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Engagement of Rat Striatal Neurons by Cortical Epileptiform Activity Investigated With Paired Recordings

¹Department of Optometry and Neuroscience, University of Manchester Institute of Science and Technology, Manchester M60 1QD, United Kingdom; ²Clinica Neurologica, Dipartimento di Neuroscienze, Università "Tor Vergata," Rome 00133; and ³Fondazione Santa Lucia, Rome 00179, Italy

Submitted 7 June 2004; accepted in final form 2 July 2004

The striatum is thought to play an important role in the spreading of epilepsy from cortical areas to deeper brain structures, but this issue has not been addressed with intracellular techniques. Paired recordings were used to assess the impact of cortical epileptiform activity on striatal neurons in brain slices. Bath-application of 4-amynopyridine (100 µM) and bicuculline (20 µM) induced synchronized bursts in all pairs of cortical neurons (5 mm apart) in coronal, sagittal, and oblique slices (which preserve connections from the medial agranular cortex to the striatum). Under these conditions, striatal medium spiny neurons (MSs) displayed a strong increased spontaneous glutamatergic activity. This activity was not correlated to the cortical bursts and was asynchronous in pairs of MSs. Sporadic, large-amplitude synchronous depolarizations also occurred in MSs. These events were simultaneously detected in glial cells, suggesting that they were accompanied by considerable increases in extracellular potassium. In oblique slices, cortically driven bursts were also observed in MSs. These events were synchronized to cortical epileptiform bursts, depended on non–N-methyl-D-aspartate (NMDA) glutamate receptors, and persisted in the cortex, but not in the striatum, after disconnection of the two structures. During these bursts, MS membrane potential shifted to a depolarized value (59 ± 4 mV) on which an irregular waveform, occasionally eliciting spikes, was superimposed. Thus synchronous activation of a limited set of corticostriatal afferents can powerfully control MSs. Cholinergic interneurons located <120 µm from simultaneously recorded MSs, did not display cortically driven bursts, suggesting that these cells are much less easily engaged by cortical epileptiform activity.

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