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The Journal of Neuroscience, May 1, 1998, 18(9):3416-3425

Calcium Waves Precede Electrophysiological Changes of Spreading Depression in Hippocampal Organ Cultures

Phillip E. Kunkler¹ and Richard P. Kraig^{1, 2, 3}

Departments of ¹ Neurology and ² Pharmacological and Physiological Sciences, and ³ Committee on Neurobiology, The University of Chicago, Chicago, Illinois 60637

Although intercellular Ca²⁺ waves resemble spreading depression (SD) and occur in hippocampal organ cultures (HOTCs), SD has not been reported in these cultures. Accordingly, electrophysiological and Ca²⁺ imaging techniques were used to examine potential interrelations between Ca²⁺ waves and electrophysiological changes of SD. Our results show, for the first time, that HOTCs can support SD. Furthermore, two distinct Ca²⁺ waves were found to precede SD. The first traveled >100 µm/sec along the pyramidal cell dendritic layer. The second subsequently traveled mostly perpendicular to the pyramidal cell layer from CA3 (or CA1) but also in all directions from its area of initiation. This second, slower wave spread with the interstitial DC change of SD at millimeters per minute but always ahead of it by 6-16 sec. Heptanol, which uncouples gap junctions, blocked both of these Ca²⁺ waves and SD. Thus, two types of Ca²⁺ waves occur with the initiation and propagation of SD. The first might reflect interneuronal changes linked by gap junctions, whereas the second might stem from interastrocyte changes linked via similar connections. Because individual cells can be followed in space and time for protracted periods in HOTCs, this preparation may be ideal for studies designed to explore not only the mechanisms of SD but also the long-term consequences of SD, such as ischemic tolerance.

Key words: calcium waves; spreading depression; hippocampal organ cultures; ischemic tolerance; astrocytes; calcium-sensitive dyes; Fluo-3

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Copyright © 1998 Society for Neuroscience  0270-6474/98/1893416-10$05.00/0

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