He first denoted the variety and complexity of behavioral deficits. Despite certain shared features, the panel of behavioral changes observable after brain lesions thus remains difficult to explain; despite numerous studies in the field over the last decades, a unified, widely accepted model is still lacking. Second, behavioral changes are generally difficult to quantify by standard testing. They are not always evident – and can be overlooked due to well-preserved performance on routine examination. Moreover, behavioral deficits evolve (acute vs. chronic stages), can fluctuate under certain circumstances, and may be contained in the examination room (e.g., due to external control). Finally, any occurring changes must be evaluated against the background of pre-morbid personality traits “rather than in reference to any set of absolute behavioral standards” [4].
Behavioral impairments have been associated with lesions to cortical and sub-cortical structures across a wide array of etiologies, including trauma, tumors, surgical interventions (e.g., lobectomy, lobotomy), strokes, infections (e.g., syphilitic), and dementia. Striking behavioral disorders are associated with the broad, yet somewhat poorly defined concept that has been named the “frontal syndrome” [5]. Typically, despite behavioral deficits, patients with a “frontal syndrome” can perform quite well on classical cognitive tasks. In this chapter, we shall outline how, over the past 150 years, behavioral measurements have been developing hand-in-hand with attempts to unravel the mysteries of the frontal lobe. Of note, we thus intentionally focus on semiology consecutive to frontal lobe damage to discuss the introduction of behavioral assessment in neurological patients. Overall, we shall span 3 main themes by introducing (1) the first case reports based on thorough clinical descriptions, dating back to the 19th century. We then examine (2) the emergence of checklist questionnaires and their application to large cohorts of individuals starting after World War II. Finally, we outline (3) how, over the last 3 decades, the pace has significantly accelerated in the pursuit of defining and measuring the fine-grained processes underlying behavioral functioning, as well as the development of new and more complex measures, along with the emergence of the social cognition concept.
From Descriptive Single Case Reports to First Neuroanatomical Correlates
The original case of Phineas Gage, a 25-year-old railroad foreman who was caught in a dramatic explosion that resulted in a 3 cm-thick tamping iron penetrating his left cheek, skull, and brain, remains the classic introduction to the field of behavioral disorders [2, 3]. Gage survived and recovered without any motor or cognitive impairment. However, “he was no longer Gage,” according to his friends [2]. Formerly, a responsible and socially well-adapted individual, he became irreverent and capricious, could not hold a job and died 12 years later under the custody of his family. Harlow published a very comprehensive description of the behavioral changes occurring after Gage’s accident, which included a several-year-long follow-up of the patient and testimony of relatives and friends [2]. He also presumed that these behavioral modifications were associated with lesions to a particular region of the frontal cortex, making it one of the earliest correlations between behavioral disorders and neuroanatomy.
In addition to medical records, behavioral changes have occasionally become the object of public perception through artistic acknowledgment and penal proceedings. Contemporary to Phineas Gage, Eadweard Muybridge, a bookseller established in San Francisco, survived a stagecoach accident in 1860 [6]. Again, this patient recovered physically and intellectually but his personality transformed dramatically. He changed the spelling of his name dozens of times and was even charged with the murder of a man suspected of having an affair with his wife. Yet, this lesion triggered a new artistic expression and re-oriented his career: He became a pioneering photographer and developed the “zoopraxiscope,” a precursor of motion pictures. Based on visual symptoms and the loss of smell and taste, Eadweard Muybridge’s brain lesion is assumed to have occurred in the orbitofrontal cortex.
These 2 case reports of trauma established the relationship between lesions to a specific brain area and acquired behavioral deficits that spared intellectual abilities. A few decades later and with the development of neurosurgical procedures, neuroanatomical correlates became accessible to more specific investigation and further underscored the relevance of behavior assessment. One of the sessions at the 2nd International Neurological Congress in London (1935) was thus dedicated to the functions of the frontal lobe [7], and included the well-documented follow-up of patient Joe A., the first bilateral frontal lobectomy case with long survival [8]. Intellectual performance in this patient was assessed using psychometric testing, whereas behavioral status remained at the descriptive level, relying (as for almost all cases of that era) mainly on the neurologist’s observations and heteroanamnesis. Following the resection, Joe A. became logorrheic, self-absorbed, puerile and distractible, with perseverations and sudden mood changes. Whilst Brickner showed severe deterioration in Joe A.’s behavior after surgery, Hebb and Penfield reported a 27-year-old patient who improved after partial bilateral frontal lobectomy [9, 10]. Following a traumatic brain injury to the frontal poles at the age of 16 years, K. M. suffered from severe epileptic seizures. During interictal states, he was described as “childish, violent, stubborn and destructive” by his relatives and the whole neighborhood. After operation, he became “normal in every way” [9]. The 6-year follow-up showed that he had been independent in his daily life activities and successful in finding jobs since his discharge from the army. Although he frequently changed jobs, he was able to save for the future. Here, K. M.’s post-surgical behavioral improvement was evaluated through information given by his parents and his brother, as well as through the “independent testimony of 3 residents of the village,” namely a taxi driver, a storekeeper, and a waitress.
Two decades later, Luria et al. [11] went a step further and published a seminal detailed experimental analysis about the impairment in behavioral regulation after the removal of part of a left frontal meningioma. Patient Zav underwent a full test battery addressing different modalities (verbal, non-verbal, symbolic instructions) and assessing various levels of behavioral regulation (apprehension of instructions, evaluation of errors). This study also introduced the innovative concept of “orienting reaction,” that is, an autonomic signal based on previously registered feedbacks produced by the outcomes of actions, which is assumed to be disturbed in patient Zav. The recording of vascular and galvanic skin responses (GSR) indeed showed the absence of activation during tasks and reinforced the hypothesis of a lack of error utilization underlying behavioral regulation and decision-making impairments. As described below, this pioneering approach was made popular 30 years later with the “somatic marker hypothesis” [12, 13].
Advances in neurosurgery and the London congress also led to the rise of lobotomy. Initiated by Swiss psychiatrist Gottlieb Burckhardt as early as 1888 and later extensively implemented by Egas Moniz and Walter Freeman, the controversial “psychosurgery” consisted mainly of frontal lobotomy, that is, the (minimal-to-extensive) deletion of the fibers connecting the frontal areas with the rest of the brain, to decrease symptoms of mental illness [14, 15]. Post-surgery
