Archives of Clinical Neuropsychology, Vol. 12, No. 2, pp.

173-188, 1997
Copyright 0 1997 National Academy of Neuropsychology
Pergamon Printed in the USA. All rights reserved
0887-6177/97 $17.00 + .oO

PI1 SOsS7-6177(96)00022-4

Grand Rounds

Disturbance of Social Cognition

After Traumatic Orbitofrontal Brain Injury

Keith D. Cicerone

1%johnson Rehabilitation lnsitute and

New Jersey Neuroscience Institute, JFK Medical Center, Edison, NJ, USA

Lawrence N. Tanenbaum

New Jersey Neuroscience Institute, JFK Medical Center, Edison, NJ, USA

A patient with traumatic orbitomedial frontal lobe damage demonstrated good neurocognitive
recovery but a lasting, profound disturbance of emotional regulation and social cognition. Initial
neuiopsychological findings included a complete anosmia, mildly reduced fluency and disturbed
motor regulation. The impairments offluency and motor regulation resolved, andformal measures of
“frontal 1obe”finctioning were generally intact. However; she remained impaired on tasks requiring
the interpretation of social situations, whiih mirrored her impairment in real life functioning. This
disturbance in social cognition appeared related to di#kulty appreciating and integrating the
relatively subtle social and emotional cues requiredfor the appropriate interpretation of events. The
patient’s presentation represents an intermediate position between patients with profound neurobe-
havioral deficits and patients with impaired real-life social cognition despite intact neuropsycholog-
ical performance following orbitofrontal damage. Variations in the orbitofrontal behavioral syn-
drome may be related to extent of lesion, time post injury and the course of recovery in dtxerent
patients. 0 1997 National Academy of Neuropsychology

The disturbance of higher executive functioning due to acquired brain injury continues to
represent a significant challenge in neuropsychology. Disorders of executive functioning may
affect the ability to anticipate the effects of our actions, appreciate alternative perspectives,
and to recognize other people’s reactions to our behavior and modify our actions accordingly.
Disruption of these processes may not be apparent when the elementary bases of neurocog-

The authors would like to acknowledge Joseph T. Giacino, Ph.D. for his discussions concerning the case. Peter
Rutan, Ed.D. and David Tupper, Ph.D. provided helpful comments and assistance during preparation of the
manuscript.
Address correspondence to: Keith D. Cicerone, Ph.D., JFK-Johnson Rehabiliation Institute, 2048 Oak Tree
Road, Edison, NJ, 08820.

173
Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717
by guest
on 08 August 2018
 174 K. D. Cicerone and L. N. Tanenbaum

nition are examined; indeed, neuropsychological functioning may appear to be entirely intact
when examined in isolation or in highly structured or familiar interactions (Bigler, 1988;
Hebb, 1945). In contrast, marked disturbances may be apparent in the ability to function
effectively and appropriately in the rich, complex matrix of interpersonal and social rela-
tionships.
Recent studies have emphasized the anatomic subdivision of the prefrontal lobes in
relation to specific neuropsychological abilities and impairments (Barbas & Pandya, 1991;
Mesulam, 1986). Damage to the orbitofrontal cortex has been related to disturbances of
complex social and emotional behavior in humans (Lhermitte, 1986; Luria, 1980). The
orbitofrontal cortex (also referred to a ventromesial frontal cortex) is considered by Mesulam
(1986) to be part of paralimbic cortex, along with the cingulate cortex and paraolfactory
region, which receives information from polysensory association areas via the dorsolateral
frontal lobe, and also has extensive reciprocal connections with the anterior temporal, medial
temporal and limbic regions (Mesulam, 1986). Animals with orbitofrontal lesions demon-
strate an alteration in emotional reactivity and regulation (Butter & Snyder, 1972), which may
result in marked disruption of socially appropriate responding and social adaptation (Kling
& Steklis, 1976; Mesulam, 1986).
Malloy, Bihrle, and Duffy (1993) identified a number of well-described clinical features
which they considered to constitute the orbitomedial frontal syndrome. These included
anosmia, amnesia with confabulation, deficits in go-no/go tasks, personality change (both
aspontaneity and disinhibition), intrusive errors, and perseveration. These findings prompted
Malloy et al. (1993) to suggest that the clinician now had a number of tools at his disposal
to document the “relatively subtle (but profoundly disabling) deficits” after orbitomedial
frontal injury. Despite these findings, there remain patients for whom formal neuropsycho-
logical testing does not reveal deficits, yet the patient may be profoundly impaired in real life
in the area of complex social behavior. Eslinger and Damasio (1985) provided a seminal
description of a patient, EVR, who had resection of an orbitofrontal meningioma involving
the ventromesial frontal cortices bilaterally. The patient did not exhibit deficits on extensive
neuropsychological testing, including tests considered sensitive to frontal lobe dysfunction,
but he exhibited a marked deterioration of interpersonal functioning and marked impairment
of judgement and decision making as required in everyday functioning.
In these cases, the fundamental deficit is one of social cognition. We use the term social
cognition to refer to the application of mental abilities, which are otherwise relatively
preserved, in the context of problems which emerge from and require the interpretation of
emotional and social cues and the self-regulation of behavior in the context of complex social
functioning.
The purpose of this paper is to describe a patient with disturbance of social cognition
following traumatic damage to the orbitofrontal lobe. The neuropsychological findings in this
case stand between those presented by Malloy et al. (1993) and those presented by Eslinger
and Damasio (1985) and contribute to the characterization the nature of possible neuropsy-
chological test results after orbitofrontal damage. The case also demonstrates the marked
disturbance in social behavior, despite relatively preserved neurocognitive abilities, follow-
ing traumatic orbitofrontal brain injury and may contribute to the understanding of the nature
of that disturbance.

CASE REPORT

Patient SAL is a 38-year-old right-handed woman who was struck by a car as a pedestrian.
She sustained a left temporal skull fracture with evidence of a left temporal lobe punctate

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 Orbitofrontal Injury and Social Cognition 17s

TABLE 1
Basic Neuropsychological Functioning on Initial and Re-Evaluation

Measure Initial Evaluation Re-Evaluation

Digit Span (WMS-R)

Forward (raw score) 9 (64 %ile) 10 (81 %ile)
Backward (raw score) 6 (53 %ile) 7 (70 %ile)
Trailmaking A 48” (T = 28) 65” (T = 20)
Trailmaking B 68” (T = 38) 95” (T = 30)
Logical Memory I (WMS-R) 24/50 (43%) 21/50 (26 %ile)
Logical Memory II 20/50 (41%) 21/50 (46 %ile)
California Verbal Learning Test
Trials l-5 Total 62 (T = 50) 59 (T = 46)
Short delay free recall 12 (7, = 0) 15 (z = 1)
Short delay cued recall 10 (z = -2) 15 (2 = 1)
Long delay free recall 12 (2 = -1) 12 (z = -1)
Long delay cued recall 11 (z = -2) 14 (z = 0)
Recognition 13 (z = -2) 14 (z = -1)
Rey-Osterrieth Complex Figure
COPY 70/72 (SS = 12) 69/72 (SS = 11)
Immediate recall 34172 (SS = 9) 47172 (SS = 13)
Delayed recall 32/72 (SS = 8) __
Multilingual Aphasia Examination
Token Test 41/44 (33 %ile) 44/44 (82 %ile)
Boston Naming Test 55/60 (50 %ile) __
Boston Diagnostic Aphasia Examination
Repeating phrases 7/8 (wnl) 8/8 (wnl)
Complex ideation 1202 (T = 55) 12/12 (T = 55)
Reading sentences and paragraphs 1000 (wnl) 1000 (wnl)
Speech Sounds Perception Test 5 errors (T = 44)
Booklet Category Test 40 errors (T = 38) 39 CT--=38)
Wechsler Adult Intelligence Scale - Revised
Information 12 (T = 49)
Digit Span 10 (T-= 43) 11 (T= 47)
Arithmetic 12 (T= 52) 13 (T = 56)
Comprehension 8 (T= 33) 8 (T= 33)
Similarities 10 (T = 42) 9 (T= 39)
Picture Completion 5 (T = 28) 3 (T = 21)
Picture Arrangement __ 7 (T= 37)
Block Design 9(T=44) 9(T=44)
Digit Symbol 6 (T = 28) 6(T=28)
Verbal IQ (prorated) 99 (T = 37) 104 (T= 42)
Performance IQ (prorated) 86 (T = 33) 82 (T = 30)
Full Scale IQ (prorated) 94 (T = 34) 94 (T = 34)

hemorrhage on the CT scan obtained immediately on admission to the local trauma center.
She remained neurologically stable and 1 month later she was transferred to a rehabilitation
hospital with reduced responsiveness, but she made significant neurologic improvement over
the course of her treatment for about the next two months. Limited neuropsychological
evaluation during that period indicated good neurocognitive recovery with performance on
formal neuropsychological tests generally within normal limits, although it was felt that this
might still represent a decline from her previously higher level of intellectual functioning.
Following her discharge home her husband became concerned regarding her episodes of
abrupt crying and laughing, her rigidity and “obsessive” behaviors during the course of her
daily homemaking activities, and her increased sensitivity to feedback or criticism, which had
resulted in increasingly frequent arguments between them and conflicts with her four
children. Because of these concerns, she was referred to a post-acute neurorehabilitation
program for neuropsychological evaluation and possible treatment,

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 I76 K. D. Cicerone and L. N. Tanenbaum

FIGURE 1. MRI coronal section demonstrating encephalomalacia of the left frontal orbital gyrus (1A) and
an additional area of encephalomalacia of the left orbital gyrus associated with an area of encephalomalacia
of the left anterior temporal lobe (1B). MRI transverse sections demonstrating post-traumatic hemorrhage of
the left orbital gyrns of the frontal lobe and encephalomalacia of the gyrus recti bitalerally on T2 weighted
imaging (1C) and two small hemorrhagic contusions on the lateral surface of the right temporal and
temporal-parietal cortices (1D).

When seen for neuropsychological consultation 6 months after her injury she demon-
strated inconsistent and superficial awareness of her neurologic deficits. When questioned
directly regarding her current cognitive status she initially denied any problems. With
prompting, she stated that her big problem was her head but then stated that “I was told to
say that,” and this had apparently been the subject of considerable discussion between herself
and her husband. She later spontaneously reported that “I know that I am not as intelligent
as I used to be.” Prior to her injury she had obtained a university degree and she came from
a family of origin that highly valued intellectual accomplishments. It was very apparent that
she placed significant value on her intellectual ability and the intellectual accomplishments
of herself and her family. Her husband reported that she needed to start planning dinner the
night before and she demonstrated significant perseveration, for example, asking people
repeatedly what they wanted for dinner, which SAL explained on the basis of wanting to
show her family that she cared about them.

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 Orbitofrontal Injury and Social Cognition 177

FIGURE 1. Continued.

On neuropsychological evaluation (Table 1) she had a complete anosmia, but visual,

auditory and tactile cortical sensory functions were intact. Right-left orientation, topographic
orientation, and finger gnosis were intact. Proprioception, kinesthetic praxis and reciprocal
alternating movement were within normal limits bilaterally. There was no ideomotor or
ideational apraxia. Basic attention functions were intact, although she demonstrated moderate
slowing on tests of auditory, visual and motor processing speed. Her performance on the
Trailmaking tests was slow, but she did not have difficulty with the relatively more complex
cognitive demands of Trailmaking B. Constructional ability and perceptual abilities were
intact. Verbal and non-verbal memory were generally within normal limits. Language
functioning was generally intact. Intellectual functioning and conceptual reasoning were in
the average to low average range, although this was probably reduced from her pre-morbid
level. Despite her relatively intact memory, language and intellectual functioning, she
exhibited impaired performance on language and memory tests which required her to
overcome the habitual or “direct connotations” (Luria, 1980) of verbal statements. For
example, in response to the inverted question “If the lion was attacked by the tiger, which was
the victim?” she stated that the lion was king of beasts and could therefore not be the victim.
Despite the fact that she could repeat Luria’s (1980) fable of “the crow and the doves” nearly
verbatim, she had no appreciation of the ironic or moral aspects of the story. On formal

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 178 K. D. Cicerone and L. N. Tanenbaum

FIGURE 1. Continued.

measures of frontal lobe functioning she exhibited significant disinhibition on tests of motor
regulation and reduced verbal and behavioral fluency, but other measures of executive
functioning were generally normal limits (see below). Personality assessment with the MMPI
produced a valid profile with the clinical scales all essentially within the normal range (Welsh
code 82316497-O/5: KL-F/), although she exhibited a tendency to portray herself in an
unrealistically favorable manner.

MRI

On the basis of the findings of a complete anosmia and impaired behavioral regulation an
MRI of the brain was obtained when she was seven months post injury, and subsequently
interpreted with specific reference to analyzing the anatomical-behavioral correlates of her
lesion (Damasio & Damasio, 1989; Orrison, 1995). The MRI demonstrated an area of
post-traumatic encephalomalacia occupying the left orbital gyrus of the frontal lobe (Figure
1A) with a larger area of encephalomalacia of the left orbital gyrus associated with an area
of encephalomalacia of the left anterior temporal lobe (Figure 1B). On T2 weighted imaging
there was a post-traumatic hemorrhage of the left orbital gyrus and extensive encephaloma-
lacia of the gyrus recti bilaterally (Figure 1C). Two smaller areas of hemorrhagic contusion

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 Orbitofrontal Injury and Social Cognition 179

FIGURE 1. Continued.

were seen on the lateral surface of the right temporal and temporal-parietal cortices (Figure
ID).

Intervention

Because of her difficulties in daily functioning she received a course of neuropsycholog-

ical rehabilitation. During the course of her treatment, a primary area of intervention was the
attempt to increase her awareness of problem areas and their impact on her abilities to
perform her customary activities of daily living and social functioning. SAL participated in
several community based out trips that were videotaped in order to provide her with feedback
regarding her behavior. Initially, she exhibited difficulties with her interpersonal interactions
related to her inability to inhibit socially inappropriate behaviors and appreciate an alternative
perspective, for example, interrupting salespeople and becoming argumentative when her
needs were not addressed immediately. She was able to acknowledge these behaviors when
viewed on the videotape, and fairly quickly appeared to modify her behavior when the
camera was present to serve as a cue while in the community. However, she continued to have
difftculty internalizing these constraints in order to guide her behavior. Videotaped feedback
from her individual and group treatment sessions was also provided. The videotaped sessions

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 180 K. D. Cicerone and L. h? Tanenbaum

TABLE 2
Tests of Frontal Lobe Function and Social Cognition

Initial Normal
Measure Evaluation Re-evaluation Mean (SD)

Motor Regulation
Conflict Reactions Trial 1: II20 errors O/20 errors
Trial 2: l/20 errors
Anti-saccades Trial 1: 1 l/20 errors O/20 errors 1.84 (1.3)
Trial 2: l/20 errors
Word Fluency 31 46 44.4 (5.7)
Ruff Figural Fluency
Unique Designs 55 104.31 (28.7)
Perseverations 1 10.76 (19.2)
Wisconsin Card Sorting Test (64 trials)
Categories 4 5 3.76 (1.2)
Perseverative responses I 5 7.44 (3.78)
Mazes (WISC-R)
Errors 3 3 ___
Scaled Score 11 8 10.0
Tinker Toy Test
Number of pieces 40 42.2 (10.3)
Complexity I 7.8 (1.9)
Tower of London
Total score (max = 36) 33 33.2 (2.1)
Tests of Social Intelligence
Cartoon Predictions 13 20.93 (4.8)
Missing Cartoons 12 18.00 (5.7)
Social Translations 9 18.24 (4.3)
Means-End Problem Solving
Relevant means (mean) 0.50 2.05 (0.9)
Relevancy score (max = 1.00) 0.29 0.91

Note. For each measure, age and/or education corrected normative interpretations are in parentheses.

were reviewed in the context of her neuropsychological treatment sessions in order to

facilitate her recognition of any discrepancies between her spontaneous evaluation of her
performance and her “objective” evaluation of the videotaped sessions; the emphasis of these
sessions was on questioning to guide and encourage her own self-monitoring and evaluation
of these discrepancies, with limited direct interpretation of her behavior by the therapist.
SAL’s primary difficulties appeared to be related to her failure to use all of the relevant
information available to her in a situation, resulting in marked problems with her inferential
reasoning. Not surprisingly, she appeared to have particular difficulty utilizing complex or
subtle forms of information arising from social interactions, so that her social judgement was
particularly affected. Over the course of this treatment, SAL did appear to develop an
increased awareness of the types of problems she was having, however, she remained largely
unable to monitor and recognize these problems as they were emerging in the context of her
real-life interactions. She again appeared to benefit from tangible cues to signal her behavior,
and to develop some control over her behaviors in response to cuing, but with little apparent
internalization of this process. She also appeared unable to utilize her own emotional states
or feelings of cognitive dissonance to guide her behavior. For example, throughout her
treatment as well as in her daily functioning she exhibited frequent instances of pathological
laughter (which was one of the reasons that her husband had eliminated many of their shared
public social activities). The pathological laughing frequently emerged in treatment in
response to her frustration or her overt acknowledgement of an area of difficulty. (She
interpreted her laughter on these occasions as “feeling happy that she was being helped with

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 Orbitofrontal Injury and Social Cognition 181

her problems.“) This was addressed in her neuropsychological treatment through a behavioral
reinstatement procedure which interrupted whatever task she was doing until her laughter
was under control. She was eventually able to suppress these instances of laughing, but
continued to require some degree of external cuing to do so. Her attempts to control her
behavior, such as the laughing and her verbal tangentiality, were often accomplished through
the suppression of nearly all spontaneous behavior.
After several months of intervention, SAL began to exhibit increased anger and depression
in response to feedback. She again appeared to become increasingly defensive and resistant
to treatment.
Neuropsychological re-evaluation was conducted 14 months after the initial injury, with
emphasis upon her frontal lobe functioning and social cognition. Results from neuropsycho-
logical re-evaluation of general neuropsychological abilities are shown in Table 1. The results
on the various measures of frontal lobe functioning and social cognition from the initial and
re-evaluations are shown in Table 2.

Measures of “Frontal Lobe” Functioning and Social Cognition

Self-report measures. A number of self-report interview procedures were given to SAL and
her husband surrounding the neuropsychological re-evaluation, in order to assess their
perception of problems, especially in the areas of interpersonal and social functioning. On a
structured awareness interview, she reported that her family relationships had suffered due to
her injury, and attributed this to her husband’s increased negativity and expression of
animosity towards her in front of their children, which had created more tension in her
relationships with them. She denied that she had any cognitive or psychological problems
contributing to these difficulties. She reported that she was physically slower in performing
activities, which she attributed to an orthopedic injury, but not mentally slower. With direct
questioning regarding specific cognitive impairments, she acknowledged her anosmia and
stated that there are “brain cells dead and this will never change,” but she denied any
functional difficulties related to this. She denied problems with her attention, memory,
perceptual ability, language, or reasoning abilities: given specific feedback regarding past test
performance, she acknowledged that it may take her longer to respond to things going on
around her, but she again denied any functional impact. She reported that there had been
emotional changes related to her injury, in that she was “more sensitive” because of what she
had been through. With prompting regarding direct neurologic consequences of her injury,
she acknowledged that she had more difficulty controlling her emotions. On the Frontal Lobe
Personality Scale (Grace & Malloy, 1992), she reported an increase since her injury on the
“disinhibition” subscale, although this was accounted for by her responses to items that “food
has no taste or smell” and she “laughs or cries too easily.” She also reported some increase
on the “executive dysfunction” sub-scale in her ability to plan ahead since her injury,
although she indicated that she “chooses not to plan things” but could do so if desired. Her
husband reported significant changes related to his wife’s “disinhibition,” which in his case
also reflected her tendency towards anger and irritability, emotional lability and inappropriate
social behaviors. He also acknowledged increased “executive dysfunction,” which he char-
acterized primarily as her unawareness of problems or mistakes and inability to benefit from
feedback or accept constructive criticism from others. On the Iowa Collateral Head Injury
Interview (Vamey & Menefee, 1993) SAL’s husband reported substantial problems with his
wife’s inflexibility and rigidity, failure to learn from experience, lack of insight, and
non-reinforcing social behaviors; he reported moderate problems regarding her indecisive-

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 182 K. D. Cicerone and L. N. Tanenbaum

ness and tendency to become perplexed by changes in her environment, poor judgement,
impulsivity and disinhibition, poor empathy, and self centeredness.

Tests of Motor Regulation

On the initial evaluation, her performance on tests of motor regulation requiring condi-
tional reactions (Luria, 1980) was notably impaired due to numerous echopraxic responses.
On testing her ability to suppress a reflexive saccades and direct her gaze according to verbal
instructions her performance was impaired, again suggestive of disinhibition (Currie, Rams-
den, McArthure, & Maruff, 1991). On repeated testing, however, she was able to improve her
performance on both anti-saccade and motor regulation tasks, indicating that she retained
some capacity to bring her behavior under volitional control. Reproduction of a dynamic
movement sequence (fist-edge-palm) (Luria, 1980) was initially mildly fragmented bilater-
ally, although this again improved with practice. On re-evaluation, her performance on the
tests of motor regulation, including reproduction of fist-palm-edge sequences and conditional
motor responses, and on the clinical anti-saccade test, were all performed without error. Her
performance on anti-saccade and conditional motor responses in particular demonstrated a
pattern of progressive improvement in her capacity for basic behavioral self-regulation.

Fluency
Initial performance on testing her ability to generate words to a phonemic cue was mildly
reduced, although semantic naming was intact. On re-evaluation, her phonemic fluency had
improved to an average level. Behavioral fluency was assessed with the Figural Fluency Test
(Ruff, 1988), which required her to generate novel designs by connecting five regularly
arranged dots. Her performance was reduced on this measure, which appeared to be related
to significant behavioral slowing; repetition of the instructions emphasizing speed of re-
sponding did not appreciably change her performance. There was no evidence of persevera-
tion.

Planning and Self-Monitoring

On the 64 trial version of the Wisconsin Card Sorting Test (Robinson, Kester, Saykin,
Kaplan, & Gur, 1991) her ability to monitor and shift her responses according to concrete
feedback was well within normal limits on the initial neuropsychological evaluation and
remained intact on re-evaluation. Planning and organization of responses on the WISC-R
Mazes was within normal limits on initial evaluation; on re-evaluation her performance was
mildly reduced from the earlier evaluation, which appeared to be due to her deliberation and
slowing on the final trial. Initiation and organization on a relatively less structured task was
assessed with the Tinker Toy Test (Lezak, 1994). Qualitatively, she had some difficulty
modifying her initial intention when this did not produce the desired result, but this did not
significantly affect her quantitative performance, which was within normal limits according
to the criteria of Bayless, Vamey, and Roberts (1989) and Lezak (1994). Planning ability as
assessed with the Tower of London (Krikorian, Bartok, & Gay, 1994; Shallice, 1982) was
also within normal limits. She was able to complete all eight of the trials requiring 2, 3, or
4 moves without error. On trials requiring 5 moves she correctly completed two of the four
trials on her first attempt, which is consistent with the performance of non-injured subjects
(Shallice, 1982). On an extended version of this task requiring 6 or 7 moves to completion,
she successfully completed three of the four trials, again suggesting intact psychometric

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 Orbitofrontal Injury and Social Cognition 183

performance. Given the opportunity, she was able to utilize an overt verbal mediation strategy
to correct 2 of her 3 failed trials.

Tests of Social Cognition

She was administered several measures to more fully characterize her apparent difficulty
with the social aspects of cognition. On the Tests of Social Intelligence (O’Sullivan &
Guilford, 1976) she demonstrated significant impairment, once again, with her ability to
interpret thematic relationships involving non-verbal interpersonal interactions and behav-
ioral sequences (centile score = 3) and the varied meanings of verbal, social exchanges in
different contexts (centile score = 3). Her ability to appreciate non-verbal events in order to
predict the most likely consequences of a social situation was similarly impaired (centile
score = 2).

Means-End Reasoning
On the test of written expression from the Scholastic Abilities Test for Adults (Bryant,
Patton, & Dunn, 1991), her thematic expression to a visual story involving complex
relationships was notable for her poor ability to integrate the relevant features and subsequent
impairment in inferential reasoning. Of note, her vocabulary usage and the structure of her
story content were quite good, so that the scoring on this measure does not reflect her
inappropriate interpretations of the social relationships and social context. On the Means-
Ends Problems Solving (MEPS) test, she was able to describe relevant means on only 5 of
the 10 of the stories presented and she completed 2 stories with no logical means; 6 of 11
means which she described in her attempts to analyze the causal relationships were irrelevant.
The number and percentage of relevant means generated by SAL was below the 5th
percentile compared with 54 female university students (Platt & Spivack, 1975). She again
demonstrated a tendency to rely on limited and specific aspects of the stimulus situation, and
to be pulled toward affectively charged or personalized interpretations of the material. In
analyzing SAL’s responses on these measures, it appeared that her errors were not related to
a lack of knowledge regarding the appropriate behaviors, but were characterized by the
intrusion of idiosyncratic or emotionally charged associations which guided her decisions.
For example, the rationale that she spontaneously applied to her responses reflected a need
to “achieve a high level of status” or “show her family how much she loved them.” Although
these responses may not in themselves be considered aberrant, they were expressed without
an appreciation of the social context in which they occurred. Thus, it was the failure to
appreciate the relationship between her actions and goals in the relevant social context which
characterized her impairment.
In general, she demonstrated progressive improvement in her capacity for basic behavioral
regulation, as well as continued evidence of intact planning, self monitoring, and self-
regulation on formal neuropsychological testing. Despite this, she exhibited continued
difficulty and functional impairments in monitoring and controlling her emotional responses,
and particularly her complex social interactions. This impairment was evident on several
aspects of the neuropsychological evaluation. First, there was a tendency for her behavior to
be egocentric, and pulled by her idiosyncratic and personalized responses to a situation. She
demonstrated a similar tendency for her behavior to be pulled by the most salient aspects of
the environment, and a corresponding tendency to ignore relevant aspects of the environment.
These impairments were most apparent, both on neuropsychological testing and in her daily
functioning, when she needed to analyze and integrate the relatively subtle aspects of a
multifaceted “real-life” situation and to anticipate the impact of her behavior within that

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 184 K. D. Cicerone and L. N. Tanenbaum

context. Thus, when presented with a single, well structured situation with well-defined
response requirements she was able to regulate her behavior. However, she continued to have
difficulty when she needed to analyze social situations containing multiple, hierarchical
priorities and to guide her behavior according to a repertoire of potentially appropriate
responses.
While SAL was able to resume many of the basic, instrumental activities of daily living
that she performed before her injury, she continued to exhibit a profound impairment in her
social functioning. She exhibited significant marital difficulties as well as disruption of the
relationships with her children, resulting in severe distancing from her family. She attempted
but could not tolerate marital counseling. Her husband considered obtaining a divorce, but
eventually elected to remain together with marked curtailment of their social and marital
interactions. On re-administration of the Iowa Collateral Head Injury Interview two years
post-injury, there was no change in his evaluation of SAL’s behavior.

DISCUSSION

In terms of her neuropsychological functioning, the patient SAL represents an interme-

diate position between the cases presented by Malloy et al. (1993) and Eslinger and Damasio
(1985). She exhibited a number of behavioral signs of orbitofrontal damage, such as anosmia,
disinhibition, and lack of self-criticism. Her performance on tests of attention, memory and
intellectual functioning was generally normal, and she was also able to perform well on most
tests considered to be sensitive to executive dysfunction after frontal lobe lesions. In contrast,
she exhibited a significant impairment on formal tests of social cognition, which reflected her
similar difficulties in real-life social situations. It is of interest to note that her performance
on several basic tasks of behavioral regulation improved with practice and over time. This
suggests a degree of resolution of executive dysfunction which may influence the nature of
the observed deficit. This is supported by the fact that the patient described by Malloy et al.
(1993) was evaluated at 3 months post-injury while patient EVR was 8 years after surgery
when evaluated by Eslinger and Damasio (1985). Thus, our findings may represent the
various features on a continuum in the evolution of the cognitive disturbance after frontal
lobe injury. Our patient demonstrated improvement in performance on tests of frontal lobe
function, yet continued to exhibit a fundamental deficit in the area of social cognition.
We believe that the disturbance of social cognition can be ascribed to the breakdown of
regulatory processes usually attributed to the frontal lobe. In many ways, the patient SAL
resembles those patients with orbitofrontal lesions described by Lhermitte (1986) and
Shallice, Burgess, Schon, and Baxter (1989) whose behavior is rigidly dictated by their
immediate environment. Lhermitte (1986) described an environmental dependency syndrome
in which patients’ behaviors in complex, social situations are based primarily upon the salient
characteristics of the immediate environment, with loss of the flexibility and adaptability
required to behave effectively in those situations. These patients also exhibited apathy,
indifference. to social rules, and lack of self-criticism. Lhermitte reported that environmental
dependency was particularly apparent with lesions of the orbitofrontal lobes, due to the loss
of the normal frontal functions of modulation and inhibition which allows the unmediated
activation of parietal lobe systems and a direct response to environmental stimuli. Shallice et
al. (1989) described a patient with utilization behavior following an inferior-medial bifrontal
vascular lesion, and suggested that the deficit could be explained by the breakdown between
two neurologic control systems. One of these, contention scheduling, refers to the direct
activation of behavioral routines by the relevant perceptual input. A second level of control
is represented by the supervisory system of the frontal lobes, which serves to monitor and

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 Orbitofrontal Injury and Social Cognition 185

select the relevant behavioral schema and inhibit irrelevant schemata when novel responses
are required, or where the activation of habitual responses by contention scheduling fails to
produce an appropriate response. Following frontal lobe damage, there is an increased
likelihood that behaviors will be carried out in the absence of this supervisory selection and
inhibition.
Eslinger and Damasio (1985) have discussed the disturbance of social cognition following
orbitofrontal lesions in terms of the inability to analyze and integrate the premises of real-life
situations in order to select the appropriate response from among many options. According
to Damasio, Tranel, and Damasio (1991) the process of response selection in social cognition
requires the integration of numerous temporally dispersed and anatomically separated sets of
cognitive representations. The orbitomedial frontal cortex is anatomically well situated and
organized to integrate the heteromodal sensory information projected from parietal cortices
and the autonomic, visceral information projected from limbic cortices. This confluence of
external and internal information in orbitofrontal cortex allows the assignment of emotional
and motivational significance to the representation of events in the environment. The
fundamental mechanism by which orbitofrontal cortex guides social behavior, is therefore
through the activation of “somatic markers” in conjunction with the cognitive representations
of the environment to mark the “implied meaning” of a situation, that is, the value and
anticipated consequences of possible responses. It has subsequently been shown that orbito-
frontal damage may result in a failure of autonomic processes to trigger the appropriate
behavioral response (Damasio, Tranel, & Damasio, 1990), and insensitivity to future conse-
quences (Bechera, Damasio, Damasio, & Anderson, 1994). Although Shallice et al. (1989)
note that activation of the supervisory system is required in situations demanding a novel
response, they do not identify a specific mechanism through which this occurs. It is likely that
at least one of the ways in which the supervisory system would be activated would be through
covert, autonomic processes of recognition similar to those attributed by Damasio et al.
(1991) to somatic markers. This would occur when there is automatic recognition that routine
behavioral plans are inadequate for responding to a novel or problematic situation. Patients
with bilateral frontal-lobe lesions may fail to exhibit “surprise” in response to unexpected
occurrences in the environment, a finding associated with decreased emotional and auto-
nomic responsivity (Brazzelli, Colombo, Della Salla, & Spinnler, 1994). This disruption of
the cognitive and emotional processing of context-dependent environmental discrepancies
would also result in the failure to activate the appropriate behavioral responses to novel
situations. Thus, failure to activate the somatic markers and implied meanings to situations
would be accompanied by failure to activate the frontal lobe supervisory system, resulting in
the disturbance of complex, social cognition.
While the operation of such a system might be most apparent, and most necessary, when
responding to the varied and complex demands of social decision making, a similar mech-
anism might well be invoked in other forms of planning, monitoring and response regulation
attributed to the frontal lobes. In the performance of artificial problems or psychometric tests
(including most tests of “frontal-lobe” function) the premises are provided verbally and
within the limited constraints of the test, while in real-life the constraints are more variable,
diverse, and loosely configured. Although EVR-type patients are unable to select an appro-
priate response to real-life demands, they appear able to utilize verbal information to
formulate an appropriate response to hypothetical social problems (Saver & Damasio, 1991).
Although SAL demonstrated intact functioning on artificial tests of “frontal lobe function-
ing,” she was not, unlike EVR, able to effectively extract the requisite information from
hypothetical social problems presented either verbally or nonverbally, and her impairment on
these tasks was fairly representative of her behavior in naturally occurring real-life situation.
These measures required her to integrate the multiple possible interpretations and relation-

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 186 K. D. Cicerone and L. N. Tanenbaum

ships among the available information as a basis for her response. Similar deficits have been
observed after frontal-lobe lesions on tasks requiring responses to novel (Sirigu, Zalla, Pillon,
Grafman, Agid and Dubois, 1995) or open-ended situations (Brazzelli et al., 1994; Shallice
& Burgess, 1991), especially those which required integration of varied, multiple responses.
In analyzing SAL’s responses on these measures of social cognition, her performance
reflected intact basic cognitive abilities and adequate knowledge of social principles and
behaviors, but was characterized by the activation of interpretations and behaviors which did
not integrate the relevant aspects of the social context necessary to direct her behavior. Thus,
her errors were characterized not merely by the absence of an appropriate response but by the
failure to inhibit an inappropriate emotional or habitual response. In this regard, her behavior
is consistent with the role of orbitofrontal cortex in emotional learning, and specifically the
failure to inhibit historically salient emotional responses, which has also been related to the
disturbance in social functioning (Rolls, Homak, Wade, & McGrath, 1994). While SAL
generally demonstrated diminished emotionality, she also demonstrated instances of emo-
tional disinhibition, and a striking feature of her impairment in complex social situations was
the intrusion of highly personal or emotionally charged responses, which we feel is consistent
with the breakdown of frontal lobe regulation as described above.
Thus, the neuropsychological impairment on formal tests and in real-life situations may be
determined by the same fundamental cognitive disturbance. Successful performance on
measures of social cognition would require (a) inhibition of immediate, less relevant
responses and (b) conjunctive re-activation of the cognitive representations and implied
meanings of relevant situations based on prior (real-life) experience. Although this impair-
ment may be evident on both formal testing and real-life behaviors, the cognitive disturbance
after orbitofrontal lesions would be most apparent when the environment imposes relatively
fewer constraints on the interpretation of environmental events and selection of the appro-
priate behavioral response, and when it is necessary to infer the relevant aspects of a situation
from more subtle social or emotional cues and adapt one’s behavior accordingly.
Given that SAL sustained a traumatic brain injury, it is possible that areas of damage
outside of orbitofrontal cortex contributed to her functional impairments. Previous desdrip-
tions of the orbitofrontal deficit have included patients with lesions extending beyond the
ventromesial frontal cortex, including involvement of the dorsolateral and superior mesial
frontal lobes (Eslinger & Damasio, 1985), frontal white matter (Eslinger & Damasio, 1985;
Lhermitte, 1986), basal ganglia (Lhermitte, 1986; Shallice et al., 1989) and the anterior and
mesial temporal lobe (Brazelli et al., 1994; Rolls et al., 1994). In the case of SAL, there was
an area of left anterior temporal damage in addition to the bilateral damage to orbitofrontal
cortex. The anterior temporal cortex projects directly and indirectly, via dorsomedial thala-
mus, to orbitofrontal cortex, and receives projections from the orbitofrontal cortex in return.
The reciprocal interaction between orbitofrontal and anterior temporal cortices may contrib-
ute to the cognitive processes required for social cognition. For example, the orbitofrontal
cortex participates in the identification of neutral objects and faces, while the anterior
temporal cortex of both hemispheres appear necessary for the recognition of personally
relevant material. The nature of deficits after damage to the anterior temporal lobe suggests
an inability to evoke the relevant information which provides meaning to personal events
(Sergent, 1994). Cancelliere and Kertesz (1990) have also demonstrated that damage to the
anterior temporal lobe produces deficits in the comprehension of emotional expressions and
situations. EVR, whose damage was restricted to frontal cortex and white matter with sparing
of temporal, parietal and subcortical structures, was able to interpret hypothetical social
situations and his deficit was primarily one of impaired response selection and initiation.
SAL’s inability to both accurately interpret the meaning of emotional and social information

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 Orbitofrontal Injury and Social Cognition 187

(also reflected on nemopsychological testing) and to select the appropriate response may
reflect the combined contribution of lesions in the anterior temporal and orbitofrontal cortex.
Finally, SAL received an extensive course of rehabilitation directed at remediation of her
self-awareness and functioning in social situations. She did benefit from verbal and videotape
feedback concerning her social and emotional behavior in specific situations, and this
frequently enabled her to correct her mistakes and produce the appropriate response within
those situations. However, in novel, real-life situations, she remained unable to appreciate the
subtle social cues required to effectively guide her behavior and she appeared unable to
monitor her own emotional responses or to acknowledge the socially inappropriate aspects of
her behavior. Von Cramen and Mathes-von Cramen (1994) have also described a patient with
bilateral traumatic frontal lobe injury resulting in decreased social behavior, which they
related to an inability to use subtle social signals and monitor the effect of his behavior on
others, as well as an inability to use his preserved knowledge to organize his behavior.
Following treatment, they noted that the patient was able to utilize a routinized, external
structure to improve specific behaviors in the situations in which they had been trained, but
this improvement was not applied to novel situations. Thus, rehabilitation of patients with
disturbances of social cognition after orbitofrontal lesions may improve their functioning
through the establishment of specific competencies, but they appear unlikely to regain the
ability to integrate and respond fully to the subtle complexities and rich nuances of the social
environment.

REFERENCES

Barbas, H., & Pandya, D.N. (1991). Patterns of connections of the prefrontal cortex in the rhesus monkey associated
with cortical architecture. In Levitt, H.S., Eisenberg, H.M., & Benton, A.L. (Eds.), Frontal lobe function and
dysfunction (pp. 35-58). New York: Oxford University Press.
Bayless, J.D., Vamey, N.R., &Roberts, R.J. (1989). Tinker Toy Test performance and vocational outcome in patients
with closed-head injuries. Journal of Clinical and Experimental Neuropsychology, 11, 913-917.
Bechara, A., Damasio, A.R., Damasio, H. & Anderson, S.W. (1994). Insensitivity to future consequences following
damage to human prefrontal cortex. Cognition, 50, 7-15.
Bigler, E.D. (1988) Frontal lobe damage and neuropsychological assessment. Archives of Clinical Neuropsychology,
3, 219-297.
Brazzelli, M., Colombo, N., Della Salla, S., & Spinnler, H. (1994). Spared and impaired cognitive abilities after
bilateral frontal damage. Cortex, 30, 27-5 1.
Bryant, B.R., Patton, J.R., & Dunn, C. (1991). Scholastic abilities testfor adults. Austin, TX: Pro-Ed Publishers.
Butter, C.M., & Snyder, D.R. (1972) Alterations in aversive and aggressive behaviors following orbital frontal
lesions in rhesus monkeys. Acta Neurobiologica Experimental, 32, 525-565.
Cancelliere, A.E., & Kertesz, A. (1990) Localization in acquired deficits of emotional expression and comprehen-
sion. Brain and Cog&ion, 13, 133-147.
Currie, J., Ramsden, B., McArthure, C., & Maruff, P. (1991) Validation of a clinical antisaccadic eye movement test
in the assessment of dementia. Archives of Neurology, 48, 644-648.
Damasio, A.R., Tranel, D., & Damasio H.C. (1990) Individuals with sociopathic behavior caused by frontal damage
fail to respond autonomically to social stimuli. Behavioral Brain Research, 41, 81-94.
Damasio, A.R., Tranel, D., & Damasio, H.C. (1991). Somatic markers and the guidance of behavior: Theory and
preliminary testing. In Levitt, H.S., Eisenberg, H.M., & Benton, A.L. (Eds.), Fronral lobe function and
dysfunction (pp. 217-229). New York: Oxford University Press.
Damasio, H., & Damasio, A.R. (1989). Lesion analysis in neuropsychology. New York: Oxford University Press.
Eslinger, P.J., & Damasio, A.R. (1985). Severe disturbance of higher cognition after bilateral frontal ablation: Patient
EVR. Neurology, 35, 1731-1741.
Grace, J., & Malloy. P. (1992). Frontal Lobe Personality Scale. National Academy of Neuropsychology Research
Consortium.
Hebb, D.O. (1945). Man’s frontal lobes: A critical review. Archives of Neurology and Psychiatry, 54, 10-24.
Kling, A., & Steklis, H.D. (1976). A neural substrate for affiliative behavior in nonhuman primates. Brain, Behavior
and Evolution, 13, 216238.

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018
 188 K. D. Cicerone and L. N. Tanenbaum

Krikorian, R., Bartok, J., & Gay, N. (1994). Tower of London procedure: A standard method and developmental data.
Journal of Clinical and Experimental Neuropsychology, 16, 84&850.
Lezak, M. (1994). Neumpsychological assessment New York Oxford University Press.
Lhermitte, F. (1986). Human autonomy and the frontal lobes. Part II: Patient behavior in complex and social
situations: The “‘environmental dependency syndrome.” Annals of Neurology, 19, 335-343.
Luria, A.R. (1980). Higher cortical functions in man. New York: Basic Books.
Malloy, P., Bibrle, A., Duffy, J., & Cimino, C. (1993). The orbitomedial frontal syndrome. Archives of Clinical
Neuropsychology, 8, 185-201.
Mesulam, M.-M. (1986). Frontal cortex and behavior. Annals of Neurology, 19, 320-325.
Grrison, W.M. (1995). Atlas of brain funcfion. New York Thieme Medical Publishers.
O’Sullivan, M., & Guilford, J.P. (1976). Four factor tests of social intelligence (behavioral cognition) manual of
instructions and interpretations. Palo Alto: Consulting Psychologists Press.
Platt, J.J., & Spivack, G. (1975). Manual for the means-ends problem solving procedure. Philadelphia: Hahneman
Medical College and Hospital.
Robinson, L.J., Kester, D.B., Saykin, A.J., Kaplan, E.F., & Gur R.C. (1991). Comparison of two short forms of the
Wisconsin Card Sorting Test. Archives of Clinical Neuropsychology, 6, 27-33.
Rolls, E.T., Homak, J., Wade, D., & McGrath, J. (1994). Emotion-related learning in patients with social and
emotional changes associated with frontal lobe damage. Journal of Neurology, Neurosurgery and Psychiatry, 57,
1518-1524.
Ruff, R.M. (1988). Rufffiguralfluency test administration manual. San Diego: Nemopsychological Resources.
Saver, J.L., & Damasio, A.R. (1991) Preserved access and processing of social knowledge in a patient with acquired
sociopathy due to ventromedial frontal damage. Neuropsychologia, 12, 1241-1249.
Sergent, J. (1994). Cognitive and neural structures in face processing. In Kertesz, A. (Ed.), Localization and
neuroimaging in neuropsychology (pp. 473-494). San Diego, CA: Academic Press.
Shallice, T. (1982). Specific impairments of planning. Philosophical Transactions of the Royal Sociery of London
[Biology], 298, 199-209.
Shallice, T., & Burgess, P.W. (1991). Deficits in strategy application following frontal lobe damage in man. Brain,
114, 727-741.
Shallice, T., Burgess, P.W., Schon, F., & Baxter, D.M. (1989). The origins of utilization behavior. Brain, 112,
1587-1598.
Sirigu, A., Z&a, T., Pillon, B., Grafman, J., Agid, Y., & Dubois, B. (1995). Selective impairments in managerial
knowledge following pre-frontal cortex damage. Cortex, 31, 301-316.
Varney, N.R., & Menefee, L. (1993) Psychosocial and executive deficits following closed head injury: Implications
for orbital frontal cortex. Journal of Head Trauma Rehabilitation, 8, 3244.
von Cramen, D. Y., & Matthes-von Cramen, G. (1994). Back to work with a chronic dysexecutive syndrome? (a case
report). Neuropsychological Rehabilitation, 4, 399-417.

Downloaded from https://academic.oup.com/acn/article-abstract/12/2/173/1717

by guest
on 08 August 2018