Ontogeny of Feline Temporal Lobe Epilepsy. III: Spontaneous Sleep and Arousal Disorders in Amygdala‐Kindled Kittens

Abstract

We report the ontogeny and persistence of sleep and arousal disorders in amygdala-kindled kittens. We also identify procedural differences that may explain discrepancies in the literature on postkindling sleep disorders. The study population consisted of 12 preadolescent kittens kindled between 2.5 and 6.5 months of age, 8 of which were followed to adulthood (> or = 1 year), and 8 unkindled implanted control animals. Sleep and seizure patterns were monitored on 12-24-h polygraphic or split-screen video recordings of EEG and behavioral activity. Kindled kittens displayed spontaneous seizure and interictal sleep anomalies that persisted to adulthood, as follows. As compared with neurosurgical controls, kindled kittens exhibited slow-wave sleep (SWS) and REM sleep insomnia at least 1 year after kindling and 1-5 months after convulsions, regardless of postictal recording delay. Sleep and arousal defects in kindled kittens were similar to but more pronounced than those in kindled adult cats, possibly because kittens spontaneously became epileptic. Detection of postkindling SWS insomnia could be masked by brief scoring epochs (less than the preferred 1-min epoch for cats); recurrent behavioral arousals after kindling frequently aborted 1-min SWS epochs but often did not interrupt 30-s SWS epochs (based on 1-min vs. 30-s minimum duration scoring criteria). Detection of postkindling REM sleep insomnia could be masked in kittens with alternating patterns of REM loss and REM rebound; all these kittens showed periodic bouts of REM onset from waking after kindling. Different data collection and analysis procedures influence detection of sleep and arousal disorders in amygdala-kindled cats when replication of findings is attempted. We conclude that these differences explain some controversies regarding the nature and prevalence of sleep disturbances in the kindling literature in temporal lobe epilepsy (TLE).

Kindling Limits the Interictal Neuronal Temporal Response Properties in Cat Primary Auditory Cortex

“…Thus we speculate that decreased sleep‐spindle activity and the appearance of strong delta waves may be a potential cause of the reduced modulation frequency seen in this study. Several previous studies demonstrated that kindling can alter sleep patterns in cats (28–30), including a slow‐wave‐sleep insomnia (31).…”

Paroxysmal Microarousals in Amygdala‐Kindled Kittens: Could They Be Subclinical Seizures?

“…The criteria we use to score sleep stages has been described in detail (Shouse et al, 1994) and compared with human scoring procedures. The three main differences in our criteria are use of a I-min minimum duration criterion to score onset or shift from a stable sleep or waking state, use of 1-min scoring epochs to score continuation of a stable state after onset, and methods for distinguishing depth of non-rapid eye movement (NREM) sleep.…”

“…Higher rates of disruptive, epileptiform microarousals during sleep correlated with sleep fragmentation (r = -0.68, p < 0.05). Sleep fragmentation was indexed by reduced time in stable sleep states in kindled kittens as compared to unkindled controls (Table 1) (Shouse et al, 1994). The ratio of disruptive epileptiform arousals to total arousals was the most reliable predictor of interictal sleep disruption of several factors assessed, such as history or frequency of spontaneous GTCs (r = 0.01, NS) and postictal recording delay ( r = 0.3, NS).…”

“…We chose kindled kittens because they tend to develop spontaneous seizures that persist to adulthood (age 3 1 year), whereas cats kindled as adults rarely do (Shouse et al, 1990a(Shouse et al, ,b, 1992(Shouse et al, , 1994. Because various postkindling anomalies in kittens persist to adulthood, findings should be relevant to various age groups.…”