Different behaviors during paradoxical sleep without atonia depend on pontine lesion site.

Bilateral pontine tegmental lesions in cats release a state of paradoxical sleep (PS) without atonia that possess all other electrographic criteria of PS. PS without atonia has been previously considered as a unitary phenomenon, but the present work demonstrates that different behavioral syndromes result from different lesion placements. Five of 25 cats exhibited the minimal syndrome of increased proximal limb and head movements. The head was not raised; and coordinated behavior was not seen. The nuchal electromyogram (EMG) showed tone for 25-100% of such an episode. Selective destruction of the origin (n = 2) or caudally projecting fibers (n = 1), of the tegmentoreticular pathway released this minimal syndrome of unorganized limb and head movements. This pathway had previously been proposed to mediate atonia, but the present work demonstrates that additional damage is necessary to release tone completely as well as the elaborate behaviors discussed below. Eight cats raised their heads, righted their forequarters, and moved head, neck and forelimbs in movements resembling orienting, staring, reaching and attempting to stand. The lesions releasing such behavior were centered at P = 3.0, H = 2.0, V = -4.0, and damaged a region projecting to the superior colliculus. Two cats with slightly more ventral lesions did not exhibit the orienting behavior. Six cats demonstrated violent phasic behavior resembling attack punctuating tonic periods of quiet staring or searching movements. Attack resulted from damage extending rostroventrally into the midbrain at P = 2.0, H = 2.5, V = -4.5 (4/6) or from unilateral damage to a lateral pathway arising in the central amygdalar nucleus (2/6). In 4 cats, coordinated fore- and hindlimb activation resulted in locomotion during PS. Walking resulted from larger, more ventral lesions centered at P = 3.0, H = 2.0, V = -5.5. Considering the anatomy of the lesions in relationship to brain stem systems known to play a role in orienting, attack and locomotion, we conclude that inhibitory systems were damaged by these lesions and that PS without atonia is not simply a state during which neural activity of normal PS can be expressed behaviorally.