NeuroRehabilitation An InterdllClplllI8ry Journal

ELSEVIER

NeuroRehabilitation 5 (1995) 161-182

Impact of frontal lobe lesions on rehabilitation and recovery from acute brain injury Paul J. Eslinger*a,b, Lynn M. Grattan C , Laszlo Geder a aDepartment of Medicine

(Division of Neurology) and University Hospital Rehabilitation Center, College of Medicine, Penn State University, The Milton S. Hershey Medical Center, 500 University Drive, Hershey, PA 17033, USA b Department of Behavioral Sciences, College of Medicine, Penn State University, The Milton S. Hershey Medical Center, Hershey, PA 17033, USA C Department of Neurology, University of Maryland, School of Medicine, Baltimore, MD 21201, USA accepted 16 December 1994

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Abstract The frontal lobe has been viewed historically in very different ways, ranging from enigmatic and mystifying to the crucial neural substrate for higher cognition and social behavior. Frontal lobe damage poses a unique and difficult set of challenges to the patient, their family and the neurorehabilitation team. Because of the role of the frontal lobe in adaptation and adjustment, such damage adversely affects a patient's participation in the process and content of rehabilitation. To aid diagnosis and treatment planning, a model of frontal lobe organization is outlined, focusing on the specific cognitive and behavioral symptom clusters associated with superior mesial, inferior mesial, dorsolateral and orbital frontal lesions. A taxonomy of social executive processes is presented for identifying impairments in social behavior and personality, based upon the domains of social self-regulation, social self-awareness, social-sensitivity (empathy), and social-salience. Specific interventions are described that encompass dopamine agonist therapy for blunted affect, mutism and akinesia, cognitive strategies for improving organization and planning deficits, and evolving treatments for social impairments. Keywords:

Frontal lobe; Executive functions; Brain damage; Rehabilitation; Social impairments; Pharmacologic

treatment

1. Historical views of the frontal lobe Although the frontal lobe has long been recognized for its important role in motor planning and

* Corresponding author.

activation, elucidation of the varied and sometimes baffling behavioral impairments that result from damage to this cerebral region has been more difficult. Such impairments were first recognized formally by the reports of Harlow [1,2], who described the consequences of traumatic frontal lobe injury in Phineas Gage, the crowbar case. The most prominent changes in

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Gage after his accident included disinhibition, impulsivity and disregard for rules and nuances of social interaction. These occurred without notable change in language, perceptual, reasoning, motor and sensory abilities. Although the social impairment was dramatic, it was so different from the established notions of neurologic impairment that it was difficult to place within a neurologic or psychologic framework for a long time. The conceptual developments in frontal lobe theory since the time of Harlow have mirrored many of the changing views about brain function over the past 100 years, including localization of function, mass-action equipotentiality and neuronal networks. In addition to the contributions of Harlow and Broca [3] during the 19th century, others argued for a role of the frontal lobe in personality, character, social behavior and emotion, particularly Goltz, Bianchi, Welt, Jastrowitz and Oppenheim (see Benton [4] for detailed discussion). But it was in the first half of the 20th century that a blossoming of scientific and clinical interest in the frontal lobe and behavior emerged. During this period, comprehensive studies were undertaken in nonhuman primates with frontal lobe lesions [5], soldiers recovering from brain injuries [6-8] and neurosurgical patients with cerebral tumors, epilepsy and other brain diseases affecting the frontal lobe [9-12]. By the middle of the 20th century, psychosurgery was introduced and studies of prefrontal leucotomy abounded [13-17]. However, .controversy over the effectiveness and objective evaluation of frontal leucotomy, combined with a growing appreciation for the complex yet subtle functions of the frontal lobe encouraged a more cautious approach in the 1960s. This era emphasized scientific rigor and empirical analysis of behavioral change after frontal lobe lesion [18-23]. The role of the frontal lobe as 'executor of the brain' and mediator of specific cognitive processes began to emerge more clearly as a result of the talents of scientists and clinicians who devoted themselves to neuropsychology and behavioral neurology. The notion of multiple frontal lobe syndromes crystallized, capturing the varied behavioral impairments associated with damage to this region. Frontal lobe

research was further rejuvenated during the 1970s and 1980s by the shift from behaviorism to cognitivism, the growth of computer technology-artificial intelligence theory, and the advances in brain imaging such as MRI, PET and SPECT. These developments revolutionized the dominant modes of scientific inquiry. Within the framework of cognitive neuroscience, it is now possible to empirically consider a broad range of cognitive and social processes mediated by frontal lobe networks, including mental models, symbolic representation, social knowledge domains and the neural bases of adaptation and adjustment [24-30]. 1.1. Contemporary issues As a result of these developments, several of the contemporary frontal lobe issues for behavioral neurology and neuropsychology center around: (a) understanding the organizational networks of the frontal lobe and their relation to specific disease states and specific cognitive-behavioral symptoms; (b) deriving a taxonomy for the personality and social impairments associated with frontal lobe damage; and (c) facilitating the development of neurorehabilitation procedures that have a strong scientific foundation. For these reasons, the article is organized into the following four sections: 1.

2.

3.

4.

Organization of the frontal lobe, where a model of anatomic-functional subdivisions, with their common clinical presentations, is elucidated. Frontal lobe damage and rehabilitation, where the unique challenges posed by patients with frontal lobe damage and the relation of frontal lobe-executive processes to rehabilitation goals are outlined. Social impairments, where a taxonomy for identifying and managing personality and social changes associated with frontal lobe damage is presented. Specific interventions for frontal lobe-executive impairments, where treatment effects of bromocriptine, cognitive rehabilitation strategies and management of social behavior impairments are discussed.

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2. Organization of the frontal lobe The frontal lobe can be divided anatomically into agranular and granular portions. Agranular frontal regions include the primary motor and premotor cortices. Granular frontal regions encompass the multiple facets of prefrontal cortex. Specific regions of the superior mesial frontal lobe, dorsolateral (or lateral) frontal lobe, orbital frontal lobe and inferior mesial frontal lobe can be identified (Fig. 1). A summary of anatomic features is presented in Table 1. These areas are affected to different degrees and in different combinations by a variety of diseases. Some of the more common neurologic diseases affecting the frontal lobe include: • • •

infarction of the anterior cerebral artery and rostral branches of the middle cerebral artery rupture of anterior cerebral and anterior communicating artery aneurysms head injury with and without skull fracture

l

• • • • • •

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tumors AVM multiple sclerosis hydrocephalus degenerative diseases including Pick's disease, Alzheimer's disease and frontal lobe dementia herpes simplex encephalitis.

Clinical presentation of frontal lobe disease is determined by the momentum (e.g. slow growing tumor, sudden onset of CVA), anatomic location (e.g., unilateral vs. bilateral, inferior vs. superior) and cumulative extent (e.g. focal lesion vs. multifocal or diffuse lesions) of pathophysiology. These occur within the neurologic context of a patient's particular pattern of cerebral organization. With the exception of motor, language and select cognitive processes, most frontal lobe functions are not as strongly lateralized as posterior cerebral regions. However, there has been steady progress in establishing a model of frontal lobe organization that is based upon specific sectors with dif-

LATERAL FRONTAL

Fig. 1. Schematic drawing of lateral, mesial and orbital surfaces of the frontal lobe. Regions of specialized functional-clinical significance include the lateral (also referred to as dorsolateraI), superior mesial, inferior mesial and orbital sectors. (Abbreviations: O-occipital lobe, P-parietal lobe, T-temporal lobe, ac-anterior cingulate gyrus, cc-corpus callosum).

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Table 1 Summary of general anatomic features of frontal lobe regions Frontal lobe regions

Brodmann's cytoarchitectonic areas Prominent landmarks

Superior mesial

Inferior mesial

Dorsolateral

Orbital

Motor-lateral premotor

24, 6 (mesial)

25,32,12

8, 9, 10, 11, 43, 46,47

10, 11, 12, 13,14

4, 6 (lateral) 44,45

anterior cingulate gyrus; supplementary motor area

basal forebrain (septal nuclei) (precommissural fornix) (nucleus accumbens) (substantia in nominata) (diagonal band of Broca) subcallosal gyrus posterior gyrus rectus

frontal gyri .inferior .middle .superior frontal pole

gyrus rectus olfactory tracts orbital gyri

central sulcus precentral sulcus precentral gyrus Broca's area (left)

Source: Authors

ferent anatomic and functional characteristics, [30-32]. The advances in identifying organizational features of the frontal lobe has also provided numerous clues and suggestions for managing specific clusters of cognitive, neurologic and social impairments. (Note: Aphasias are covered elsewhere in this issue).

Based upon anatomic, physiological and behavioral data from animal and human studies, we argue that four neurobehavioral sectors of the frontal lobe can be identified. These include the superior mesial region, the inferior mesial region, the dorsolateral region and the orbital region. The specific clinical and cognitive-behavioral im-

Table 2 Prominent neurobehavioral impairments associated with damage to specific frontal lobe regions Frontal lobe regions Superior Mesial

Inferior Mesial

Akinesia Mutism Apathy

Amnesia Confabulations Disinhibition Lack of motivation Inattention Utilization behavior

Source: Authors

Dorsolateral Poor integration and synthesis Disorganized thinking and behavior Perseveration Cognitive rigidity Poor planning Impulsive responding Stimulus-boundedness Lack of empathy Impaired self-regulation left right Left hemispatial neglect Nonfluent aphasias Poor spatial cognition

Orbital Personality change Impulsive actions Poor social judgment Reduced empathy Lack of goal-directed behavior

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R

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L

Superior Mesial

Inferior Mesial

Right Dorsolateral

Left Dorsolateral

Orbital

Fig. 2. CT scans showing lesions to different frontal lobe regions. The superior mesial lesion is shown by contrast study of ischemic CY A. The inferior mesial lesion is a consequence of rupture and clipping of an anterior communicating artery aneurysm. The right dorsolateral lesion is a hemorrhagic CYA, the left dorsolateral lesion an ischemic CY A. The orbital lesion is a meningioma.

pairments that are associated with damage to these regions are summarized in Table 2, with examples of specific lesions to the frontal lobe in Fig. 2. These four regions of the frontal lobe can be summarized as follows. 2.1. Superior mesial frontal region

The superior mesial frontal lobe is defined anatomically by the anterior cingulate gyrus (area 24) and the supplementary motor area-SMA (mesial area 6). These structures are strongly interconnected and also communicate with major motor system structures (including motor cortex as well as basal ganglia and pons), with diverse limbic system structures through connections of the anterior cingulate gyrus and via these latter connections with diencephalon and cortical association areas [33]. Thus, motor, endocrine and autonomic systems are influenced by this region. Bilateral injury to the superior mesial region causes profound akinesia and mutism with complete or near-complete absence of responsiveness and spontaneity. In most instances, patients are

not confused or even aphasic, and may briefly speak or otherwise respond normally. As described later, treatment with a dopamine agonist such as bromocriptine appears to improve the range of affective expression, speech and initiation in these patients. Unilateral lesions cause lesser forms of impairment including apraxias as well as reduced spontaneity, initiation and range of emotional expression. While mutism is somewhat more common after left superior mesial damage, there is usually not strongly lateralized findings. Thus, the superior mesial frontal lobe contributes a prominent activation component to internal states and to behavior, including the expression and possibly the experience of emotion. It is involved in several aspects of intentional behavior, programming of skilled motor acts, self-regulation and flexibility of behavior [33,34]. Diseases that affect this region include infarction of the anterior cerebral artery (sometimes as a complication of anterior communicating artery aneurysm rupture and clipping), parasagittal tumors, closed head injury and hydrocephalus.

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2.2. Inferior mesial frontal region The inferior mesial frontal region refers to structures of the basal forebrain (see Table 1), including the ventral striatum and proximal cortices of the subcallosal gyrus and posterior ventromedial frontal lobe. This region is affected by rupture of anterior communicating artcry aneurysms and orbital frontal tumors, usually in bilateral fashion. The subcortical nuclei and pathways of the basal forebrain are strongly interconnected with the medial temporal lobe, including the hippocampus, as well as other limbic system structures. The posterior ventromedial frontal cortex is considered a paralimbic area which is strongly interconnected with the temporal pole and medial temporal region as well as diencephalic structures. Common effects of damage to this region include amnesia, particularly for temporal-spatial aspccts of recent memory, disinhibition, confabulations, inattentiveness, lack of motivation and in some cases utilization behavior [35-38].

2.3. Dorsolateral frontal lobe region The dorsolateral region encompasses large areas of the prefrontal cortex, including the frontal pole, and mediates higher cognitive processes that are to some degree lateralized to left and right regions. The cognitivc and behavioral systems operating in the dorsolateral region are multimodal and even supramodal in nature, respecting but not limited to a single modality, type of material (e.g. object vs. spatial) or even the immediate environmental circumstances. This region is strongly interconnected with posterior cortical association regions, including the inferior parietal lobule and superior temporal gyrus, that provide highly processed visual, auditory and somatosensory information [39,40]. There are also strong connections with subcortical structures, including the thalamus, hypothalamus, amygdala and septum. The dorsolateral frontal lobe contributes significantly to the converging corticostriate pathways to the head of the caudate nucleus that form functional circuits linked to cognitivc flexibility and the capacity to shift response set [41]. There are also strong connections between the dorsolateral frontal lobe and the orbital frontal lobe,

providing for mediation of internal states and autonomic functions with perceptions and decisions related to external circumstances. The characteristic impairments associated with damage to the dorsolateral frontal region include poor integration and synthesis of information, disorganization in thinking and behavior, perseveration with cognitive rigidity and stimulus boundcdness, concrete-literal thinking, poor planning and impulsive responding, impaired cognitive fluency (such as generation of words and designs), irritajJility and lack of empathy. The left dorsolateral frontal region, by virtue of its proximity to Broca's area and its intrahemispheric connections to the left temporal and parietal regions, has been associated with transcortical motor aphasia and to other executive-cognitive processes that require verbal mediation and verbal regulation of behavior. Damage to the right dorsolateral frontal region, in contrast, has been associated more strongly with spatial cognitive impairments including left hemispatial neglect and spatial disorganization to thought and behavior. Both regions have been associated with disorganized communication [42,43] and learning [44]. Patients with dorsolateral frontal damage are also noted to be very poor in self-monitoring and self-awareness; hence, their ability to recognize the extent of their disability is often quite limited, which is a very strong constraint on participation in the rehabilitation process. Common causes of damage to the dorsolateral and polar frontal regions include stroke and tumor (which are most commonly unilateral), and head injury (which varies along a continuum of unilateral-bilateral damage).

2.4. Orbital frontal region The orbital frontal region is very different from the mesial and dorsolateral regions of the frontal lobe in connectivity and clinical characteristics. Orbital frontal lobe damage without involvement of the basal forebrain region has been associated with significant change in personality and social behavior as well as impulsive actions, lack of sustained goal-directed behavior and significantly reduced empathy [24,45]. This region of the frontal lobe also influences certain autonomic functions

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and somatic states which may play a role in learning and self-regulation [46], and is also connected with limbic system structures, the dorsolateral frontal lobe, the diencephalon and to a lesser extent, posterior cortical association areas. Patients with damage to this region, which can occur with meningiomas, head injury and anterior communicating artery aneurysm rupture and clipping, may recover to the point of having normal measured intelligence, language abilities, learning and short-term memory, structured problem solving and perception. They typically do not show the marked cognitive impairments associated with dorsolateral frontal damage (e.g. perseveration, concrete thinking, disorganization), the akinesia associated with superior mesial damage or the amnesia associated with inferior mesial damage. However, patients with orbital frontal damage develop marked difficulties in adjustment and adaptation, out of proportion to any degree of cognitive or neurologic disability. Orbital frontal impairments are most evident later in the process of recovery and rehabilitation, and particularly when high level judgment of social and other complex situations is required. Interestingly, such patients may appear to be malingering because their neurologic and neuropsychologic exams are normal. In fact a subtle but disabling form of executive impairment is present, particularly in social and other spontaneous or real-world domains that require anticipation of consequences, empathy and decision-making processes. Unlike the other frontal sectors, the orbital frontal lobe has a specialized role in social knowledge and in several aspects of social executive processes that are discussed in section 4. 2.5. Summary

For acquired lesions that involve the superior mesial, inferior mesial, dorsolateral or orbital sectors of the frontal lobe, in isolated or multi-focal fashion, the recognition and diagnosis of executive and self-regulatory impairments can be guided by the current model of anatomic-functional organization of the frontal lobe. Even when the pathophysiology involves several frontal lobe sectors, as in head trauma, it is still likely that discrete elements of localized prefrontal lobe dys-

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function, such as akinesia and mutism, can be identified and targeted for behavioral intervention and treatment, as well as evaluated over the course of recovery and rehabilitation. 3. Frontal lobe damage and rehabilitation

The effects of frontal lobe damage upon recovery and rehabilitation are numerous, and present a formidable challenge to the patient, their family and the neurorehabilitation team. Frontal lobe damage frequently alters the patient's capacity to understand, conceptualize and participate in a rehabilitation program by virtue of its effects on executive control networks of the brain. Such higher cognitive networks mediate initiation, inhibition, sustained responding and shifting of thought and behavior. The content of rehabilitation, therefore, must often address acquired deficits in self-regulation, and the executive control of cognition and social behavior. These frequently represent primary consequences of frontal lobe injury and a primary focus of management and treatment. When motor, sensory, language or memory deficits are present, damage that extends to the prefrontal cortex or its white matter pathways can complicate the process of diagnosis and rehabilitation to a greater extent than non-frontal cerebral lesions. Prefrontal lobe damage directly affects mechanisms underlying human adjustment and adaptation [30] that include coping strategies, compensation, problem-solving, formulation of goals and incorporating new approaches to goal attainment. Damage to the frontal lobe, particularly the orbital region, also carries the prospect that its most profound effects are not evident in the acute or even subacute phases. Rather, the impact of frontal lobe lesion on resumption of many premorbid activities may persist and even worsen over time as the environmental complexity and burden of adjustment and adaptation exceed the patient's capabilities. 3.1. Recovery phases

During the acute recovery phase, it is usually not possible to diagnose and treat all of the patient's frontal lobe-related cognitive and behav-

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ioral impairments. The primary rehabilitation goal at this point is to provide a treatment plan that encourages the patient's cooperation and engagement in the rehabilitation process. Barriers to such participation, directly attributable to frontal lobe damage, can range from behavioral underactivation (e.g. akinesia, mutism) to overactivation (e.g. disinhibition and release of childish, superficial and impulsive responding). In the case of akinesia and mutism, treatment with a dopamine agonist (described in section 5) may be indicated. Conversely, management of disinhibition and impulsive responding requires more environmental manipulations. This includes simplifying and structuring the environment as well as establishing clear routines. Behavioral management programs that minimize the amount of stimulation present, provide consistent and immediate feedback on inappropriate behaviors and identify very specific and concrete goals for patients to focus on and follow are also useful. Although highly desired by therapists, it is often not possible for the frontal lesion patient to learn, conceptualize and remember the various sequence of steps and activities that are required to improve their selfcare and other functional activities. Therefore, it is incumbent upon the therapist to persistently make the component steps of a task explicit and provide direct feedback upon completion of each one. Eventually sequences of action can be taught as component steps are acquired. It is not uncommon for patients with frontal lobe damage to fail to use available information to guide their behavior. Curiously, this may occur even when they are able to verbalize the steps or other guidelines that they should be following, and yet this information does not seem to actually guide their behavior. This is an example of a disconnection between knowing required information and actually utilizing that information to drive and guide behavior; hence, the inability to control and regulate their behavior. Many of these clinical interventions focus on the need to provide structure to patients with frontal lobe damage [47]. Recognition of such impairments by neuropsychologists, behavioral neurologists and neurorehabilitation professionals provides a critical component to program planning and evaluation of progress.

During the early phases of recovery, important treatment goals also include increasing attention, impulse control and depth of information processmg. Common treatment goals during the intermediate phase of rehabilitation include: (1) providing organizational strategies to improve perception, communication, memory, IADL's and problem solving; (2) emphasizing verbal mediation and external cueing during problem solving and other daily tasks; (3) stimulating goal setting activities by the patient; (4) improving self-awareness and self-monitoring of the patient's own behavior; (5) focusing on alternate thinking, perspective-taking and cognitive flexibility skills; and (6) improving social sensitivity and management of strong emotional responses such as anger, aggression and depression. During this phase, it becomes increasingly important to involve the patient's family in evaluation and management of the patient's everyday cognitive and social behaviors, as well as management of any motor or sensory impairments. Table 3 provides a summary of several rehabilitation goals that are common for patients with frontal lobe damage during intermediate and later recovery phases. These represent difficult tasks for patients as multimodal processing with higher cognitive and integrative operations is required. Patients with severe frontal lobe damage may reach few of these goals. To evaluate the relevance of these goals for individual patients, standardized neuropsychological tests are recommended, as they aid in the identification and treatment of executive impairments. Table 4 is a summary of several domains that can be assessed as part of neuropsychological evaluation of frontal lobe processes. For most of these areas, standardized psychometric measures are available and results should be considered along with patient background as well as other clinical and diagnostic information. It is noteworthy that the procedures best established in neuropsychological assessment focus on cognitive aspects of frontal lobe impairments. This reflects both the state of current psychometric development and the complex challenge of evaluating

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Table 3 Relationship of different aspects of the rehabilitation process to executive-frontal lobe processes and their common expressions of impairment Rehabilitation process

Executive processes needed

Common target symptoms in rehabilitation

Engagement and motivation

Initiation Volitional responding Attentional control Self-awareness Self-monitoring

Akinesia Lack of responsiveness Short attention span Lack of insight for treatment Impulsivity

Relationship with Rehabilitation team

Social self-regulation Social self-awareness Social sensitivity Social salience

Lack of responding or impulsivity Lack of insight regarding deficits Disregard for feedback Tactless comments and aggressive behavior Overfriendly or indifferent to therapists

Goal setting

Abstraction Planning-organization Anticipate consequences

Identifies only immediate and concrete goals Cannot set specific steps and subgoals Does not consider gains/losses from actions

Learning

Focussed attention Encoding and rehearsal of information and procedures Organized recall

Distractibility Superficial processing

Transfer/Generalization

Cognitive flexibility Abstraction

Stimulus-bound, perseveration Use of new strategies in only one situation

Adjustment to illness

Cognitive flexibility Social self-awareness Social self-regulation

Views self and goals only in pre-illness terms Unrealistic expectations or goals Lack of control over expressions of fear, anger and depression

Source: Authors

social-interpersonal impairments after frontal lobe damage. 4. Social impairments

The notion that the frontal lobe provides crucial mechanisms for personality and social behavior has been documented in case studies where traumatic brain injury, stroke, aneurysm rupture, tumor and other neurologic diseases affect the frontal lobe. The social disability of these patients is often their most distinctive characteristic as their personality and behavioral problems often produce greater barriers to rehabilitation and functional recovery than other neurologic and cognitive deficits [30,48]. Despite this realization,

Failure to use cues from self and others

---

accumulated knowledge has not resulted in an effective working model for understanding the role of the frontal lobe in personality and social behavior to date. The constraints have been largely methodological, and have produced fragmentation of behavioral concepts and psychological constructs, broad generalizations, and diverse descriptions of social problems that may not refer to the same underlying processes. We have argued that lists of characteristic personality and social difficulties may not be satisfactory as organizing principles for assessment and rehabilitation. There is a need for a working taxonomy or framework for sorting the social sequelae after frontal lobe damage into pathological entities, determining which behavioral processes allow

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Table 4 Neuropsychological testing of cognitive-executive processes Executive processes

Measures

Cognitive flexibility spontaneous reactive

Fluency paradigms Wisconsin card sorting test

Environmental judgments

Cognitive estimation Frequency judgments

Planning

Tower of London/Hanoi Porte us mazes Rey complex figure

Learning/Memory temporal processing

Digit sequence learning Recency judgments

organization

Serial position effects Subjective organization index Sematic clustering

source-context

Time-place judgments of learning

metamemory

Self-judgments

encoding

Levels of processing Release from proactive interference

Discourse organization intentional states

Narratives Test of language competence

Working Memory verbal

Paced auditory serial addition test

visual spatial Attention selective divided

Delayed alteration Delayed responding Visual search Peterson interference task Trails B Dichotic listening

Self-regulation

Self-ordered pacing

Self-monitoring response suppression-conflicting stimuli environmental independence inhibition

Stroop test Utilization behavior tasks Go-no go tasks

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Source: Authors

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clear anatomic correlates, which are primarily psychologic, and how these compare across studies. Towards this end, we propose a heuristic model for social processes mediated by the frontal lobe, which is best operationalized by the concept of the 'social executor.' In current concepts of neuropsychology and behavioral neurology, the brain is viewed as organized by functional systems, through which various components of complex behavioral processes such as memory, language or perception are mediated by parallel and distributed neural networks. The role of the frontal lobes in these functional systems is typically that of the 'executor,' organizing and directing component percepts and processes in time and place toward adaptively meeting the needs and goals of the organism. Therefore, it is plausible that adaptive social behavior may be viewed as a complex functional system for which the frontal lobe operates as an executor. From this perspective, when the frontal lobe is intact, personality and social behavior systems operate in a unique and organized pattern for each individual their personal history, temperament, psychological needs, environment demands and emotional state. Mter frontal lobe damage, personality and social behavior may become fragmented, disorganized and unregulated, resulting in behavior that is inappropriate to the context or emotional state of the individual. The proposed model of social executors encompasses those processes that facilitate or impede the formulation and maintenance of effective, meaningful interpersonal relationships. The social executors may be distinguished from other emotional, interpersonal and reactive processes such as anxiety, depression, mania or low self-esteem by virtue of their close relationship with higher cognitive and executive control processes [49]. Specifically, social executors mediate how emotional and reactive states are expressed; taking into account a person's needs, goals and social cognition (i.e. knowledge related to roles, norms, expectations and what is considered fair and just by one's culture). The way social impairments express themselves, therefore, depends to a large degree upon each patient's unique concatenate of

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characteristics that include both pre-morbid features as well as the specific effects of the neurologic illness (see Fig. 3). The integrity of the social executive system can be evaluated through a taxonomy that includes four specific aspects of social and interpersonal behavior. These are as follows:

4.1. Social self-regulation This refers to the patient's ability to manage the initiation, rate, intensity and duration of their interaction with others. Difficulties with social self-regulation occur along a continuum ranging from apathy to disinhibition. Although these impairments are most evident during the early phases of recovery, they may persist in attenuated forms as lasting features of the patient's personality. Difficulties with social self-regulation are most commonly expressed as reduced initiation and volition in social settings; viscosity or stickiness in social discourse; limited appreciation for interpersonal boundaries; and difficulty inhibiting impulsive responses in social contexts. In the rehabilitation setting, these difficulties most frequently result in social withdrawal or disturbing comments and behavior to other patients and members of the rehabilitation team. 4.2. Social self-awareness This refers to a specialized form of knowledge and insight about one's self in social situations. It involves the accurate perception of one's own emotional states, ability to manage strong emotions, impact of one's behavior on others and general interpersonal effectiveness. Accurate social-self-awareness is crucial to arriving at appropriate social judgments and maintaining positive social relationships over time. Difficulties with social self-awareness have been reported after closed head injury and frontal lobe damage as a result of a stroke [50-52]. Specifically, these patients under or overestimated their social and emotional effectiveness compared to their significant reports of others. In the rehabilitation setting, reduced social self-awareness may lead to a denial of social deficits and reduced motivation for, or responsiveness to, treatment for personality and social problems.

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SOCIAL EXECUTORS

MODERATING VARIABLES

OUTCOME

PremorbkJ State

Personality Traits Family System Social System Occupation-Education Cognitive Capacities Co in Resources & Strate ies

Social Self-Regulation Social and Interpersonal Behaviors

Social Self-Awareness Social Sensitivity Social Salience Characteristics ACQuired from Injurv

Cognitive & Executive Deficits Neuropsychiatric Syndromes (e.g., depression, mania, obsessivecompulsive disorder) Reactive Psychological States (e.g., denial, post-trauma stress disorder

Fig. 3. Summary of a model specifying several of the variables that underlie social and interpersonal impairments after cerebral damage. Four specific types of social executors are identified and defined in the text. Moderating variables represent both premorbid patient characteristics and acquired effects of neurologic injury.

4.3. Social sensitivity

4.4. Social salience

This refers to the ability to understand another person's perspective, point of view or emotional state. This social executor most closely resembles the psychological construction of cognitively-based empathy. Empirical studies have demonstrated that empathy scores are reduced after frontal lobe damage, and decline for different reasons depending upon the specific site of injury [45]. However, the most common basis for reduced empathy after frontal lobe lesion is the patient's difficulty with perspective-taking in unfamiliar, novel or ambiguous social situations. Difficulties with social sensitivity may be indicated by unusually self-centered behavior and insensitivity to others. As a result, patients may become alienated in the rehabilitation setting, and health professionals and family members may feel unappreciated for their efforts and concerns.

This includes a variety of cognitive, autonomic and visceral processes that regulate somatic and emotional states, and impart a sense of meaningfulness to social situations and to specific individuals within the situations. The orbital frontal region may playa prominent role in such processes, as damage to this region has been associated with reduced autonomic responsiveness to social stimuli [46]. Disrupted social salience may also be conceptualized as a deficit in affectively-based empathy or the inability to share the emotional experiences of another. Presumably, these psychologic and autonomic processes influence the individual's level of arousal as well as allocation of attention, interest, and mental and emotional resources in social situations. When all interpersonal and environmental stimuli have similar social salience, they cannot be organized into hier-

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archies of meaningfulness or domains of social relevance. As a result, impaired social salience may limit a patient's ability to learn from positive and negative social experiences in rehabilitation, family and other social settings. Further studies are required to confirm and extend these entities of social impairments commonly encountered after frontal lobe damage. In particular, there is a need to further develop criteria that advance the empirical analysis and treatment of these complex disorders and to establish more clearly their neural or psychological correlates. 5. Specific interventions for frontal lobe-executive impairments

5.1. Bromocriptine treatment The special importance of dopamine as a neurotransmitter of the central nervous system was recognized when its role in the pathogenesis of Parkinson's disease and schizophrenia was confirmed [53,54]. Animal studies further indicated the presence of dopamine terminals in rat and cat cerebral cortex, with dense terminal fields detected in limbic areas (particularly the anterior cingulate and entorhinal cortices) and in two rostral portions of the frontal cortex that are homologous to the prefrontal cortex of primates [55,56]. The significance of the frontal dopaminergic receptor fields is supported by the major role of frontal cortex in the activation and control of cognitive functions [26,27,30,32]. The main site of dopaminergic fibers is the frontal agranular cortex (Brodmann's areas 4, 6 and 24). The primary motor strip and the anterior cingulate cortex possess the densest innervation. Dopaminergic fibers are present in every layer of the agranular areas, but concentrated mainly in layer I and to lesser extent, layers V-VI. Occasional local accumulations can be noted in layers II-III. The dopaminergic innervation of area 9 of the prefrontal cortex is of a lower density and mainly in layers I and V-VI. The most intensively studied ascending dopaminergic projections from the midbrain are the nigro-striatal and mesocorticolimbic pathways [57-60]. The neurons of the mesocorticolimbic

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pathway arise from the central tegmental area and consist of mesoallocortical axons which terminate in the phylogenetically old cortical derivatives (olfactory tubercle, amygdala, septal nuclei and pyriform cortex) and the mesoneocortical pathways terminating in all neocortical areas. The dopaminergic innervation of the neocortex in humans and non-human primates is widespread and has highly differentiated laminar distribution patterns [61,62]. The dopaminergic receptors in the human cerebral neocortex are mainly of the Dl type [63-65], which in animal models playa role in self-stimulation and motivation. The mesoneocortical dopamine system may have a role in cognition [66]. As mentioned earlier, lesions of the superior mesial part of the frontal lobe (anterior cingulate gyrus, supplementary motor area) cause akinesia, mutism and apraxia. Damage to Broca's area and the frontal pole cause other forms of disturbed initiation and motor programming. In focal lesions of the frontal lobe the mesoneocortical pathways are disrupted postsynaptically. In such lesions, postsynaptic dopaminergic agents, like bromocriptine, might be of therapeutic value by improving synaptic activation in the frontal lobe [68]. Recovery from hemispatial neglect in monkeys with unilateral resection of the frontal polysensory association cortex was reported after treatment with bromocriptine [69]. Bromocriptine improved the speaking skills of patients with chronic nonfiuent aphasia and hemispatial neglect due to ischemic injury to the fronto-parietal operculum and the fronto-temporo-parietal area [68,70]. In a preliminary clinical trial, we studied the effect of bromocriptine on the recovery from frontal injury of seven patients. The goal of this study was to determine the effect of bromocriptine on several aspects of frontal lobe-executive impairments, the minimum effective dose of bromocriptine for recovery, and the individual responsiveness of prefrontal (appreciation of social nuances, goal-directed behavior) and mesial frontal lobe signs (affect, mutism and akinesia) to treatment with bromocriptine. Four patients suffered stroke and three had traumatic brain injury. Three patients had solely frontal lobe injury and

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174

four had additional hemispheric damage. The starting dose of bromocriptine was 5 mg p.o. qd for 6 days, followed by 10 mg p.o. qd for 14-22 days, then 15 mg for the rest of the treatment period. The medication was started at the time of admission to the rehabilitation unit. Changes in affect, mutism, appreciation of social nuances, goal directed behavior and akinesia were followed by daily bedside evaluation at morning rounds, and scored as shown in Table 5. During the treatment period, all patients were involved in cognitive, physical, occupational, speech and recreational therapies. Results indicated that every patient showed significant improvement of frontal lobe functions during prolonged treatment with bromocriptine, though individual differences in the therapeutic response to the drug existed. The end-of-treat-

Table 5 Bedside evaluation parameters for frontal lobe functions Affect 1 = Normal 0= Blunt Mutism 4= 3= 2= 1=

o=

Imminent response Hesitation with a latency period less than 30 s Slow response with a latency period of 1-2 min Very slow response with a latency period of 2-4 min Severe apathy, no response to questions

Appreciation of social nuances 3 = Intact 2 = Minimally impaired 1 ~ impaired o= Lack of appreciation Goal directed behavior 3 = Intact 2 = Outlines acceptable goals 1 = inappropriate goals o= Lack of goal directed behavior Akinesia 4 = Complex purposeful voluntary movements 3 ,= Good voluntary movements 2 = Slow voluntary movements 1 ~ Occasional voluntary movements 0= Akinesia Score Range - 0-15 Source: Author

ment improvement was almost identical for patients with single frontal vs. frontal with multiple cerebral injuries. Only one patient of each group failed to reach maximum scores of frontal lobe functions (Table 6). The end-of-treatment improvement of patients with traumatic brain injury was somewhat better than those with stroke. All patients of the trauma group showed maximum posttreatment functional scores, while two patients of the stroke group failed to do so (Table 7). The abnormal affect, mutism and akinesia responded well to bromocriptine, while the appreciation of social nuances and goal-directed behavior was more refractory to treatment. The discontinuation of bromocriptine treatment in one case resulted in a decline of appreciation of social nuances and goal-directed behavior. Restoration of therapy reversed the process (Table 8). In summary, the treatment of mesial frontal and prefrontal brain injures with bromocriptine confirmed the effectiveness of this drug for recovery. The abnormal affect, mutism, and akinesia responded better to bromocriptine, while the appreciation of social nuances and goal-directed behavior was more refractory to treatment. Patients with traumatic injury showed better improvement than those with stroke, most likely because of their younger age group. These data support the therapeutic use of a dopaminergic agent in patients with frontal lobe injury. However, further study with a double-blind, placebocontrolled design is necessary. 5.2. Cognitive rehabilitation strategies

There is increasing literature regarding the remediation and management of cognitive-executive impairments, prompted in part by the significant number of head injury cases where frontal lobe damage is prominent. While several clinical guidelines were offered in section 3 (Frontal lobe damage and rehabilitation), we focus here on three approaches that provide useful examples of remediation and management of cognitive-executive impairments. Specific guidelines for managing social and personality changes are described in the next section.

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Table 6 Improvement of frontal lobe-executive functions during prolonged treatment with bromocriptine Pre-treatment

Patient

Scores

End of treatment

Maximum scores

Mean

Scores

Mean

0.7

15 15 13

14.33

15

14

15

Sole frontal lesion

J.S.

2

o

T.A. S.M.

o

Frontal and multiple brain lesions

M.C. AC. W.J. K.L.

8

15 15 15 11

4.50

2 2

6

Source: Author

Table 7 Summary scores of improvement of frontal lobe-executive functions of patients with stroke and traumatic brain injury during treatment with bromocriptine Patient with

End of treatment

Pre-treatment Scores

Mean

Stroke T.A. S.M. W.J.

o o

2

K.L.

6

Scores 15 13 15 11

2

Maximum scores Mean

13.5

15

15

15

Traumatic brain injury

J.S. M.C. AC.

2 8 2

15 15 15

4

Source: Author

Table 8 The effect of early discontinuation of bromocriptine treatment on the recurrence of frontal lobe symptoms in one patient Frontal lobe symptoms

Affect Mutism Appreciation of social nuances Goal directed behavior Akinesia

Maximum scores

1 4 3 3 4

Bromocriptine treatment patient scores 5 mgq.d. 6 days

10 mg q.d. 14 days

15 mg q.d. 35 days

Discontinued

0 3 1 0 4

0 4

1 4 3 3 4

1 4 I'

'Indicates significant decline during period of discontinued medication. Source: Authors

2

1 4

2' 4

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P.J. Eslinger et al. / NeuroRehabilitation 5 (1995) 161-182

One of the first steps in treatment planning is to inventory the type and severity of cognitiveneuropsychological impairments. This is completed with the combined approaches of objective neuropsychological testing (see Table 4) and astute clinical observation and examination. Neuropsychological testing can disclose what cognitive-executive impairments are present, together

with their severity relative to other cognitive domains such as elementary perception, language, memory, measured intellect and problem-solving. In addition, emphasis must be placed on how cognitive-executive processes go awry, so as to better define the points at which such processes break down, the elements that contribute to the break down, if the patient is aware of these

A

B

c

D EE ffi

ffi

~ ~

~ ~ ~ ~ ~ ~

8 ~ ~ ".

-~ '.

Fig. 4. The Rey (A) and Taylor (B) complex figures were used as stimuli to examine patients' constructional praxis. In standard administration form, the patient copies either figure, using their own organizational approach. In contrast, an experimental approach (C) presented the figure in a step-by-step examiner-directed organizational plan.

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P.l. Eslinger et al. / NeuroRehabilitation 5 (1995) 161-182

c

A

SA Frontal Head Injury 2:22 Copy SrD Score=15

CP Dorsolateral Frontal 2:27 Copy SrD Score=8

erp

D

.; ~ CP Dorsolateral Frontal 3:1 Copy SEa Score=33

:,. )

IV

-- .~~

SA Frontal Head Injury 2:24 Copy SEa Score=34

Fig. 5. Two examples of constructional copy by frontal lesion patients under standard (subject-generated) (STD) and experimental (examiner-directed sequential) (SEQ) conditions. Scores can range from 0-36. Right dorsolateral frontal lesion subjects showed the largest gains in copy (see A-B), where scores improved from the impaired to average range when the organizational strategy was applied. Head Injury subjects with frontal lobe pathology also showed significant improvement from the impaired to average range when the organizational strategy was applied (see CoD). A similar pattern of improvement was also evident for recall of the complex figures. While parietal lesion patients also improved in copy, their recall performance was no different between the two conditions.

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P.l. Eslinger et al. / NeuroRehabilitation 5 (J995) 161-182

factors, and the environmental circumstances that provide effective cues and compensatory strategies [71]. A useful tool to complement objective testing and behavioral observations is the Executive Function Behavioral rating scale [47]. This scale, which the authors describe in detail, provides individualized ratings for three areas that impact a patient's participation in rehabilitation programs and that can be evaluated over the course of recovery. These areas are: selection and execution of cognitive plans (such as knowledge of appropriate steps, high level organization skills), time management (such as creating schedules, revising schedules), and self-regulation (such as control of responding, environmental independence). A second approach is geared toward specific cognitive interventions during the early rehabilitation phases. One of the prominent areas of cognitive difficulty for frontal damage patients is organizing a step-by-step approach to complex tasks. To establish the beneficial effect of providing such patients an organizational strategy, we modified a common neuropsychologic assessment procedure for spatial planning and constructional praxis [72]. Our goal was to compare and contrast subject-generated vs. examiner-directed strategies. The paradigm was copy of the complex figures of Rey and Taylor (see Fig. 4). Standard administration (STD) required subjects to copy one of the figures, with delayed recall after 20 min. Two days later, the examiner-directed administration (SEQ) was presented, in which the subject copied the alternate figure during a series of 17 sequential steps, as shown for the Taylor Fig. in Fig. 4. Thus, the subject constructed the alternate figure one element at a time until completion. For a sample of 25 subjects with frontal lobe lesions, the formats were counterbalanced for type of administration (STD vs. SEQ) and stimulus figure (Rey vs. Taylor), separated by 48 h. The results indicated a significant beneficial effect of the organizational strategy, particularly for patients with right dorsolateral frontal damage. Two examples are provided in Fig. 5 from patients with head injury involving frontal lobe damage (case SA) and focal lesion from tumor

resection in the dorsolateral region (CP). The mean improvement for the frontal lesion sample was from a score of 27.5/36 « 10th percentile) under standard administration format to 32.7/36 (approximately 50th percentile) under sequenced administration format. Although similar benefits were also observed in temporal and parietal lesion samples, the right dorsolateral frontal lesion cases showed the most striking change (improving from a mean score of 13/36 for standard administration to 31/36 for sequenced administration). In addition, their retention of the vi suo spatial information was most improved (with a gain of 11 points), whereas parietal lesion patients showed almost no benefit for retention. Finally, interventions for cognitive executive impairments may prove beneficial even in the chronic phase of recovery. In fact, this phase may be an opportune time to tackle such issues. An example of this approach is provided by Cicerone and Wood [73]. In their case study, the focus of treatment was a planning deficit that persisted 4 years after concussive injury in a young man. Using a paradigm that required planning and executing a series of spatial moves on a Tower of London task (Le. moving different-sized disks from a start to a goal configuration according to certain rules), the investigators focused the patient on using verbal-mediational strategies. That is, the self-instructional program required the subject to verbalize aloud the reason for the anticipated move, with gradual reduction to silent verbalmediation only. The improvement in the patient's performance also led to using a similar approach for more complex problems he faced in everyday activities. Thus, well beyond the period of spontaneous recovery, it appears possible to modify the cognitive strategies patients employ to solve problems.

5.3. Social intervention strategies Disruption of the various social executive processes is not mutually exclusive and neither are the associated intervention strategies. Remediation of social executive dysfunction in the rehabilitation setting is one of the most difficult procedures to implement. It is often labor intensive, dependent upon the patient's language, cog-

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179

Table 9 Treatment guidelines for interpersonal disturbances in patients with frontal lobe damage

1. Recognize interpersonal difficulties as an important domain for assessment and intervention. 2. Identify the source of the social difficulty with a comprehensive clinical evaluation of cognitive, executive, interpersonal, affective and personality processes. Obtain as much information as possible about patient's premorbid personality and interpersonal style. 3. Set realistic goals, preferably multiple short-term goals that members of the rehabilitation team can address and track. 4. Acknowledge that maintenance of acceptable social behavior is a reasonable goal. 5. Start therapy from each patient's level of interpersonal functioning. Bring their attention to any inappropriate behaviors only after a positive therapeutic relationship is developed, with an emphasis on increasing self-awareness. 6. Educate the patient's family to social-emotional alterations after frontal lobe damage. This often involves confirming their observations and concerns regarding the patient's inappropriate behaviors, and offering support for recovery. 7. Support the patient's interpersonal strengths, such as a sense of humor. 8. Reassure the patient that the troublesome behaviors may be modified. 9. Encourage a sense of optimism and hope with the patient, their family and the rehabilitation team. 10. If group therapy is indicated, restrict groups to patients with similar etiology (avoid mixing patients with head injury and stroke). 11. Incorporate as many of the patient's prior interests, activities and goals as possible into their current self-perspective. 12. If litigation is in progress for traumatic injury, encourage rapid resolution to reduce associated stresses. 13. When the frustration and anger of the patient or family members are directed at the treatment team, do not take it personally. This may reflect the helplessness and self-doubt of the patient and/or their family. They may need assistance in more directly and productively expressing these anxieties. 14. Offer the family a 'take-home' plan for how to manage residual social-emotional deficits, and provide outpatient follow-up as needed.

----------------------------------------------------------------Source: Authors

nitive flexibility, perception and memory abilities, and sometimes met with much resistance from the patient. It requires tremendous fluidity, flexibility and creativity by a psychologist or psychiatrist, careful coordination among the rehabilitation team as well as patience and cooperation from family members. Finally, interventions for social executive impairments often require an otherwise effective psychotherapeutic treatment program. General guidelines for psychotherapeutic management of interpersonal problems are summarized in Table 9. With these considerations in mind, we have found the following interventions useful. 1.

Social self-regulation. Interventions in this area revolve around implementing external cueing systems and verbal mediation, the specifics of which will be driven by the patient's particular self-regulatory impairments. If the patient

is apathetic and withdrawn secondary to problems with initiation, providing structured interactions (group or individual) may prove useful. Periods for social exchange should be time limited, focussed and started with low levels of social stimulation. Interpersonal cues may be provided through questions and comments by the caregiver. Since watching a movie or television program or listening to 'talk radio' (e.g. 'talk show,' baseball or football game) may represent a passive form of social interaction, this activity may be incorporated into the rehabilitation program, particularly during the early treatment phases. This activity may also provide the basis for active discussion at a later time. For the more disinhibited patient, the external cues need to revolve around helping them to inhibit their impulsive behaviors. For example, one patient's husband would touch his ear when

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P.l. Eslinger et al. / NeuroRehabilitation 5 (1995) 161-182

her conversation became lengthy, repetitive and tangential. This method successfully limited the length of her verbal communications and increased her satisfaction in social settings. Similar cueing procedures may be effective if specifically tailored to the needs of the patient. The ultimate goal is to enable the patient to self-cue. 2. Social self-awareness. Increasing a patient's social self-knowledge is best done within the context of a psychotherapeutic relationship. This is particularly important since some elements of psychological denial may be operating in conjunction with the executive impairments, thus heightening the patient's resistance to treatment. Feedback and confrontation need to be carefully regulated, taking into account the patient's psychological capacity to accomodate and integrate this information objectively. Once the patient is able to acknowledge and accept a difficulty in social self-awareness, and is interested in improving their social skills, a group treatment modality may be considered. 3. Social sensitivity. The goal of the intervention is to help patients extricate themselves from a set position and consider alternate perspectives in a social situation. At the basic level, exercises that advance the patient's ability for alternative-solution thinking, consequential and means-end thinking are essential. Once those are mastered, increasing the number of references to others and the accuracy of person perception can be addressed. At the advanced level, improving the patient's accuracy in communicating empathic understanding is important. Role-taking activities are often effective in this regard, particularly if the patient is encouraged to reflect upon and evaluate their accuracy and success in their adopted role. Meanwhile, the therapy may be facilitated by encouraging other members of the treatment team, family and patients to directly verbalize their thoughts and feelings to the patient. Hence, the patient can unambiguously be presented with information regarding other perspectives. 4. Social salience. At this time, knowledge regarding the most effective means of treating

this social executive deficit is limited. With some patients, it is useful to make cognitively explicit that which the patient cannot appreciate at an affective level, e.g. encourage them to cognitively process who is most important to them and what emotion is usually associated with certain circumstances. This information may then be used to guide some of their interpersonal behavior. It is noteworthy that this methodology is largely behavioral and has not been demonstrated to significantly alter their actual affective experience of others. In this regard, use of alternative or complementary therapies such as music therapy and pet therapies may hold some promise.

6. Summary The impact of frontal lobe lesions on recovery and participation in rehabilitation programs can be dramatic and constitute exceptional challenges to rehabilitation professionals. Frontal lobe damage affects both the process and content of rehabilitation in a way which is different than for patients with damage to other regions of the brain. This is related to the diversity of cognitive deficits, the disturbed control of behavior, and the social-personality impairments that affect adaptation and adjustment. Certain consequences of frontal lobe damage may not be readily observable in the early phases of recovery, and deficits may in fact emerge or become exacerbated over time, requiring a long-range treatment program. Rehabilitation strategies for behavioral, cognitive and social impairments after frontal lobe damage are clearly identified as domains of scientific and clinical research that are stimulating an increasing range of pharmacologic and neuropsychologic interventions. Although several treatment protocols hold promise, further empirical study is necessary. Acknowledgement We thank Claire Flaherty and Ryan Butler for assistance in data collection. Supported in part by NIH grant R21 RR09415.

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