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J Physiol Volume 558, Number 3, 825-839, August 1, 2004 DOI: 10.1113/jphysiol.2004.065649
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Electrotonic coupling between stratum oriens interneurones in the intact in vitro mouse juvenile hippocampus

Xiao-Lei Zhang1,3, Liang Zhang2,3 and Peter L. Carlen1,2,3

Departments of
1 Physiology
2 Medicine, University of Toronto, Toronto, Ontario, Canada
3 Toronto Western Research Institute, University Health Network, 399 Bathurst Street, Toronto, Ontario, Canada M5T 2S8

Using the isolated juvenile (7–14 days) mouse whole hippocampus preparation, which contains intact complex local circuitry, 145 dual whole cell recordings were made from stratum oriens (s.o.) interneurones under infrared microscopy. In 11.7% of paired recordings, evidence for direct electrotonic coupling between the s.o. interneurones was obtained from the response of one interneurone to a long (400–600 ms) constant current pulse passed into the coupled interneurone. When specifically orienting the dual recordings in the transectional plane of the hippocampus, 18.5% of paired recordings showed electrotonic coupling. The coupling coefficient, estimated from averaged data, was 6.9 ± 4.7%, ranging from 1.3 to 17.6%. The time constant of the electrotonically transmitted hyperpolarization was inversely related to the coupling coefficient between the two neurones. The electrotonic responses of one neurone to constant current pulses injected into the other coupled neurone were intermittent. Spikes in one of the coupled neurones were associated with small electrotonic EPSPs (spikelets) in the other coupled neurone, in those neuronal pairs with coupling coefficients greater than 10%. Failure of spikelet production following a spike in the coupled cell occurred 5–10% of the time. Electrotonic coupling and spikelets persisted in the presence of chemical synaptic transmission blockade by CNQX, APV and bicuculline, or in zero Ca2+ perfusate, but were abolished by carbenoxolone (100 µM), a gap junctional blocker. These data confirm the existence of electrotonic coupling between s.o. interneurones, presumably via gap junctions located in dendrites.

(Received 5 April 2004; accepted after revision 9 June 2004; first published online 11 June 2004)
Corresponding author P. L. Carlen: McL 12-413, Toronto Western Hospital, 399 Bathurst Street, Toronto, Canada, M5T 2S8. Email: carlen{at}uhnres.utoronto.ca




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