bechara - brain 2002 - neurology of social cognition

3
Impairments of emotion and social behaviour are often observed after damage to the ventromedial (VM) region of the prefrontal cortex [Brodmann areas (BA) 25, lower 24, 32, and medial aspect of 11, 12 and 10] (Fig. 1). Previously well- adapted individuals become unable to observe social con- ventions and decide advantageously on personal matters. Their ability to express emotion and to experience feelings in appropriate social situations becomes compromised. Studies aimed at understanding the nature of these deficits revealed that impaired ‘judgement and decision-making’ is at the heart of the problem (Bechara et al., 2002). Specifically, evidence suggests that the VM region serves as a link between (i) a certain category of event based on memory records in high order association cortices and (ii) effector structures that produce an emotional response, and also (iii) the substrates of feeling. During judgement/decision-making, category events are brought to ‘working memory’, which includes several processes (Baddeley, 1992). However, maintaining an active representation of memory over a delay period involves the dorsolateral sector of the prefrontal cortex (Fuster, 1997). Effector structures that mediate the emotional response are in the brainstem, whereas neural representations of feelings are thought to involve the insula, surrounding parietal cortices, and the cingulate (Damasio, 1994). Thus judgement/decision-making depends on systems for memory, emotion and feeling. Damage to the systems that impact emotion, feeling and/or memory compromise the ability to make advantageous decisions. The VM region links these systems together, and therefore when damaged there are many manifestations, including alterations of emotional experience and social functioning. However, the cognitive processes that subserve the extremely diverse and flexible social behaviours are complex, and very little is known about their neural substrates. In this issue of Brain, Berthoz and colleagues (Berthoz et al., 2002) have taken the lead in tackling this important challenge. Using functional MRI methodology, they borrowed concepts from social cognition and sought to identify neural systems involved in the processing of transgressions of social norms. In the experiment, subjects were instructed to imagine what they would feel if they were in the situation described in a story incorporating: (i) a normal social situation; (ii) an unintentional violation of social norms, e.g. choking on food during a social dinner; and (iii) an intentional violation of social norms, e.g. purposefully spitting food on a plate during a social dinner. Each story was delivered in: (i) a personal condition, where the events were described as they occurred to the subject; and (ii) an impersonal condition, where the events were described as they occurred to another person. Presumably, there were no differences between the personal and impersonal conditions, so the data from the two conditions were collapsed. The difference in brain activity was between intentional and unintentional violations of social norms on one hand versus normal social situations on the other. Except for slight differences (e.g. BA 21), the activation sites in the intentional and unintentional conditions were by and large very similar. Surprisingly, increased activity was not observed in the VM region, but it was observed bilaterally in a more dorsal region of the medial prefrontal cortex (the medial aspects of BA 6, 8 and 9), and in the temporal poles (BA 38). Both regions overlap with areas engaged in Theory of Mind, i.e. representing the mental states of others. However, these regions are also known to play roles in mechanisms of memory, emotion and decision-making. Hence the question: does Theory of Mind, processing of transgressions of social norms, and other mechanisms of social cognition draw upon neural processes specialized for social information, or do they depend on known mechanisms of memory, emotion, deci- sion-making and other basic functions? Indeed, the dorsal part of the medial prefrontal region as a whole (including the anterior cingulate) forms a bottleneck region where systems concerned with movement, emotion, attention and working memory interact (Damasio, 1994). Patients with bilateral lesions of this region suffer from ‘akinetic mutism’, in which the patient ceases to attend to external stimuli, movements become very limited, and facial expressions are blank reflecting no signs of emotion and feeling (Damasio, 1994; McPherson and Cummings, 2002). Similarly, the temporal pole region overlaps with systems involved in memory retrieval. Patients with such lesions have difficulties retrieving memories of unique entities (Damasio et al., 1996). A similar question can be asked with regard to the observed activity in the lateral aspect of the left orbitofrontal cortex (BAs 47 and 10), which has been shown to respond to Editorial The neurology of social cognition ª Guarantors of Brain 2002 Brain (2002), 125, 1673–1675

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Page 1: Bechara - Brain 2002 - Neurology of Social Cognition

Impairments of emotion and social behaviour are often

observed after damage to the ventromedial (VM) region of

the prefrontal cortex [Brodmann areas (BA) 25, lower 24, 32,

and medial aspect of 11, 12 and 10] (Fig. 1). Previously well-

adapted individuals become unable to observe social con-

ventions and decide advantageously on personal matters.

Their ability to express emotion and to experience feelings in

appropriate social situations becomes compromised. Studies

aimed at understanding the nature of these de®cits revealed

that impaired `judgement and decision-making' is at the heart

of the problem (Bechara et al., 2002). Speci®cally, evidence

suggests that the VM region serves as a link between (i) a

certain category of event based on memory records in high

order association cortices and (ii) effector structures that

produce an emotional response, and also (iii) the substrates of

feeling. During judgement/decision-making, category events

are brought to `working memory', which includes several

processes (Baddeley, 1992). However, maintaining an active

representation of memory over a delay period involves the

dorsolateral sector of the prefrontal cortex (Fuster, 1997).

Effector structures that mediate the emotional response are in

the brainstem, whereas neural representations of feelings are

thought to involve the insula, surrounding parietal cortices,

and the cingulate (Damasio, 1994).

Thus judgement/decision-making depends on systems for

memory, emotion and feeling. Damage to the systems that

impact emotion, feeling and/or memory compromise the

ability to make advantageous decisions. The VM region links

these systems together, and therefore when damaged there are

many manifestations, including alterations of emotional

experience and social functioning. However, the cognitive

processes that subserve the extremely diverse and ¯exible

social behaviours are complex, and very little is known about

their neural substrates. In this issue of Brain, Berthoz and

colleagues (Berthoz et al., 2002) have taken the lead in

tackling this important challenge. Using functional MRI

methodology, they borrowed concepts from social cognition

and sought to identify neural systems involved in the

processing of transgressions of social norms.

In the experiment, subjects were instructed to imagine what

they would feel if they were in the situation described in a

story incorporating: (i) a normal social situation; (ii) an

unintentional violation of social norms, e.g. choking on food

during a social dinner; and (iii) an intentional violation of

social norms, e.g. purposefully spitting food on a plate during

a social dinner. Each story was delivered in: (i) a personal

condition, where the events were described as they occurred

to the subject; and (ii) an impersonal condition, where the

events were described as they occurred to another person.

Presumably, there were no differences between the personal

and impersonal conditions, so the data from the two

conditions were collapsed. The difference in brain activity

was between intentional and unintentional violations of social

norms on one hand versus normal social situations on the

other. Except for slight differences (e.g. BA 21), the

activation sites in the intentional and unintentional conditions

were by and large very similar.

Surprisingly, increased activity was not observed in the

VM region, but it was observed bilaterally in a more dorsal

region of the medial prefrontal cortex (the medial aspects of

BA 6, 8 and 9), and in the temporal poles (BA 38). Both

regions overlap with areas engaged in Theory of Mind, i.e.

representing the mental states of others. However, these

regions are also known to play roles in mechanisms of

memory, emotion and decision-making. Hence the question:

does Theory of Mind, processing of transgressions of social

norms, and other mechanisms of social cognition draw upon

neural processes specialized for social information, or do they

depend on known mechanisms of memory, emotion, deci-

sion-making and other basic functions?

Indeed, the dorsal part of the medial prefrontal region as a

whole (including the anterior cingulate) forms a bottleneck

region where systems concerned with movement, emotion,

attention and working memory interact (Damasio, 1994).

Patients with bilateral lesions of this region suffer from

`akinetic mutism', in which the patient ceases to attend to

external stimuli, movements become very limited, and facial

expressions are blank re¯ecting no signs of emotion and

feeling (Damasio, 1994; McPherson and Cummings, 2002).

Similarly, the temporal pole region overlaps with systems

involved in memory retrieval. Patients with such lesions have

dif®culties retrieving memories of unique entities (Damasio

et al., 1996).

A similar question can be asked with regard to the observed

activity in the lateral aspect of the left orbitofrontal cortex

(BAs 47 and 10), which has been shown to respond to

Editorial

The neurology of social cognition

ã Guarantors of Brain 2002

Brain (2002), 125, 1673±1675

Page 2: Bechara - Brain 2002 - Neurology of Social Cognition

expressions of anger. This region is also implicated in

mechanisms of `impulse control or response inhibition'

(Rahman et al., 2001). There are several mechanisms of

impulse control that can be measured by different tasks and

linked to different prefrontal regions (Bechara et al., 2002).

Some researchers describe these mechanisms of inhibitory

control as `executive functions' or `executive processes' of

working memory. It is important to note that although all

these mechanisms are inter-related, decision-making was

shown as distinct from working memory and mechanisms of

impulse control both cognitively and anatomically (Bechara

et al., 2002).

Despite its known role in emotion and social behaviour

(Adolphs et al., 1994), activity was not observed in the

amygdala, which is consistent with studies showing failure of

amygdala activation under similar conditions, i.e. when the

emotion is triggered by `mental imagery' (Damasio et al.,

2000).

Thus processing transgressions of social norms involve

neural systems implicated in Theory of Mind and in

responding to emotional expressions of others. However,

the same neural systems are involved in working memory,

impulse control and decision-making. Can social cognition be

decomposed into these more basic mechanisms, which are

rooted in neuroscience, in both human and animal studies?

What are the manifestations at the social level if any of these

mechanisms were impaired? Many instances of social

cognition involve `judgement/decision-making' about social

conventions, intentions of others, trust, morals, ethics, and so

on. Is the mechanism for these judgments specialized for

social information and independent of the one described

earlier in VM patients? Or can we tie all these instances to

known mechanisms of decision-making, albeit that judgment

may take different forms, just like working memory has

different modules of (e.g. spatial, object, etc.) and impulse

control has different mechanisms? These are important

questions to consider because introducing functional terms

that are mere descriptions of the social behaviour modelled by

a given task without tying the behaviour to its root

components, or using different languages to describe the

Fig. 1 A BA map with its different areas designated by numbers. Courtesy of Hanna Damasio.

1674 Editorial

Page 3: Bechara - Brain 2002 - Neurology of Social Cognition

same neural system in two different ®elds, would inevitably

lead to confusion and poor understanding of the neurology of

social cognition.

Antoine Bechara

Department of Neurology

University of Iowa College of Medical

Iowa City, USA

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