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J Physiol Volume 586, Number 7, 1867-1883, April 1, 2008 DOI: 10.1113/jphysiol.2007.146159
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NEUROSCIENCE

Network hyperexcitability within the deep layers of the pilocarpine-treated rat entorhinal cortex

 Philip de Guzman1, Yuji Inaba1, Enrica Baldelli2, Marco de Curtis3, Giuseppe Biagini2 and Massimo Avoli1,4

1 Montreal Neurological Institute and Departments of Neurology & Neurosurgery, and of Physiology, McGill University, Montreal, QC, H3A 2B4, Canada
2 Dipartimento di Scienze Biomediche, Università di Modena e Reggio Emilia, 41100 Modena, Italy
3 Fondazione Istituto Neurologico C. Besta, 20133 Milano, Italy
4 Dipartimento di Medicina Sperimentale, Università di Roma La Sapienza, 00185 Roma, Italy

In this study we report that in the presence of normal buffer, epileptiform discharges occur spontaneously (duration = 2.60 ± 0.49 s) or can be induced by electrical stimuli (duration = 2.50 ± 0.62 s) in the entorhinal cortex (EC) of brain slices obtained from pilocarpine-treated rats but not in those from age-matched, nonepileptic control (NEC) animals. These network-driven epileptiform events consist of field oscillatory sequences at frequencies greater than 200 Hz that most often initiate in the lateral EC and propagate to the medial EC with 4–63 ms delays. The NMDA receptor antagonist CPP depresses the rate of occurrence (P < 0.01) of these spontaneous epileptiform discharges but fails in blocking them. Paradoxically, stimulus-induced epileptiform responses are enhanced in duration during CPP application. However, concomitant application of NMDA and non-NMDA glutamatergic antagonists abolishes spontaneous and stimulus-induced epileptiform events. Intracellular recordings from lateral EC layer V cells indicate a lower frequency of spontaneous hyperpolarizing postsynaptic potentials in pilocarpine-treated tissue than in NEC (P < 0.002) both under control conditions and with glutamatergic receptor blockade; the reversal potential of pharmacologically isolated GABAA receptor-mediated inhibitory postsynaptic potentials has similar values in the two types of tissue. Finally, immunohistochemical analysis shows that parvalbumin-positive interneurons are selectively reduced in number in EC deep layers. Collectively, these results indicate that reduced inhibition within the pilocarpine-treated EC layer V may promote network epileptic hyperexcitability.

(Received 3 October 2007; accepted after revision 29 January 2008; first published online 31 January 2008)
Corresponding author M. Avoli: 3801 University Street, Montreal, QC, H3A 2B4, Canada. Email: massimo.avoli{at}mcgill.ca






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