Eye movement-related modulation of trigeminal neuron activity during active sleep and wakefulness

Abstract

The amplitude of electrically-evoked mass action potentials recorded in the spinal cord and brainstem has been reported to decrease only during eye movement events of active sleep. In contrast, we have reported that the response of trigeminal sensory neurons to peripheral stimuli is modulated throughout the behavioral state of active sleep. It is unclear whether eye movement events contribute to the modulation of trigeminal sensory neuron activity during active sleep. In the present study, eye movement events were demarcated in order to investigate how these events affect peripheral input to trigeminal sensory neurons in chronic, intact, behaving cats. When compared with wakefulness, the mean response of 45 trigeminal sensory neurons to low-intensity electrical stimulation of the canine tooth pulp was significantly suppressed by 28% during periods of active sleep where no eye movement activity was present and by 41% during periods of active sleep with eye movement events. Hence, during active sleep, tooth pulp-evoked responses were significantly decreased by 16% during eye movement events when compared with non-eye movement active sleep. To investigate whether presynaptic inhibition played a role in this phenomenon, the excitability of eight individual tooth pulp afferent terminals during eye movement periods was compared with non-eye movement periods of active sleep. No evidence of eye movement-related depolarization of tooth pulp terminals was detected. When compared to wakefulness, the responses of six trigeminal sensory neurons to air puff stimulation of facial hair mechanoreceptors were significantly increased by 96% during periods of active sleep where no eye movement activity was present but were significantly decreased by 15% during eye movement events when compared with non-eye movement active sleep. The results of the present study indicate that neuronal responses to both tooth pulp and facial hair mechanoreceptor stimulation are significantly attenuated during eye movement events of active sleep.