA1 pyramidal cells in hippocampal slices by the use of field and intracellular recordings. The excitability of these neurons under various osmotic conditions was gauged by population spike (PS) amplitude, single cell properties, and evoked synaptic input. 2. The orthodromic PS recorded in stratum pyramidale and the field excitatory postsynaptic potential (EPSP) in stratum radiatum were inversely proportional in amplitude to the artificial cerebrospinal fluid (ACSF) osmolality over a range of +/- 80 milliosmoles/kgH2O (mosM). The effect was osmotic because changes occurred within the time frame expected for cellular expansion or shrinkage and because permeable substances such as dimethyl sulfoxide or glycerol were without effect. Dilutional changes in ACSF constituents were experimentally ruled out as promoting excitability. 3. To test whether the field data resulted from a change in single-cell excitability, CA1 cells were intracellularly recorded during exposure to +/- 40 mosM ACSF over 15 min. There was no consistent effect upon CA1 resting potential, cell input resistance, or action potential threshold. 4. Osmotic alteration of orthodromic and antidromic field potentials might involve a change in axonal excitability. However, the evoked afferent volley recorded in CA1 stratum pyramidale or radiatum, which represents the compound action potential (CAP) generated in presynaptic axons, remained osmotically unresponsive with regard to amplitude, duration, or latency. This was also characteristic of CAPs evoked in isolated sciatic and vagus nerve preparations exposed to +/- 80 mosM. Therefore axonal excitability and associated extracellular current flow generated periaxonally are not significantly affected by osmotic shifts. 5. The osmotic effect on field potential amplitudes appeared to be independent of synaptic transmission because the inverse relationship with osmolality held for the antidromically evoked PS. Moreover, as recorded with respect to ground, the intracellular EPSP-inhibitory postsynaptic potential (IPSP) sequence (evoked from CA3 stratum radiatum) was not altered by osmolality. 6. The PS could occasionally be recorded intracellularly as a brief negativity interrupting the evoked EPSP. In hyposmotic ACSF, the amplitude increased and action potentials arose from the trough of the negativity as expected for a field effect. This is presumably the result of enhanced intracellular channeling of current caused by the increased extracellular resistance that accompanies cellular swelling.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				R. D. Andrew, M. W. Labron, S. E. Boehnke, L. Carnduff, and S. A. Kirov Physiological Evidence That Pyramidal Neurons Lack Functional Water Channels Cereb Cortex, April 1, 2007; 17(4): 787 - 802. [Abstract] [Full Text] [PDF]

				J. E. Fox, M. Bikson, and J. G. R. Jefferys Tissue Resistance Changes and the Profile of Synchronized Neuronal Activity During Ictal Events in the Low-Calcium Model of Epilepsy J Neurophysiol, July 1, 2004; 92(1): 181 - 188. [Abstract] [Full Text] [PDF]

				G.-F. Tian and A. J. Baker Protective Effect of High Glucose Against Ischemia-Induced Synaptic Transmission Damage in Rat Hippocampal Slices J Neurophysiol, July 1, 2002; 88(1): 236 - 248. [Abstract] [Full Text] [PDF]

				M. A. Whittington, H. C. Doheny, R. D. Traub, F. E. N. LeBeau, and E. H. Buhl Differential Expression of Synaptic and Nonsynaptic Mechanisms Underlying Stimulus-Induced Gamma Oscillations In Vitro J. Neurosci., March 1, 2001; 21(5): 1727 - 1738. [Abstract] [Full Text] [PDF]

				E. Bracci, M. Vreugdenhil, S. P. Hack, and J. G. R. Jefferys On the Synchronizing Mechanisms of Tetanically Induced Hippocampal Oscillations J. Neurosci., September 15, 1999; 19(18): 8104 - 8113. [Abstract] [Full Text] [PDF]

				N. R. Kreisman and J. C. LaManna Rapid and Slow Swelling During Hypoxia in the CA1 Region of Rat Hippocampal Slices J Neurophysiol, July 1, 1999; 82(1): 320 - 329. [Abstract] [Full Text] [PDF]

				L. Tao Effects of Osmotic Stress on Dextran Diffusion in Rat Neocortex Studied With Integrative Optical Imaging J Neurophysiol, May 1, 1999; 81(5): 2501 - 2507. [Abstract] [Full Text] [PDF]

				K. G. Lurie, A. Sugiyama, S. McKnite, P. Coffeen, K. Hashimoto, and S. Motomura Modulation of AV nodal and Hisian conduction by changes in extracellular space Am J Physiol Heart Circ Physiol, March 1, 1999; 276(3): H953 - H960. [Abstract] [Full Text] [PDF]

				S. C. Baraban and P. A. Schwartzkroin Effects of Hyposmolar Solutions on Membrane Currents of Hippocampal Interneurons and Mossy Cells In Vitro J Neurophysiol, February 1, 1998; 79(2): 1108 - 1112. [Abstract] [Full Text] [PDF]

				R. Huang, D. F. Bossut, and G. G. Somjen Enhancement of Whole Cell Synaptic Currents by Low Osmolarity and by Low [NaCl] in Rat Hippocampal Slices J Neurophysiol, May 1, 1997; 77(5): 2349 - 2359. [Abstract] [Full Text] [PDF]