Spontaneous paroxysmal circling behavior in the ci2 rat mutant: epilepsy with rotational seizures or hyperkinetic movement disorder?

Circling, turning, rotating, spinning, wheeling, and cursive hyperkinesia are all synonymous terms used to describe the active movement of an animal in a circular direction. Circling behavior can be evoked by unilateral electrical and chemical stimulation or lesions of various brain sites, but can also occur after systemic drug administration or spontaneously in normal animals or mutant rodents. In humans, stereotypic body rotation can occur as a distinctive entity of generalized and focal epilepsy, and may be due to involvement of the striatum. We have previously described a Lewis rat mutant (ci2) with a behavioral phenotype characterized by lateralized circling, hyperactivity, opisthotonus, and ataxia. In these rats, circling occurs in phases or bursts either spontaneously or in response to stress. Neurochemical data indicate that the circling behavior of the ci2 mutants is related to an abnormal asymmetry in dopaminergic activity in the striatum. Because of the similarities to rotational epilepsy, we used video and electroencephalographic recordings to study whether the rotational behavior of the ci2 mutant rat is a result of a partial or generalized epilepsy. Epileptic WAG/Rij rats were used for comparison. Video monitoring of ci2 rats in the absence of any stress or disturbance showed that circling occurs in paroxysmal bursts during active wakefulness, but not during passive wakefulness or sleep. Circling was not preceded or followed by any convulsive motor seizures and was not associated with epileptiform abnormalities in the electroencephalogram, whereas WAG/Rij rats exhibited myoclonic seizures and epileptic spike-wave discharges during passive wakefulness and sleep. As a result of the association of circling with active wakefulness, ci2 rats exhibited many more rotations during the dark (active) phase compared with the light (rest) period. Increase in active wakefulness during the light phase by transfer of the rats to a new environment induced or intensified circling behavior. Most ci2 rats showed a consistent lateral preference during circling, but some rats changed their preference from one session to another. The data indicate that spontaneous paroxysmal circling behavior in the ci2 rat is not a consequence of epilepsy but reflects a hyperkinetic movement disorder with abnormal lateralization of brain function.