Developing animals primarily receive two kinds of somatosensory input. One arises from stimulation in the external environment (“exafference”) and the other arises from self-produced movements (“reafference”), especially those associated with the myoclonic twitches during active sleep. Neural recordings have shown that exafferent and reafferent neural signals activate sensorimotor structures throughout the brain, but it is not known whether twitches are accompanied by corollary discharge that inform the nervous system that twitches are self-generated.
Recordings from the cerebellum in infant rats suggested that motor structures could be conveying twitch-related corollary discharge signals to the cerebellum. If true, one would expect to see evidence of corollary discharge in the precerebellar nuclei. We hypothesized that two precerebellar nuclei: the inferior olive (IO) and the lateral reticular nucleus (LRN), receive corollary discharge associated with the production of twitches. We tested the hypothesis by recording spontaneous activity of the IO and LRN during sleep and wake in infant rats.
In the majority of IO units, and in a subset of LRN units, neural activity was particularly pronounced at the time of twitch onset. This activity was remarkably precise, reaching a peak in firing within ±10 ms of a twitch. This unique pattern suggested that, unlike sensory areas that receive reafference from twitches, these two structures receive corollary discharge associated with the production of twitches.
Next, using anatomical tracing, immunohistochemistry, and neurophysiology, we identified non-overlapping premotor areas in the midbrain that send corollary discharge to the IO and LRN. Finally, using pharmacological inhibition, we identified that slow potassium channels are responsible for the sharp peak of twitch-related corollary discharge in the IO.
Altogether, the current findings suggest that the infant brain has the capacity to distinguish between exafferent stimulation and twitch-related reafference. This capacity may underlie the developing infant’s burgeoning ability to distinguish between self- and other-generated movements.