Interacting Minds--A Biological Basis

Volume 286, Number 5445 Issue of 26 Nov 1999, pp. 1692 - 1695
by Chris D. Frith1* and Uta Frith2
1 Wellcome Department of Cognitive Neurology, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK.
2 Institute of Cognitive Neuroscience and Department of Psychology, University College London, 17 Queen Square, London, WC1N 3AR, UK.

The following has been edited by John Schmidt for the students in the Neurobiology course he teaches. See the original article in Science for the full article. For over 100 years the work of philosophers such as Brentano has been the center of efforts to keep the mind walled off from the brain. This review article by Chris Frith and Uta Frith gives a good description of how scientists are starting to get a handle on some of the very special cognitive capacities that we are so proud of as humans.

Abstract
The ability to "mentalize," that is to understand and manipulate other people's behavior in terms of their mental states, is a major ingredient in successful social interactions. A rudimentary form of this ability may be seen in great apes, but in humans it is developed to a high level. Specific impairments of mentalizing in both developmental and acquired disorders suggest that this ability depends on a dedicated and circumscribed brain system. Functional imaging studies implicate medial prefrontal cortex and posterior superior temporal sulcus (STS) as components of this system. Clues to the specific function of these components in mentalizing come from single cell recording studies: STS is concerned with representing the actions of others through the detection of biological motion; medial prefrontal regions are concerned with explicit representation of states of the self. These observations suggest that the ability to mentalize has evolved from a system for representing actions.
The Friths  cite  Dan Dennett as for his work concerning the awareness that people have of the beliefs and desires of other people..... the "intentional stance" (2).The Firths like the term "mentalizing" (3). Mentalizing allows us to compute what another person will do on the basis of a false belief ( Fig. 1). The Firths point out that in terms of the limitations of experimental psychology, to predict what a person will do on the basis of a true belief is not as stringent a test, since for a true belief the belief coincides with reality, and it is hard to tell whether the action is governed by a person's deep and unconscious knowledge of the world or a particular conscious episode of factual knowledge use. 
Figure 1. The Sally-Anne task. The child is shown the scenario illustrated, which can be enacted by puppets or real people. At the end the child is asked, "Where will Sally look for her ball?" To answer this question the child must realize that Sally has not seen the ball being moved and, therefore, that Sally falsely believes that the ball is still in the basket (17). [Artist, Axel Scheffler.]

 

The Firths seem interested in the idea that only humans can "mentalize".They say that "There is as yet no unequivocal evidence from laboratory-based tasks that chimpanzees or other great apes can make use of intentional deception (9)". However, after having read the descriptions of chimp behavior provided by  Savage-Rumbaugh, I find it hard to play the game of trying to construct artificial cognitive barriers between humans and other apes. These observations suggest that monkeys are not capable of attributing mental states to others and that apes, which may be able to make such attributions, have a primitive form of the ability at the very limits of their cognitive skills.

The Firths breifly review what is known about the normal development of the ability to attribute mental states to others (10). "By age four, deliberatedeception is commonplace and can easily be demonstrated in laboratory-based tasks (11). By 18 months, infants show clear evidenceof understanding pretence, an ability that requires not just the representation of an event, but of an agent's informational relation to the event (12). At the same age, children can imitate and complete an action that they have seen an adult attempt, but fail to finish (13). During the first year of life infants can orient toward another person's focus of attention and can point out objects of interest. However, whether such behavior requires mentalizing remains controversial (14)."

The Firths review situations where the normal development of mentalizing is compromised such as in children diagnosed with autism (15). "In infancy, these children are remarkable by not appearing to orient toward other people's focus of attention, by not showing or pointing out things, and by not engaging in pretend play (16). As they get older, many individuals with the diagnosis of autism remain unable to understand the concept of a false belief. In a simple experiment (see Fig. 1),a child watches two actors and observes the transfer of a ball from one hiding place to another. Most normal 4-year-olds recognizethat Sally, who has not seen Anne transfer the ball, must thinkthat the ball is still in its original place. She has a false belief that causes her to look for the ball in the original place. Most children with autism even up to their teens say that Sally will look for the ball where it really is, failing to take into account her false belief (17). The developmental consequences of mentalizing failure are severe and manifest themselves in a lack of social insight and impaired communication."

The Firths describe other tests of cognition that indicate that the ability to attribute mental states is largely independent of other abilities. "Cases have been described where individuals with autism have achieved tertiary levels of education but still make errors on tasks requiring mentalizing (18). More important, dissociations can be seen even within the domain of social intelligence. Thus autistic children can use sabotage to prevent another person from attaining a goal, demonstrating their understanding of simple social situations, but they cannot use deception for this purpose (see Fig. 2). They can use instrumental communicative gestures ("come here") to affect another's behavior, but not expressive gestures ("well done") to affect another's mental state (20). They can feel the basic pleasure in mastering a task, but not pride, an emotion that requires taking into account other people's expectations (21)." 

Figure 2. Deception and sabotage. Children participated in a game where he or she had to prevent a rival (enacted by the experimenter with the aid of puppets) from obtaining a reward, which was kept in a box. In the sabotage condition this could be achieved by locking the box. In the deception condition this could be achieved by claiming (untruthfully) that the box was locked (19).

The Firths address the issue of if there is "a brain system dedicated to the representation of mental states, analogous to those systems already identified for spatial navigation (27) or face recognition (28). It has become possible to try to localize particular regions of the brain that are important for specific cognitive tasks by using functional brain imaging."

The Firths list some of the studies in the literature in which "volunteers have been asked to monitor and report their own mental states (in circumstances in which these states are not simply a reflection of external reality). The reported states have included pain (29), emotions aroused by pictures (30), spontaneous thoughts(31), actions (32), and tickling (33).However, in spite of the wide variation in the nature of the statesreported on, activity was observed in all these studies in medialfrontal cortex, or, more precisely, along the border between rostralanterior cingulate cortex and medial prefrontal cortex (the paracingulatesulcus, see Fig. 3A)." 

Figure 3. (A) Medial frontal regions associated with mentalizing. An outline of the medial surface of the human brain is shown in Talairach space with location of activity in three experiments of mentalizing [square, circle (31), triangle (32)]. Arrows indicate the location of peak activity from the studies mentioned in the text in which subjects reported on their mental states [pain (26), emotion (27), thoughts (28), action (29), and tickling (30)]. (B) Regions in superior temporal sulcus associated with mentalizing. An outline of the lateral surface of the right hemisphere of the human brain is shown in Talairach space with location of activity in two studies of mentalizing [square (31), triangle (32)]. Arrows indicate the location of peak activity from two studies of biological motion (37). Similar activations in the left hemisphere were also observed in the majority of these studies. The location V5/MT responds to motion in general, both biological and nonbiological (37).

 

The Friths then get to data that are now being collected that are directly relevant to "mentalizing". "To date there are very few brain imaging studies in which volunteers have been asked to report on the mental states of others.In the two earliest positron emission tomography (PET) studies(34), activity was observed in medial prefrontal cortex. This observation was confirmed in a recent functional magnetic resonance imaging (fMRI) study in which volunteers had to make inferences about the mental states of characters in stories or nonverbal cartoons (35). Activity associated with mentalizing was again observed in medial prefrontal cortex. Both forms of presentation also elicited activity in the region of the temporo-parietal junction, and in lateral inferior frontal cortex."

"Although preliminary, these results suggest that a brain system dedicated to mentalizing can be localized. Simple localization, however, is not enough. We also need to know something about the functions of the different areas comprising the system. The interpretation of results from human brain imaging studies has depended critically on information gained from single-cell studies in nonhuman primates. Of necessity, such information is not available for studies ofmentalizing. We do not believe, however, that mentalizing abilitiesarose in humans de novo. Nature is a tinkerer and not an inventor(36). New abilities are adapted from preexisting abilities. Likely preexisting abilities that are relevant to mentalizing include (i) the ability to distinguish between animate and inanimate entities, (ii) the ability to share attention by following the gaze of another agent (14), (iii) the ability to represent goal-directed actions (37), and (iv) the ability to distinguish between actions of the self and of others (38)."

The Friths conclude their review with citations to experimental work on monkeys that deals with electrophysiological recordings of the activity of "cells with properties relevant to these abilities [that] have already been found in a number of brain regions." The naturalization of human mentality is well on its way. Go here to return to the general discussion of memory and intentionality. Go here for some details on what happens in the brain when we learn something new like how to "mentalize".

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Volume 286, Number 5445 Issue of 26 Nov 1999, pp. 1692 - 1695
Copyright © 1999 by the American Association for the Advancement of Science.