The tonic control of cortical responsiveness by inhibitory and facilitatory diffuse influences

Abstract

The responsiveness of the visual neothalamo-cortical complex in cats has been investigated by single or paired thalamo-cortical evoked potentials (E.P.), to obtain information about: (a) the brain-stem mechanisms able to maintain tonic cortical arousal; (b) the functional picture of the complex when deprived of the main ascending influences, and (c) its alteration by active inhibitory and facilitatory processes elicited by ascending influences, during effective arousal. 1. 1. The E.P. facilitation with after-effect, exerted by posterior hypothalamic or central gray stimulation, has been abolished by a caudal central gray lesion; thereafter direct RF stimulation has again induced facilitation, but without after-effect. These and related previous data show that a driving mechanism, having its main descending circuit in the periventricular and periaqueductal gray matter, interacts with the RF, establishing a positive feedback circuit, to maintain tonic arousal. This would explain the impairment of enduring wakefulness and the occurrence of ECoG spindles in animals with central gray or posterior hypothalamic lesions. 2. 2. Either a caudate or an RF (rostro-pontine to rostral midbrain) lesion induced a strong increase of the single (or first of a pair) E.P., suppressing first the natural variability, which however recovered as time elapsed (2–6 h); the 7–10 msec delayed second E.P. was enhanced as compared with the control before the lesion. 3. 3. The association of caudate and RF lesions induces an impressive enduring increase of the first E.P., as well as of the shortly delayed (10–20 msec) second one, which appears to be released from an inhibitory process which has been further increased in latency, since the longer delayed (20–50 msec) second E.P. is strongly inhibited, or absent. In addition, these preparations have often displayed enduring cortical seizures, spontaneous or induced at a very low threshold. A further lesion of the rostral thalamus has not changed this picture. 4. 4. An opposite pattern of responsiveness appears during strong arousal (only intact brain under RF stimulation, inducing facilitation of the first E.P.), since the shortly delayed E.P. (in the first 20 msec) is strongly inhibited, while the longer delayed (30–50 msec) second E.P. is facilitated. (The responsiveness of the animal which is not strongly aroused is not essential for the present investigation.) 5. 5. An intermediary, intracortical inhibitory network of neurones has been tentatively advanced; it would be excited by the first E.P., starting the cycle of inhibition, and only activated by ascending diffuse influences (arising in the caudate and pontine RF) whose impairment explains the proportional release from inhibition of only the shortly delayed second E.P., by increasing the latency of inhibition. The strong inhibition of the same response during arousal has been explained by strong activation of the network, acting also to prevent cortical seizures, like a negative feedback circuit whose impairment would obviously release self-sustained activity (§ 3). 6. 6. Midbrain RF stimulation after rostropontine and caudate lesions has resulted only in facilitating all E.P., at any delay. Some facilitatory influences have been separated; they have occurred spontaneously in the midpontine pretrigeminal preparation, their effect having not been counteracted, as in the aroused intact brain, by a more powerful inhibition exerted on the shortly delayed second responses (§ 4). 7. 7. The ECoG “activation” was seen only in conditions in which facilitatory influences might be inferred, irrespective of the contingent occurrence of active inhibition since the midpontine preparation itself displayed ECoG spindles when its central gray was destroyed. 8. 8. As a comprehensive consequence, a patterned blending of inhibitory and facilitatory influences is advanced as supporting effective arousal, tonically maintained by brain-stem circuits which would constitute a diffuse regulating system, including inhibitory, facilitatory and driving mechanisms. It would be only triggered by sensory events, since the brain is able to self-maintain certain patterns of cortical responsiveness through this system.