TY - JOUR

T1 - Effects of excitation of sensory pathways on the membrane potential of cat masseter motoneurons before and during cholinergically induced motor atonia

AU - Kohlmeier, Kristi Anne

AU - López-Rodríguez, F

AU - Morales, F R

AU - Chase, M H

PY - 1998

Y1 - 1998

N2 - Electrical stimulation of the nucleus pontis oralis during wakefulness enhances somatic reflex activity; identical stimuli during the motor atonia of active (rapid eye movement) sleep induces reflex suppression. This phenomenon, which is called reticular response-reversal, is based upon the generation of excitatory postsynaptic potential activity in motoneurons during wakefulness and inhibitory postsynaptic potential activity during the motor atonia of active sleep. In the present study, instead of utilizing artificial electrical stimulation to directly excite brainstem structures, we sought to examine the effects on motoneurons of activation of sensory pathways by exogenously applied stimuli (auditory) and by stimulation of a peripheral (sciatic) nerve. Accordingly, we examined the synaptic response of masseter motoneurons prior to and during cholinergically induced motor atonia in a pharmacological model of active sleep-specific motor atonia, the alpha-chloralose-anesthetized cat, to two different types of afferent input, one of which has been previously demonstrated to elicit excitatory motor responses during wakefulness. Following the pontine injection of carbachol, auditory stimuli (95 dB clicks) elicited a hyperpolarizing potential in masseter motoneurons. Similar responses were obtained upon stimulation of the sciatic nerve. Responses of this nature were never seen prior to the injection of carbachol. Thus, stimulation of two different afferent pathways (auditory and somatosensory) that produce excitatory motor responses during wakefulness instead, during motor atonia, results in the inhibition of masseter motoneurons. The switching of the net result of the synaptic response from one of potential motor excitation to primarily inhibition in response to the activation of sensory pathways was comparable to the phenomenon of reticular response-reversal. This is the first report to examine the synaptic mechanisms whereby exogenously or peripherally applied stimuli that elicit motor excitation during wakefulness instead elicit inhibitory motor responses during the motor atonia of active sleep. Thus, not only are motoneurons tonically inhibited during active sleep, but the selective elicitation of inhibitory motor responses indicates that this inhibition can be phasically increased in response to sensory stimuli, possibly in order to maintain the state of active sleep. The data provided the foundation for the hypothesis that, during naturally occurring active sleep, there is a change in the control of motor systems so that motor suppression occurs in response to stimuli that would otherwise, if present during other behavioral states, result in the facilitation of motor activity.

AB - Electrical stimulation of the nucleus pontis oralis during wakefulness enhances somatic reflex activity; identical stimuli during the motor atonia of active (rapid eye movement) sleep induces reflex suppression. This phenomenon, which is called reticular response-reversal, is based upon the generation of excitatory postsynaptic potential activity in motoneurons during wakefulness and inhibitory postsynaptic potential activity during the motor atonia of active sleep. In the present study, instead of utilizing artificial electrical stimulation to directly excite brainstem structures, we sought to examine the effects on motoneurons of activation of sensory pathways by exogenously applied stimuli (auditory) and by stimulation of a peripheral (sciatic) nerve. Accordingly, we examined the synaptic response of masseter motoneurons prior to and during cholinergically induced motor atonia in a pharmacological model of active sleep-specific motor atonia, the alpha-chloralose-anesthetized cat, to two different types of afferent input, one of which has been previously demonstrated to elicit excitatory motor responses during wakefulness. Following the pontine injection of carbachol, auditory stimuli (95 dB clicks) elicited a hyperpolarizing potential in masseter motoneurons. Similar responses were obtained upon stimulation of the sciatic nerve. Responses of this nature were never seen prior to the injection of carbachol. Thus, stimulation of two different afferent pathways (auditory and somatosensory) that produce excitatory motor responses during wakefulness instead, during motor atonia, results in the inhibition of masseter motoneurons. The switching of the net result of the synaptic response from one of potential motor excitation to primarily inhibition in response to the activation of sensory pathways was comparable to the phenomenon of reticular response-reversal. This is the first report to examine the synaptic mechanisms whereby exogenously or peripherally applied stimuli that elicit motor excitation during wakefulness instead elicit inhibitory motor responses during the motor atonia of active sleep. Thus, not only are motoneurons tonically inhibited during active sleep, but the selective elicitation of inhibitory motor responses indicates that this inhibition can be phasically increased in response to sensory stimuli, possibly in order to maintain the state of active sleep. The data provided the foundation for the hypothesis that, during naturally occurring active sleep, there is a change in the control of motor systems so that motor suppression occurs in response to stimuli that would otherwise, if present during other behavioral states, result in the facilitation of motor activity.

KW - Acoustic Stimulation

KW - Afferent Pathways

KW - Animals

KW - Brain Stem

KW - Carbachol

KW - Cats

KW - Chloralose

KW - Electric Stimulation

KW - Electroencephalography

KW - Electromyography

KW - Electrooculography

KW - Masseter Muscle

KW - Membrane Potentials

KW - Motor Neurons

KW - Muscle Denervation

KW - Reflex

KW - Sciatic Nerve

KW - Sleep, REM

M3 - Journal article

C2 - 9881869

VL - 86

SP - 557

EP - 569

JO - Neuroscience

JF - Neuroscience

SN - 0306-4522

IS - 2

ER -