Control of remembered reaching sequences in monkey. II. Storage and preparation before movement in motor and premotor cortex.

Single-neuron responses in motor and premotor cortex were recorded during a movement-sequence delay task. On each trial the monkey viewed a randomly selected sequence of target lights arrayed in two-dimensional space, remembered the sequence during a delay period, and then generated a coordinated sequence of movements to the remembered targets. Of 307 neurons studied, 25% were tuned specifically for either the first or the second target, but not both. In particular, for neurons tuned during both target presentations, tuned activity related to a particular first target direction were maintained during the presentation of a second target in a different direction. During the delay period, 32% of the neurons were tuned for upcoming movement in a single direction. These delay period responses often reflected activity patterns that first developed during target presentations and may therefore act to maintain target period information during the delay. Neurons with tuned activity during both the delay and movement periods exhibited two patterns: the first exhibited tuned responses during the delay that were correlated with the tuning of first-movement responses, while the second pattern showed delay-period tuning that was better correlated with tuned responses during second movements. This indicates that, before movement, distinct neural populations are correlated with specific movements in a sequence. About half the neurons studied were not directionally tuned during the initiation, target, or delay periods, but did show systematic changes in activity during task performance. Some (34%) were exclusively tuned during movement and appear to be involved in the direct control of movement. Others (17%) showed changes in firing rate from period to period within a trial but showed no directional preference for a particular direction of movement. Population analyses of tuned activity during the target and delay periods indicated that accurate directional information about both first and second movements was available in the neuronal ensemble well before reaching began. These results extend the idea that both motor and premotor cortex play a role in reaching behavior other than the direct control of muscles. While some early neural responses resembled muscle activation patterns involved in maintaining fixed postures before movement, others probably relate to the sensory-to-motor transformations, information storage in short-term memory, and movement preparation required to generate accurate reaching to remembered locations in space.