Academic journal article Cognitive, Affective and Behavioral Neuroscience

Making Your Next Move: Dorsolateral Prefrontal Cortex and Planning a Sequence of Actions in Freely Moving Monkeys

Academic journal article Cognitive, Affective and Behavioral Neuroscience

Making Your Next Move: Dorsolateral Prefrontal Cortex and Planning a Sequence of Actions in Freely Moving Monkeys

Article excerpt

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 × 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.

Behavioral tasks that test spatial memory-the delayed alternation (DA) and delayed response (DR) tasks-have been the source of research into the cognitive functions of nonhuman primates for about 80 years (Jacobsen, 1935). Frontal lobectomy and, especially, limited resections of the dorsolateral prefrontal cortex (dlPFC), produce profound deficits in the abilities of monkeys to perform DA and DR tasks (Butters & Pandya, 1969; Goldman & Rosvold, 1970; Gross & Weiskrantz, 1962; Mishkin, 1957). Jacobsen's interpretation of these deficits was that the brain damage impaired spatial memory, but this interpretation has never achieved consensus. For example, Malmo (1942) raised the possibility that the deficit was an attentional disorder. Subsequently, many studies have addressed different aspects of the role of the dlPFC in cognition, and Patricia Goldman-Rakic's work has been at the forefront of these efforts. Without question, her research has been instrumental in providing perspectives that allow the integration of basic research in monkeys with concepts of the normal function of the prefrontal cortex as well as its dysfunction in schizophrenia (e.g., Sereno & Holzman, 1995). The DA and DR tasks have been central to research in monkeys (Goldman & Rosvold, 1970; Levy & Goldman-Rakic, 2000), and GoldmanRakic has continued to champion the view that the dlPFC is an essential component of spatial memory mechanisms, a concept that has become largely synonymous with spatial working memory (Baddeley, 1996).

Despite the robust and deleterious effect of dlPFC damage on DA/DR tasks in monkeys, it is not straightforward to reconcile these deficits with the effect of prefrontal damage in humans. Neurological studies tend to emphasize the loss of cognitive functions, such as the ability to plan (Stuss & Benson, 1986), and many studies show that memory (both spatial and nonspatial) functions tend to remain intact in people with prefrontal damage. There are many reasons for the discrepancies between monkeys and humans, and we find two reasons that are compelling. First, brain damage in humans tends to be unilateral and does not respect anatomical boundaries, whereas experimental lesions in monkeys are usually bilateral and restricted to specific cortical territories. …

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