The mechanism of tonic inhibition of crayfish escape behavior: distal inhibition and its functional significance.

The excitability of crayfish escape behavior is seldom fully predictable. A major determinant of this fickleness is a form of descending inhibition that is reliably evoked during restraint or feeding and is called "tonic inhibition." Tonic inhibition was found to inhibit postsynaptically the lateral giant neurons, the command neurons for one form of escape. This inhibition is located on lateral giant dendrites that are electrotonically distant from the neuron's spike initiating zone. in contrast, the postsynaptic inhibition due to "recurrent inhibition," which prevents new escape responses from starting while a previously initiated one is in process, occurs proximally, near the spike initiating zone. The distalness of tonic inhibition could be an adaptation for selective suppression of parts of the lateral giant dendritic tree. Consistent with this, evidence was obtained that the tonic inhibitory system can suppress responses to specific sensory fields. An independent reason for targeting recurrent inhibition proximally and tonic inhibition distally was suggested by the functional requirements of each inhibitory process: recurrent inhibition needs to be "absolute" in the sense that the response should be absolutely prevented, whereas it must be possible to override tonic inhibition. Neuronal models demonstrated that proximal inhibition gives recurrent inhibition the required property of absoluteness while distal inhibition allows tonic inhibition to be overridden ("relativity"). It was shown that the relativity of distal inhibition arises from its interaction with the process of saturation of excitation and that tonic inhibition does indeed interact with excitatory saturation as predicted. It is suggested that the property of relativity of distal inhibition is exploited in other nervous systems as well.