the relatives’ ability to cope with the subject’s behavior). Finally, the examiner filled in the Neurobehavioral Rating Scale, an inventory sensitive to aberrant behavior [21]. Overall, questionnaires were quantitative, interrogated patients and relatives, and therefore led to more systematic assessments. This set-up allowed the evaluation of behavioral deficits on large cohorts of individuals, as well as conducting follow-up investigations to shed light on the long-term outcome of patients.
1980–1990s, Innovations and Emergence of Social Cognition
A key factor in the 1980s is a change of perspective: it was realized that certain symptoms occurring in real life cannot be pinpointed with classical “laboratory” tests nor in the examination room. In other words, formal neurological/neuropsychological assessments can (1) miss certain behavioral impairments, and can (2) exert external constraints and conditions that differ sufficiently from daily life as to impact test results. This notion introduces the concept of “ecological validity.” Moreover, coming back to our neurological definition of behavior, the last decade of the 20th century has seen the emergence of a specific field dedicated to the study of cognitive processes required in social behavior, referred to as “social cognition.”
This new perspective is illustrated, for example, by the characterization of “imitation and utilization behavior,” a disturbed response to external stimuli which belongs to the “dependency syndrome” [22]. Lhermitte [23] thus established fairly unusual and innovative methodology to study the presence of this phenomenon in patients with cerebral lesions. In stark contrast to classical examination settings, the examiner remains neutral and indifferent to the patient during the whole examination, and then makes a series of gestures, such as body, symbolic and gymnastic gestures, gestures involving objects, and pronounces short sentences, sings, writes and draws. The patient is told not to copy the examiner, who then repeats his sequence of gestures. The patient’s behavior is observed and evaluated. To better understand the impact of the environment on the dependency syndrome, the study went a step further by taking the patients outside the examination room, filming and photographing all steps [23]. The patient was thus put in situations of everyday life (e.g., doctor’s office, garden, gift shop). Although creative, less structured and probably more ecological, this methodology obviously poses ethical issues with respect to the patient and his family.
The discrepancy between good performance in classical tests in the examination room and successive failures in daily life observed in some patients has led scientists to address those mechanisms which are impaired and cause emotional and behavioral changes. Before the availability of dedicated tests, such investigations made use of personality trait inventories [5, 24] and tools from developmental psychology [5, 25, 26]. In these studies, tasks targeted different components of social behavior, namely self vs. others perspective, social knowledge, and moral reasoning. All of them consisted of standardized verbal presentations of moral dilemmas or social situations that required verbal responses. Inspired by these studies, new paradigms have been designed, in particular to evaluate “pseudopsychopathy” [16], later called “acquired sociopathy” [13]. This term refers to individuals developing high levels of aggression and antisocial behavior with reduced empathy and guilt after acquired lesion to the orbitofrontal cortex. This is, for example, the case of patient EVR who underwent a resection of a large orbitofrontal meningioma compressing both frontal lobes [5]. Previously, a sensible and successful fellow, EVR changed dramatically after surgery; he separated from his family, became unable to hold a job and made unreasonable decisions. The integrity of his knowledge of normal patterns of social behavior and its application were measured. Despite his ability to reason appropriately about moral problems that were presented to him, and a performance in social cognition tasks that lay in the range of (or even excelled) healthy controls, he was unable to apply such reasoning in real-life situations [5, 13]. Of note, despite their social nature, these tasks do not seem to sufficiently match real-life situations for several reasons (e.g., verbal tasks vs. multimodal inputs, observer vs. protagonist in real life), thus suggesting that a decision-making disorder lies at the core of the impairment. The social knowledge and access to it was preserved, yet EVR failed to apply the appropriate choice-making strategy. These observations were further developed in the “somatic marker hypothesis” [13], which denotes the covert influence of a somatic process on decision-making, as suggested by Luria thirty years before [11]. To validate this hypothesis, “reversal learning” tasks were developed, such as the Iowa Gambling Task that mimics real-life decisions by including uncertainty, rewards, and penalties [12]. The subjects (players) are presented with 4 decks of cards, a loan of a certain amount of facsimile U.S. dollar bills and asked to play. They are also instructed to lose the least amount of money and win the most. There are 2 advantageous and 2 disadvantageous decks, the latter leading to an overall loss. Simultaneously, physiological data such as GSR are recorded. The reference study showed first that healthy controls chose advantageous decks whereas patients with prefrontal lesions did not [12]. Second, healthy controls generated anticipatory GSR (i.e., autonomic response) before being explicitly aware of a risky choice, whilst patients did not, even with knowledge of their risky choice.
GSR measures were utilized in combination with other modality tasks, for example, by Blair and Cipolotti [27]. Patient JS, who developed acquired sociopathy following a trauma that lesioned the orbitofrontal cortex bilaterally, has been assessed in much detail with a series of twelve tests embracing 3 types of processing, namely (1) reversal learning, (2) expression recognition and emotional responding, and (3) social cognition. Together with simultaneous GSR recordings, salient facial and environmental stimuli as well as visual and auditory inputs were applied during expression and emotional tasks. Moreover, different levels of social cognition were investigated. These measures included emotion attribution, theory of mind (i.e., the ability to attribute mental states to oneself and to others), moral/conventional distinction, and social situation tasks. JS performed well on the reversal learning tasks but was severely impaired on expression recognition and emotional responding tasks despite intact face processing. Autonomic responses (i.e., GSR) were preserved for auditory but not for visual stimuli. Finally, although showing no impairment on the theory of mind task, he failed almost all the social cognition tasks. JS’s results were significantly different from those of a dysexecutive patient without aberrant behavior as well as from a group of individuals with developmental psychopathy. This study therefore showed that autonomic measures can contribute, but are not sufficient to disentangle the complex processes underlying acquired sociopathy. More generally, it revealed that the more various and “composite” the measures are, the broader the resulting behavioral spectrum is.
Conclusions
We have discussed the introduction of assessment of emotions and behavior in neurological patients along with the understanding of frontal lobe functions. From observational and descriptive reports, behavioral