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Review
. 2024 Mar 1;147(3):794-815.
doi: 10.1093/brain/awad389.

The prefrontal cortex: from monkey to man

Richard Levy  1   2
Affiliations
Review

The prefrontal cortex: from monkey to man

Richard Levy. Brain. .

Abstract

The prefrontal cortex is so important to human beings that, if deprived of it, our behaviour is reduced to action-reactions and automatisms, with no ability to make deliberate decisions. Why does the prefrontal cortex hold such importance in humans? In answer, this review draws on the proximity between humans and other primates, which enables us, through comparative anatomical-functional analysis, to understand the cognitive functions we have in common and specify those that distinguish humans from their closest cousins. First, a focus on the lateral region of the prefrontal cortex illustrates the existence of a continuum between rhesus monkeys (the most studied primates in neuroscience) and humans for most of the major cognitive functions in which this region of the brain plays a central role. This continuum involves the presence of elementary mental operations in the rhesus monkey (e.g. working memory or response inhibition) that are constitutive of 'macro-functions' such as planning, problem-solving and even language production. Second, the human prefrontal cortex has developed dramatically compared to that of other primates. This increase seems to concern the most anterior part (the frontopolar cortex). In humans, the development of the most anterior prefrontal cortex is associated with three major and interrelated cognitive changes: (i) a greater working memory capacity, allowing for greater integration of past experiences and prospective futures; (ii) a greater capacity to link discontinuous or distant data, whether temporal or semantic; and (iii) a greater capacity for abstraction, allowing humans to classify knowledge in different ways, to engage in analogical reasoning or to acquire abstract values that give rise to our beliefs and morals. Together, these new skills enable us, among other things, to develop highly sophisticated social interactions based on language, enabling us to conceive beliefs and moral judgements and to conceptualize, create and extend our vision of our environment beyond what we can physically grasp. Finally, a model of the transition of prefrontal functions between humans and non-human primates concludes this review.

Keywords: behaviour; cognition; frontal lobes; human; primate.

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Conflict of interest statement

The author reports no competing interests.

Figures

Figure 1
Figure 1
The two canonical prefrontal regions and syndromes in humans. PFC = prefrontal cortex.
Figure 2
Figure 2
Phylogeny and comparative anatomy in primates. (A) Phylogeny of the order of the primates. (B) Comparative macroscopic anatomy of the lateral prefrontal cortex in humans and the rhesus monkey. Numbers refer to the cytoarchitectonic maps compiled by Brodmann for humans and Walker for the rhesus monkey.
Figure 3
Figure 3
The ‘Tower of London’, a prototypical planning task. Left: The lateral prefrontal cortex (PFC) is central to planning tasks. Right: An example of the Tower of London (ToL) task. The ToL task consists of transferring three coloured disks between three vertical rods, from an initial position to a pre-specified goal arrangement. Here, the solution comes in five moves. Solving the ToL problem within a limited number of moves requires planning the sequence of actions before starting to move the discs. It relies on more elementary cognitive operations such as those proposed at the bottom.
Figure 4
Figure 4
Examples of working memory and planning tasks performed by the rhesus monkey. (A) The oculomotor delayed response paradigms and their neuronal correlates. In this task, the monkey stares at a central point on a screen. A bright spot then appears in the periphery (at 13°, laterally). The animal must keep its gaze on the central fixation point. The lateral point of light disappears for a few seconds (this is the ‘delay’). At a sound signal, the monkey must make an ocular saccade towards the position where the light point was (it is not present at the time of the ‘response’). At the time of the response, the eye saccade is directed towards the presumed position of the visuo-spatial stimulation, but this stimulus is no longer present. Therefore, action is guided upon the mental trace of the stimulus. (B) The spatial Self-Ordering task. In the Self-Ordering task, the monkey sees a tray with nine wells, three of which contain rewards. The overall objective of the task is to find the three rewards in succession, without ever returning to a well already visited. The monkey starts by making a first choice after one, then a second and a third, each choice being separated by a 10-s ‘delay’, during which the visited well is again covered by a plate. If the animal returns to a visited well or goes to an unrewarded well, the trial stops and the animal does not get the maximum possible reward. The task consists of 30 trials. In each trial, the position of the rewards is reconfigured. The task is considered complete when the monkey is able to perform more than 90% of the trials correctly for five consecutive days. All monkeys were able to achieve this goal, demonstrating planning ability.
Figure 5
Figure 5
Models of anatomical and functional organization of the prefrontal cortex in the rhesus monkey and humans. (A) Anatomical and functional organization (AFO) models of the rhesus monkey. The blue-shaded area indicates the involvement of a given region in spatial cognition; the red-shaded area, an involvement in non-spatial (i.e. object) cognition; the purple-shaded area, a cross- or supra-model involvement; the green-shaded area, an involvement of the area under low working memory demand (e.g. simple maintenance); and the orange-shaded area, under higher working memory demand (e.g. updating information in working memory). (B) The current conception of prefrontal cortex AFO in humans, which comprises two orthogonal dimensions (or gradients). In the posterior lateral prefrontal cortex, one can observe a dorsal-ventral dimension (1) based on the domain of the information being processed (a verbal region in the inferior frontal gyrus, at least in the dominant hemisphere, and a spatial region in the superior frontal gyrus). According to Volle et al., the intermediate region (the middle frontal gyrus) is cross- or supra-modal. The second dimension (2) is a caudal-rostral gradient. Two different but interrelated ideas coexist: this gradient is either based on the level of abstraction or on a combination of the load of information and the time/distance between the stimulus and the response.
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