We explored the relative contributions of cortical and thalamic neuronal networks in the generation of electrical seizures that include spike-wave (SW) and polyspike-wave (PSW) complexes. Seizures were induced by systemic or local cortical injections of bicuculline, a gamma-aminobutyric acid-A (GABAA) antagonist, in cats under barbiturate anesthesia. Field potentials and extracellular neuronal discharges were recorded through arrays of eight tungsten electrodes (0.4 or 1 mm apart) placed over the cortical suprasylvian gyrus and within the thalamus. 1) Systemic injections of bicuculline induced SW/PSW seizures in cortex, whereas spindle sequences continued to be present in the thalamus. 2) Cortical suprasylvian injection of bicuculline induced focal paroxysmal single spikes that developed into full-blown seizures throughout the suprasylvian cortex. The seizures were characterized by highly synchronized SW or PSW complexes at 2-4 Hz, interspersed with runs of fast (10-15 Hz) activity. The intracellular aspects of this complex pattern in different types of neocortical neurons are described in the following paper. Complete decortication abolished the seizure, leaving intact thalamic spindles. Injections of bicuculline in the cortex of athalamic cats resulted in similar components as those occurring with an intact thalamus. 3) Injection of bicuculline in the thalamus decreased the frequency of barbiturate spindles and increased the synchrony of spike bursts fired by thalamocortical and thalamic reticular cells but did not induce seizures. Decortication did not modify the effects of bicuculline injection in the thalamus. Our results indicate that the minimal substrate that is necessary for the production of seizures consisting of SW/PSW complexes and runs of fast activity is the neocortex.