Event-related potentials in an invertebrate: crayfish emit 'omitted stimulus potentials'

Electrical signs of neural activity correlated with stimuli or states include a subclass called event-related potentials. These overlap with, but can often be distinguished from, simple stimulus-bound evoked potentials by their greater dependence on endogenous (internal state) factors. Studied mainly in humans, where they are commonly associated with cognition, they are considered to represent objective signs of moderately high-level brain processing. We tested the hypothesis that invertebrates lack such signs by looking in the crayfish Procambarus clarkii for a class of OFF-effects shown in humans to index expectancy. Disproving the hypothesis, we find, using chronic, implanted preparations, that a good omitted stimulus potential is reliably present. The system learns in a few cycles of a regularly repeated light flash to expect one on schedule. Omitted stimulus potentials are found in the protocerebrum, the circumesophageal connective and in the optic tract - perhaps arising in the retina, as in vertebrates. These potentials can be very local and can include loci with and without direct visual evoked potentials in response to each flash. In some loci, the omitted stimulus potential has a slow wave component, in others only a spike burst. Omitted stimulus potentials are more endogenous than visual evoked potentials, with little dependence on flash or ambient light intensity or on train duration. They vary little in size at different times of the day, but abruptly fail to appear if the ambient light is cut off. They can occur during walking, eating or the maintained defense posture but are diminished by 'distraction' and are often absent from an inert crayfish until it is aroused. We consider this form of apparent expectation of a learned rhythm (a property that makes it 'cognitive' in current usage), to be one of low level, even though some properties suggest endogenous factors. The flashes in a train have an inhibitory effect on a circuit that quickly 'learns' the stimulus interval so that the omitted stimulus potential, ready to happen after the learned interval, is prevented by each flash, until released by a missing stimulus.