Neuronal firing patterns from epileptogenic foci of monkey and human

The chronic, recurrent seizures induced in the monkey by cortical scarring occur spontaneously for years and share much of the phenomenology of spontaneous seizures of focal cortical onset in the human. Chronic extracellular recording in the focus of the chronic epileptic monkey reveals: A spectrum of abnormalities of unit firing ranging from grossly abnormal firing patterns to normal activity. Group I (highly epileptic) neurons fire exclusively in bursts, which are invariant during different behavioral states and during operant conditioning. Although firing within the bursts is not easily modified, the interburst interval can be modified indicating that these apparently denervated cells still have some synaptic input. All group I cells are pyramidal neurons. Group II (weakly epileptic) neurons exhibit variable burst firing, which may be intermixed with normal unit firing. The firing patterns of these cells can be modified by synaptic inputs. During operant conditioning, burst firing can decrease; during drowsiness or when inattentive, burst firing can approach that characteristic of group I cells. There is a direct relationship between the number of group I epileptic (pacemaker) neurons in the focus and the epileptogenicity of that focus as measured by frequency of spontaneous seizures in that monkey. The distribution of neurons encountered in the focus varies. On average, approximately 10% are group I (pacemaker) neurons; group II constitute 40%; and 50% of cells encountered exhibit normal firing patterns. In addition to firing in unstructured bursts, an unusual burst structure termed the long-first-interval (LFI) burst has been described that appears to be unique to the chronic focus. It is so named because the first interspike interval is longer than the remaining interspike intervals in the burst. The long first interval is extraordinarily invariant. There is little relationship between unit firing in bursts and the interictal EEG. During early parts of a spontaneous seizure, the two events become time-locked. During seizures, unit firing is synchronous with surrounding neurons and the spike portion of the EEG (as in penicillin foci). Firing of group I neurons does not change significantly preceding a spontaneous seizure. Thus, group I neurons appear to act as pacemakers to the focus and group II cells provide the critical mass that, when synchronized to the burst firing of the pacemakers, is capable of initiating the ictal event.