Perseveration, inhibition and the prefrontal cortex: a new look

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Abstract

Perseverative actions are often the result of inhibitory problems; however, inhibitory problems do not always lead to perseverative actions. Some problems of inhibition have been attributed to immaturity of, or severe damage to, the prefrontal cortex. Research in this area has generally failed both to take into account species differences in prefrontal function that lead to different perseverative errors and to distinguish between perseverative errors that arise from a failure to inhibit salient emotions or motivational drives and errors that arise from an inability to engage in conceptual change. Recent studies on humans, chimpanzees, rhesus macaques, Japanese macaques, cotton-top tamarins and marmosets support this notion.

Introduction

The act of perseveration — that is, the act of repeatedly producing a particular action or thought — often represents the consequence of a particular cognitive problem, one that is related to inhibition. To prevent perseverative actions, an inhibitory mechanism is required, one that is capable of rejecting some alternatives while favoring others. This mechanism may involve activation of the prefrontal cortex 1•, 2, 3•, 4, 5. In this review, I take a new look at the relationship between perseveration, inhibition and the prefrontal cortex. Previous work on this problem has generally been isolated from two relevant areas, evolutionary biology and human cognitive development [6]. These areas are critical, however, for they help understand how and why particular cognitive mechanisms evolved in humans, the extent to which any particular mechanism is unique or shared with other species, and how systems of knowledge develop, constrained by the underlying neural machinery 6•, 7, 8.

Section snippets

Affective and paradigmatic perseveration

Damasio [9] has raised the important point that rationality depends on a significant infusion of emotion. In the absence of a mechanism that ties decisions to emotions, we are destined to act irrationally. Under certain conditions, however, our emotions get in the way of our reasoning, causing us to make errors. The problem, in some of these cases, is that we fail to inhibit our emotions and motivations, allowing them to rule over reason. When this happens, we may perseverate, making the same

A classic test

When infants less than 7–9 months of age are rewarded for retrieving a toy from a covered well, they continue to return to this well even when they have seen the toy moved to another spot [2]. Infants at this age will also reach straight ahead for a toy trapped within a Plexiglas box, even though their access is blocked by a solid wall, and the opening is located on another side. Older infants find the opening, even if they initially bang into the transparent front wall. Adult rhesus monkeys (

Affective perseveration

To determine whether affective perseveration underlies all problem-solving difficulties for tamarins, or whether it is task specific, we presented them with a means–end task that tapped into their conceptual abilities. Having solved the means–end problem, we then examined whether they could override a significant motivational challenge [27]. The task involved pulling a piece of cloth (means) to gain access to a piece of food (end). In one set of conditions (‘On’), the food was either on or off

Paradigmatic perseveration

Some tasks, such as delayed non-matching to sample, simply require holding information in working memory, and do not involve inhibition. Other problems involve inhibition, but not working memory (e.g. the means-end cloth test). Finally, some tasks, such as delayed matching to sample, involve inhibition and working memory. Sometimes, however, it is not clear whether a deficit is attributable to a problem with working memory, as opposed to a problem of paradigmatic perseveration. This is perhaps

Conclusions

Organisms are constantly challenged by problems. Problem solving requires a capacity to select among alternative solutions. To facilitate this process, individuals must tap their emotions, but not be overwhelmed by them. They must also engage a process of conceptual change when the existing data are no longer accounted for by the current theory. Inhibition represents a critical mechanism in this process. Cognitive differences between species are probably a function of the effectiveness with

Acknowledgements

For funding, I thank the National Science Foundation (SB29357976). Support for the tamarin colony comes from the New England Primate Research Center (P51RR00168-37) and Harvard University. For comments on the manuscript, I thank Adele Diamond and Jerome Kagan.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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