Making your next move: dorsolateral prefrontal cortex and planning a sequence of actions in freely moving monkeys

Prefrontal damage disrupts planning, as measured by disorders of the activities of daily living (Humphreys & Forde, 1998; Shallice & Burgess, 1991). In a monkey model of this form of planning, a variant of the delayed alternation task was performed by freely moving monkeys. In a 16 x 16-ft. testing room, four feeders were located in the middle of each wall. In the north task, monkeys alternated between feeders: west-north-east-north-west, and so forth. In the south task, the alternation sequence was east-south-west-south-east, and so forth. Neuronal activity was recorded during walking along the eight paths, constituting the north and south tasks. To succeed, monkeys had to memorize the alternation rule and monitor both their place in the sequence and the previously made spatially directed action before deciding to walk to a new location to the left or right of the current location. Responsive dorsolateral prefrontal neurons are strikingly selective. Sustained neuronal activity reflects the spatial direction of an ongoing or upcoming response. It is important that such selective responses occur in one but not both tasks, even though the movements are exactly the same in both tasks and at each location. We suggest that selective neuronal activity is tuned through learning and reflects the fundamental units of a planning mechanism: Individual neurons encode specific components of a sequence of behavioral actions and their temporal order. Populations of such neurons represent all the steps necessary to perform the north and south tasks. The sustained activity of these neurons suggests that planning and working memory mechanisms are integrated.