Sleep-waking states develop independently in the isolated forebrain and brain stem following early postnatal midbrain transection in cats

We report the effects of permanently separating the immature forebrain from the brain stem upon sleeping and waking development. Kittens ranging from postnatal 9 to 27 days of age sustained a mesencephalic transection and wer e maintained for tip to 135 days. Prior to postnatal day 40, the electroenc ephalogram of the isolated forebrain and behavioral sleep-wakefulness of th e decerebrate animal showed the immature patterns of normal young kittens. Thereafter, the isolated forebrain showed alternating sleep-wakefulness ele ctrocortical rhythms similar to the corresponding normal patterns of intact , mature cats. Olfactory stimuli generally changed forebrain sleeping into waking activity, and in cats with the section behind the third nerve nuclei , normal correlates of eye movements-pupillary activity with electrocortica l rhythms were present. Behind the transection, decerebrate animals showed wakefulness, and after 20 days of age displayed typical behavioral episodes of rapid eye movements sleep and, during these periods, the pontine record ings showed ponto-geniculo-occipital waves, which are markers for this slee p stage, together with muscle atonia and rapid lateral eye movements. Typic ally, but with remarkable exceptions suggesting humoral interactions, the s leep-waking patterns of the isolated forebrain were dissociated from those of the decerebrate animal. These results were very similar to our previous findings in midbrain-transected adult cats. However, subtle differences sug gested greater functional plasticity in the developing versus the adult iso lated forebrain. We conclude that behavioral and electroencephalographic patterns of non-rap id eye movement sleep and of rapid eye movement sleep states mature indepen dently in the forebrain and the brain stem, respectively, after these struc tures are separated early postnatally. In terms of waking, the findings str engthen our concept that in higher mammals the rostral brain can independen tly support wakefulness/arousal and, hypothetically, perhaps even awareness . Therefore, these basic sleeping-waking functions are intrinsic properties of the forebrain/brain stem and as such can develop autochthonously. These data help our understanding of some normal/borderline sleep-waking dissoci ations as well as peculiar states of consciousness in long term patients wi th brain stem lesions. (C) 2001 IBRO. Published by Elsevier Science Ltd. Al l rights reserved.