See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/21657226

Developmental Consequences of Childhood Frontal Lobe Damage

Article in Archives of Neurology · August 1992

DOI: 10.1001/archneur.1992.00530310112021 · Source: PubMed

CITATIONS READS

242 863

4 authors, including:

Paul Eslinger Hanna Damasio

Penn State Hershey Medical Center & College of Medicine University of Southern California
223 PUBLICATIONS 13,313 CITATIONS 210 PUBLICATIONS 40,125 CITATIONS

SEE PROFILE SEE PROFILE

Antonio Damasio
University of Southern California
326 PUBLICATIONS 87,942 CITATIONS

SEE PROFILE

All content following this page was uploaded by Paul Eslinger on 07 April 2021.

The user has requested enhancement of the downloaded file.

 Developmental Consequences of Childhood
Frontal Lobe Damage
Paul J. Eslinger, PhD; Lynn M. Grattan, PhD; Hanna Damasio, MD; Antonio R. Damasio, MD, PhD

\s=b\ A 33-year-old woman underwent neurologic and neu- may not be immediately apparent or may vary throughout
ropsychological studies 26 years after she sustained damage development.32"34 In with
a comparative study 30 years ago of
to the frontal lobe. The findings ofthe neurologic examination children and adults brain lesions, Teuber and Rudel35
were normal, and magnetic resonance imaging revealed a le- differentiated three patterns of outcome after childhood le¬
sion in left prefrontal cortex and deep white matter. Cerebral sion: (1) fixed impairments with no recovery over time; (2)
blood flow studies showed an abnormal pattern in both left recovery over time by various compensatory processes; and
and right frontal regions. The patient exhibited striking neu- (3) delayed onset of impairments throughout development.
ropsychological defects in higher cognition, most notably in More recent neuropsychological studies indicate that there
self-regulation of emotion and affect and in social behavior. may be some anatomic basis for these outcome differences.
Analysis of her behavioral development failed to yield a pat- That is, nonfrontal cerebral lesions in childhood have been
tern of abrupt onset of defect immediately after the lesion oc- associated with impairments that are frequently identifiable
curred. On the contrary, there was a delayed onset of defects, in the early stages and show various degrees of recovery,
followed by a period of seeming progression, and finally an such as aphasia, amnesia, and visual disorders.36"39 However,
arrest of development in adolescence. We suggest that this pe- frontal lobe damage in childhood poses special questions
culiar pattern is the natural consequence of the varied about the pattern of outcome that may arise from the fact that
changes that occurred in brain development and social cog- the frontal lobes undergo a longer, multistage maturation
nition during the patient's formative years. While certain process extending well into adolescence.13-26"30-40"42 Hence,
long-term neuropsychological deficits in our case are similar frontal lobe damage at varying ages prior to adulthood may
to those following frontal damage in adults, the delayed onset lead to a different onset of impairments and pattern of
and progression of deficits are different. recovery.
(Arch Neurol. 1992;49:764-769) In the following study, we examined the consequences
of early frontal lobe damage on higher cognitive and psy¬
lobe le¬ chological development in a 33-year-old woman who sus¬
The neuropsychologicalbeen
consequences of frontal
sions in adults havedescribed
studies and group analyses.1"13 The spectrum
in detailed case
of associated
tained her injury at 7 years of age.

METHODS
cognitive and behavioral changes have been incorporated
in several models that address not only location of lesion Neuropsychological Studies
and disruption of intrinsic frontal lobe mechanisms, but The patient underwent comprehensive neuropsychological and
also pathologic features within the multiple neural systems neuroimaging studies 26 years after she sustained damage to the
that interact with the frontal lobes.13"16 By comparison, few frontal lobe. Cognitive evaluation with the Benton Laboratory Com¬
cases of focal, stable frontal lobe lesions sustained in prehensive Neuropsychological Examination assessed intellect,
childhood have received comparable attention. Those learning and memory, language, visual perception, constructional
available allude to significant, long-term impairment in praxis, executive functions, and academic achievement.'''43"52
The patient's personality and social behavior were assessed
social behavior and emotional maturity.17"21 Study of such through numerous clinical interviews, the Minnesota Multiphasic
cases is relevant to diagnostic, management, and theoret¬
Personality Inventory, Hogan's Empathy Scale,53 and a Moral hidg-
ical issues, many of which have been raised only through ment Interview.54 Collateral data were obtained through the pa¬
investigations with animal models or through develop¬ tient's daily diary, her parents' report, academic records, and notes
mental studies in normal children.22"31 from psychotherapy sessions spanning 7 years of young adulthood.
Neuropsychological impairments associated with child¬
hood cerebral diseases have been noted to continue well be¬ Neuroimaging Studies
yond the recovery of overt physical and neurologic symp¬ Neuroimaging studies included computed tomography, mag¬
toms. Unlike the effects of adult brain injury, the netic resonance imaging (Ti- and T2-weighted images), and single
neuropsychological consequences of early cerebral injury photon emission computed tomography with xenon 144. These
images were analyzed by an investigator blinded to the patient's
Accepted for publication February 21, 1992.
neurologic and neuropsychological data. A standard method of
anatomical analysis was used to interpret all abnormal images.55
From the Department of Medicine, Division of Neurology, and the
Department of Behavioral Science, Pennsylvania State University Col- RESULTS
lege of Medicine, The Milton S. Hershey Medical Center, Hershey, Pa
(Dr Eslinger); the Department of Neurology, University of Maryland Premorbid History
School of Medicine, Baltimore (Dr Grattan); and the Department of The patient was the older of two children born to the
Neurology, Division of Behavioral Neurology and Cognitive Neuro- same pair of biological parents in a middle-class semirural
science, University of Iowa College of Medicine, Iowa City (Drs H.
Damasio and A. R. Damasio). community. Her birth was uncomplicated and followed a
Reprint requests to Division of Neurology, The Milton S. Hershey normal pregnancy. Developmental milestones (eg, speech,
Medical Center, 500 University Dr, Hershey, PA 17033 (Dr Eslinger). language, sitting up, and toilet training) were entirely nor-

Downloaded From: http://jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 09/09/2014
 mal. Social and emotional development were appropriate dicated significant difficulties in organizing information,
until the time of her brain injury at 7 years of age. Her utilizing examiner feedback to modify her responses, and
first-grade teacher noted her to be always proper, immac¬ planning toward a remote goal. She exhibited significant
ulately dressed and groomed, and often the only child in cognitive rigidity in tasks requiring shifting of response
the classroom to remember her umbrella on rainy days. set51 (ie, reactive flexibility) and divergent production49 (ie,
Premorbidly, the patient's level of academic achievement spontaneous flexibility). Finally, on a modified cognitive
was average. Her parents and sister are also of average estimation task,9 she had difficulty in making judgments
educational and occupational achievement. There is no about environmental events. For instance, she reported
family history of mental illness, substance abuse, or that 90% of the US population was male; proposed that one
social-emotional impairment. could drive from New York to Los
decided that race horses galloped at
Angeles in 6 hours; and
5 miles
a rate of per
Neurologic History hour.
At 7 years of age, the patient sustained a spontaneous
intraparenchymal hemorrhage of unknown cause in the Personality and Social Behavior
left frontal region. An emergency craniotomy was per¬ The patient presented an austere but sloppy appearance.
formed to evacuate the hemorrhage. The patient remained Her clothing consisted of a simple dress and sandals, with¬
in coma for 5 days and was hospitalized for 1 month. out makeup. She specifically pointed out that her attire, hair¬
Thereafter, with the exception of treatment for primary style, and omission of makeup were purposely selected to be
generalized tonic-clonic seizures, which have been well compatible with the teachings of her religion. However,
controlled, her physical recovery was complete and nor¬ since our evaluation marked a special occasion, she decided
mal. The parents were instructed to return the child to to make an exception and wore a necklace.
school and usual activities. Clinical neurologic examina¬ Assessment of the patient's personality and social and
tion results have been normal. emotional development suggested that she had significant
difficulties with managing and expressing strong emo¬
Neuropsychological Examination tions, establishing meaningful relationships, and integrat¬
The patient's clinical presentation varied with the con¬ ing multiple aspects of her social and emotional self into
text of evaluation. Within her familiar home environment, a stable and consistent presentation over time. Specifically,
she was friendly, verbal, and well oriented. During exam¬
ination at the University of Iowa Hospitals and Clinics,
the Minnesota Multiphasic Personality Inventory profile
was valid, but abnormal (Welsh code 46"98'71230-5:
Iowa City, she was hostile, with puerile affect and disin- F'LK/). Women generating a similar pattern of responses
hibition. A consistent pattern during personality and cog¬ have been described as excessively demanding and de¬
nitive assessment was her lack of attention to detail, her pendent, unable to profit from experience, and harboring
disorganized approach to problem solving, her difficulty considerable hostility, which they are unable to effectively
in establishing a plan and in executing multiple steps to¬ or directly express. In addition, the patient's responses
ward a relatively remote goal, and cognitive rigidity. She were similar to those of individuals who experience and
demonstrated an impulsive response style and, unless en¬ demonstrate significant emotional shallowness toward
couraged, failed to give in-depth thought to questions and others and have seriously disrupted interpersonal rela¬
tasks. tionships. She also generated a very low score on the stan¬
Results of formal testing indicated an overall low- dardized measure of empathy (27:2 SD below the mean),
average range of intellect (Wechsler Adult Intelligence which was confirmed by parental report on an equivalent
Scale-Revised intelligence quotient [IQ] scores: verbal IQ, form. The finding indicates that the patient has unusual
81, performance IQ, 84, and full scale IQ, 80). Considerable difficulty in apprehending the viewpoints and situations of
subtest variability occurred. The patient had particular other people.
difficulty with subtests requiring "freedom from distract- Her analysis of moral dilemmas suggests that she views
ibility" (ie, arithmetic, digit span, and digit symbol substi¬ such complex situations in terms of concrete and Stereo¬
tution), but was average in verbal and nonverbal reason¬ typie notions of "good" and "bad" behavior. In the
ing, comprehension, and perceptual ability. Despite her 12 forefront of her responses are fixed rules. For instance, she
years of formal education, her academic achievement lev¬ decided it would be wrong for a poor young man to steal
els were at the third-grade level or lower in spelling, arith¬ an expensive drug from a greedy dispenser because, "It's
metic, and oral word reading. Her learning and memory against the law. It's against the Ten Commandments.
were within the low-average range, and she did not appear That's against the Bible. That's against morals." When the
amnesic in any way. genuine plight of the poor young man was pointed out to
Her conversational speech was spontaneous, fluent, and her, she quickly changed her approach to the problem. She
nonparaphasic, without evidence of word selection or indicated that when laws and rules do not permit a person
prosodical disturbance. Dichotic listening revealed a mild to do what they want, then the person should change the
left ear extinction, with normal results on screening audi- rules, basing her response on motives of instrumental he¬
ometry. Her verbal associative fluency was defective, but donism and interpersonal concordance. The discrepancy
her category (semantic) fluency was intact. between her responses was never resolved. Her approach
Visual pattern discrimination, spatial judgment, and to these conflicting situations did not adhere to a set of
block constructions were within the average range. Copy consistent ethical principles or values, but was driven by
of the Rey-Osterrieth complex figure was spatially disor¬ a varying rationale that would serve to meet immediate
ganized, perseverative, and sloppy. Her construction im¬ needs or to indicate in an absolute inflexible way what was
proved significantly, however, when it followed a pro¬ good and bad behavior. Her level of moral reasoning most
grammed format that presented one element at a time.56 closely resembled that of early adolescents, 10 to 13 years
Measures of executive and self-regulatory processes in- of age.54

Downloaded From: http://jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 09/09/2014
 Fig 1.—Magnetic resonance imaging scan (T2-weighted images) showing deep left prefrontal lobe lesion.

Through retrospective analysis of family and academic difficult relationship as "obedience to her religion" and
records, as well as extensive interviews with the patient's cites skewed and concrete biblical references to justify it.
parents, we attempted to gauge the impact of her early Meanwhile, her increasing church involvement appears to
frontal lobe lesion on her daily living. During the 3 years provide a structure for her identity and behavior, dictating
immediately following her injury (7 to 10 years of age), she her dress, interpersonal contacts, and daily activities. Her
became a slower learner and a lower achiever in school. In few friendships are initiated through the church, but are
late childhood and early adolescence, significant difficul¬ short-lived after repeated overstepping of interpersonal
ties became progressively evident in social and emotional boundaries. She extends her visits beyond the time for
domains. She eventually maintained only one friend, which she is welcome and quickly depends on newfound
alienating herself from others through noncooperative in¬ friends to meet all of her emotional needs.
teractions and frequent arguments. She became pregnant The patient's vocational record has also been maladaptive.
1 year after high school graduation by the first man she After high school graduation she attended beautician train¬
dated, and was married. After 7 years of marital conflicts, ing school for 1 year. However, she was dismissed from her
her husband divorced her and gained custody of their first position because she persistently made hurtful state¬
child because of the patient's impulsive and immature be¬ ments, asked embarrassing questions, and gave impulsive
havior. She appeared unable to regulate her emotions and responses. Since that time she has been unable to hold a job
unable to learn from her experience as a wife, homemaker, for more than a few weeks, although she has the intellectual
and mother. For instance, while she was able to wipe a ta¬ capacity and physical ability to learn the basic tasks of a
ble, wash a dish, measure a quantity, and open a can, she semiskilled occupation. Her work is characterized by poor
could not plan or execute the steps necessary for meal interpersonal skills, by her inability to execute the required
preparation or even cleaning a room. Thereafter, her pro¬ activities throughout the course of a day, and by her failure
miscuity increased. She proclaimed her love for numerous to learn from mistakes. Moreover, she responds to criticism
antisocial and unsavory characters, reporting up to seven by externalizing blame, becoming obstinate, and telling her
boyfriends at a time. She eventually met a self-proclaimed employers how they should be managing their business.
preacher, and after a 2-month courtship decided to marry Despite a poor work record for 12 years, the patient remains
him because his religion accepted second marriages. This rigid in her job-hunting strategies, naive, and unrealistic
relationship, however, has been marked by conflicts and about her vocational abilities. Her approach is to read the
abnormal sexual activity for several years. She justifies her newspaper and apply for positions that "look interesting,"

Downloaded From: http://jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 09/09/2014
 Fig 2.—Depiction of the lesion seen in Fig 1 on the best-fitting template system and the projection of the lesion onto a lateral and mesial image of
the left hemisphere.

such as an airline stewardess and a store manager. Another both left and right frontal cortices, suggesting bilateral ab¬
aspiration is to open a religious book store in the West, be¬ normal function (Fig 3).
cause a friend informed her there were none. When asked
about these vocational goals, her responses are devoid of any
COMMENT
financial or practical planning, as well as anticipation of the
various steps leading to employment. The patient's frontal lobe lesion at 7 years of age
occurred during an important phase of matura¬
tion. 13-2<s-28,3o,40-42^7-6o Neurobiological events such as myeli-
Neuroimaging Results nation, elaboration of dendritic features in prefrontal py¬
Neuroanatomical interpretation of the magnetic reso¬ ramidal neurons, and corticocortical connectivity, which
nance images revealed damage in the left prefrontal are prolonged postnatal processes, remain incomplete at
region, involving Brodmann's areas 9, 46, and 32. The le¬ this age. Development of frontal lobe cognitive operations
sion extended deep into the white matter, reaching the are far from adult and even adolescent levels. The results
most superior portion of the left frontal horn and damag¬ documented in this study indicate that maturation of sys¬
ing the white matter underlying Brodmann's areas 45 and tems dependent on frontal cortex was inexorably altered
24. No structural abnormality could be detected in the right by the childhood lesion, severely interfering with devel¬
frontal lobe (Figs 1 and 2). opment of adaptive behavior at subsequent stages of the
Single photon emission computed tomography with xe¬ patient's life. The consequences have continued to be ex¬
non 144 inhalation revealed abnormally low blood flow in pressed over a long period in cognitive and social domains,

Downloaded From: http://jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 09/09/2014
 Identity formation, for example, requires impulse control,
synthesis of personal and social experiences across time and
space, and integration with other forms of knowledge. An¬
other higher cognitive process such as considering a wide
range of possibilities, associated consequences, and alterna¬
tive viewpoints (ie, cognitive flexibility) partly underlies de¬
velopment of moral maturity and empathy. We recently re¬
ported that there is a significant correlation between mea¬
sures of cognitive flexibility and empathy in adult
patients
who have suffered brain damage.62 Furthermore, this inter¬
relationship was most pronounced after injury to the left
frontal region,63 where our patient sustained an early lesion.
In summary, we propose that the early frontal lobe lesion in
this patient had a strong impact on her social and psycho¬
logical maturation by altering underlying cognitive pro¬
cesses.
At the neurobiological level, there are diverse ana¬
tomical and physiological processes that may have been
affected by the patient's lesion and may have influenced
her course of impairment. Early frontal lobe ablation
has been associated with subsequent anatomical
changes in proximal and distal brain areas.64-65 In the
Fig 3.—Single photon emission computed tomographic study with xe¬ nonhuman primate, these take the form of anomalous
non 144 inhalation showing low flow in the left and right frontal regions. gyri and sulci in the frontal lobe as well as in cortical
areas interconnected with that site. With early unilateral
frontal lobe ablation, these anatomical changes are ob¬
though in a pattern that is quite different from that served in the contralateral frontal lobe as well. This may
observed in adults. The most disabling consequences were be the reason why our patient's clinical history and
not the most immediate. The patient's initial difficulties neuropsychological results are so similar to those in
were registered in terms of a slower rate of academic cases with bilateral lesions.1721 It is also likely that the

learning. During early adolescence, 3 to 5 years after the bilateral cerebral blood flow changes in the frontal re¬
lesion occurred, social impairment became increasingly gions reflect this contralateral effect.
evident. The patient's adjustment appeared to decline Analysis of electroencephalographlc phase and coher¬
gradually as she encountered progressively more complex ence in normal children has indicated that discrete
social situations. At the same time, developmental psy¬ "growth spurts" occur in each frontal lobe throughout
chological demands were escalating with tasks such as childhood and adolescence.42 These correspond well to Pi-
identity formation, adoption of sexual attitudes, internal- aget's cognitive-development stages. Our patient's lesion
ization of social and moral values, exploration of occupa¬ occurred at an age that would have certainly impeded such
tional roles, and participation in meaningful interpersonal physiological maturation. But the time frame in which
relationships. We believe that the appearance of progres¬ deficits become clinically evident may depend on the pre¬
sive impairment resulted from an increasing discrepancy cise site of lesion within the frontal lobe and the role of that
between the burgeoning demands of adolescent develop¬ site in subsequent maturation. In our patient, the lesion
ment and altered maturation of frontal lobe neural and was well restricted to the polar and mesial
portion of the
cognitive systems. According to available indexes, the pa¬ left prefrontal cortex and deep white matter, and her de¬
tient's social and psychological development was virtually fect did not become apparent until early adolescence, 3 to
arrested in early adolescence. As an adult, the patient 5 years after the lesion occurred.
shows many behavioral and cognitive deficits that are Another important facet of altered neurophysiological
similar to those observed in cases of adult-onset frontal processing, particularly as it pertains to the patient's social
lobe damage. These include a persistent pattern of defi¬ impairment, may involve the autonomie nervous system.
cient decision making, hallmarked by capricious social and Recently, Damasio et al15 have shown that adults with
vocational judgment, rigidity, impulsivity, interpersonal frontal lobe lesions and acquired social conduct defects
conflict, and little ability to synthesize the lessons of expe¬ exhibit a selective deficiency in autonomie responsiveness
rience. These deficits, which are not accountable by mea¬ to socially meaningful stimuli. They have hypothesized
surable impairment of perception, memory, language, and that the failure to evoke autonomie responses under these
reasoning, have had a pervasive effect on the patient's life, conditions indicates an inability to activate "somatic
precluding any consistent form of productive, goal- states" that have been learned previously in association
directed behavior. with social situations and that play a key role in decision
This unusual course of impairment may be related to al¬ making. This process would appear to be pertinent to so¬
teration of cognitive and neurobiological events. On a cog¬ cial development and learning to recognize, control, and
nitive level, the patient failed to acquire the executive and properly associate a variety of somatic states with social
self-regulatory processes associated with the frontal lobe. situations and their consequences. The patient may never
This became most apparent in early adolescence, several have acquired those associations and thus may be unable
years after her lesion occurred, at a time when maturation of to evoke in any form the expected somatic states to guide
such processes is critical to psychological development, a her social behavior. However, this remains a hypothesis to
pattern that bears certain similarities to the primate model.61 be tested in cases of early frontal lobe lesion.

Downloaded From: http://jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 09/09/2014
 This study was supported in part by program grant NS 19632 from environmental considerations. J Consult Clin Psychol. 1981;49:777-790.
the National Institute of Neurological Disorders and Stroke, Bethesda, 33. Grattan LM, Eslinger PJ. Frontal lobe damage in children and adults:
Md. a comparative review. Dev Neuropsychol. 1991;7:283-326.
We thank Tricia Johnson for preparation of the manuscript. 34. Ernhart CB, Graham FK, Eichman PL, Marshall JM, Thurston D. Brain
injury in the preschool child: some developmental considerations, II: com-
References parison of brain injured and normal children. Psychol Monogr. 1963;77:17\x=req-\
33.
1. Harlowe JM.Recovery from severe injury to the head. Publ Mass Med 35. Teuber H-L, Rudel RG. Behavior after cerebral lesions in children and
Soc. 1868;2:327-346. adults. Dev Med Child Neurol. 1962;4:3-20.
2. Brickner RM. The Intellectual Functions of the Frontal Lobes: Study 36. Cranberg LD, Filley CM, Hart EJ, Alexander MP. Acquired aphasia in
Based Upon Observation of a Man After Partial Bilateral Frontal Lobectomy. childhood. Neurology. 1987;37:1165-1172.
New York, NY: Macmillan Publishing Co Inc; 1936. 37. Ostergaard AL. Episodic, semantic and procedural memory in a case
3. Brickner RM. Brain of patient 'A' after bilateral frontal lobectomy: sta- of amnesia at an early age. Neuropsychologia. 1987;25:341-357.
tus of frontal lobe problem. Arch Neurol Psychiatry. 1952;68:293-313. 38. Young AW, Ellis HD. Childhood prosopagnosia. Brain Cogn. 1989;9:
4. Ghent L, Mishkin M, Teuber H-L. Short-term memory after frontal lobe 16-47.
injury in man. J Comp Physiol Psychol. 1962;55:705-709. 39. Loonen M, Van Dongen HR. Acquired childhood aphasia: outcome
5. Milner B. Some effects of frontal lobectomy in man. In: Warren JM, 1 year after onset. Arch Neurol. 1990;47:1324-1328.
Akert K, eds. The Frontal Granular Cortex and Behavior. New York, NY: 40. Schade JP, van Groenigen DB. Structural organization of the human
McGraw-Hill International Book Co; 1964:313-331. cerebral cortex, I: maturation of the middle frontal gyrus. Acta Anat. 1961;
6. Benton AL. Differential behavior effects in frontal lobe disease. Neu- 47:74-111.
ropsychologia. 1968;6:53-60. 41. Mrzljak L, Uylings HBM, van Eden CG, Judais M. Neuronal develop-
7. Blumer D, Benson DF. Personality changes with frontal and temporal ment in human prefrontal cortex in prenatal and postnatal stages. In: Uylings
lobe lesions. In: Benson DF, Blumer D, eds. Psychiatric Aspects of Neurologic HBM, van Eden CG, De Bruin JPC, Corner MA, Feenstra MGP, eds. Progress
Disease. New York, NY: Grune & Stratton; 1975:151-170. in Brain Research. Amsterdam, the Netherlands: Elsevier Science Publishers;
8. Hecaen H, Albert ML. Disorders of mental functioning related to fron- 1990;85:185-222.
tal lobe pathology. In: Benson DF, Blumer D, eds. Psychiatric Aspects of 42. Thatcher RW. Maturation of the human frontal lobes: physiological
evidence for staging. Dev Neuropsychol. 1991;7:397-419.
Neurologic Disease. New York, NY: Grune & Stratton; 1975:137-150. 43. Wechsler DA. Wechsler Adult Intelligence Scale-Revised. New York,
9. Shallice T, Evans ME. The involvement of the frontal lobes in cognitive
estimation. Cortex. 1978;4:294-303. NY: Psychological Corp; 1981.
10. Eslinger PJ, Damasio AR. Severe disturbance of higher cognition after 44. Benton AL. The Revised Visual Retention Test. 4th ed. New York, NY:
bilateral frontal lobe ablation: patient EVR. Neurology. 1985;35:1731-1741. Psychological Corp; 1974.
11. Lhermitte F. 'Utilization behavior' and its relation to lesions of the 45. Rey A. L'examen Clinique in Psychologie. Paris, France: Presses Uni-
frontal lobes. Brain. 1983;106:237-255. versitaires de France; 1964.
12. Milner B, Petrides M. Behavioral effects of frontal lobe lesions in man. 46. Wechsler DA. A standardized memory scale for clinical use. J Psychol.
Trends Neurosci. 1984;7:403-407. 1945;19:87-95.
13. Luria AR. The Working Brain. New York, NY: Basic Books Inc 47. Rey A. L'examen psychologique dans les cas d'enc\l=e'\phalopathietrau-
Publishers;1973. matique. Arch Psychol. 1941;28:286-340.
14. Damasio AR. The frontal lobes. In: Heilman KM, Valenstein E, eds. 48. Osterrieth PA. Le test de copie d'une figure complexe. Arch Psychol.
Clinical Neuropsychology. New York, NY: Oxford University Press; 1985: 1944;30:206-356.
339-375. 49. Benton AL. Multilingual Aphasia Examination. Iowa City, Iowa: Uni-
15. Damasio AR, Tranel, Damasio H. Individuals with sociopathic be- versity of Iowa;1976.
havior caused by frontal lobe damage fail to respond 50. Benton AL, Hamsher KS, Varney NS, Spreen O. Contributions to Neu-
autonomically to social
stimuli. Behav Brain Res. 1990;41:81-94. ropsychological Assessment. New York, NY: Oxford University Press; 1983.
16. Stuss D, Benson DF. The Frontal Lobes. New York, NY: Raven Press; 51. Heaton RK. Wisconsin Card Sorting Test. Odessa, Fla: Psychological
1986. Assessment Resources Inc; 1981.
17. Ackerly SS, Benton AL. Report of a case of bilateral frontal lobe de- 52. Jastak S, Wilkinson GS. Wide Range Achievement Test-Revised.
fect. Res Publ Assoc Res Nerv Ment Dis. 1947;27:479-504. Wilmington, Del: Jastak Associates Inc; 1984.
18. Russell WR. Brain\s=b\Memory\s=b\Learning.Oxford, England: Clarendon 53. Hogan R. Development of an empathy scale. J Consult Clin Psychol.
Press; 1959. 1969;33:307-316.
19. Ackerly SS. A case of perinatal bilateral frontal lobe defect observed 54. Kohlberg L. Stage and sequence: the cognitive-developmental ap-
for thirty years. In: Warren JM, Akert K, eds. The Frontal Granular Cortex and proach to socialization. In: Goslin DA, ed. Handbook of Socialization: The-
Behavior. New York, NY: McGraw-Hill International Book Co; 1964:192\x=req-\ ory and Practice. New York, NY: Rand McNally & Co; 1969.
218. 55. Damasio H, Damasio AR. Lesion Localization in Neuropsychology.
20. Benton AL. Prefrontal injury and behavior in children. Dev Neuropsy- New York, NY: Oxford University Press; 1989.
chol. 1991;7:275-281. 56. Eslinger PJ, Grattan LM. Constructions of frontal- and parietal\x=req-\
21. Price BH, Doffner KR, Stowe RM, Mesulam M-M. The comportmental damaged patients after an organizational strategy. Clin Neuropsychol. 1990;
learning disabilities of early frontal lobe damage. Brain. 1990;113:1383\x=req-\ 4:286.
1394. 57. Benton AL. Child neuropsychology: retrospect and prospect. In: Costa
22. Kennard MA, Fulton JF. Age and reorganization of central nervous L, Spreen O, eds. Studies in Neuropsychology: Selected Papers of Arthur
system. Mt Sinai J Med. 1942;9:594-600. Benton. New York, NY: Oxford University Press; 1985:274-294.
23. Simons D, Finger S. Some factors affecting recovery after brain dam- 58. Yakovlev PI, Lecours AR. The myelogenetic cycles of regional matu-
age early in life. In: Finger S, Alini CR, eds. Early Brain Damage: Neurobi- ration of the brain. In: Minkowski A, ed. Regional Development of the Brain
ology and Behavior. Orlando, Fla: Academic Press Inc; 1984;2:327-347. in Early Lobe. New York, NY: Basil Blackwell Publisher; 1967:3-70.
24. Kolb B. Brain development, plasticity, and behavior. Am Psychol. 59. St James Roberts I. Neurological plasticity, recovery from brain insult,
1989;44:1203-1212. and child development. Ad Child Dev Behav. 1979;14:253-319.
25. Stein DG, Rosen JJ, Butters N. Plasticity and Recovery of Function in the 60. Huttenlocher PR. Morphometric study of human cerebral cortex de-
Central Nervous System. New York, NY: Academic Press Inc; 1974. velopment. Neuropsychologia. 1990;28:517-527.
26. Passler MA, Isaac W, Hynd G. Neuropsychological development of 61. Goldman PS. Functional development of the prefrontal cortex in
behavior attributed to frontal lobe functioning in children. Dev Neuropsy- early life and the problem of neuronal plasticity. Exp Neurol. 1971;32:
chol. 1985;1:349-370. 366-387.
27. Chelune GJ, Thompson LL. Evaluation of the general sensitivity of the 62. Grattan LM, Eslinger PJ. Higher cognition and social behavior: changes
Wisconsin Card Sorting Test among younger and older children. Dev Neu- in cognitive flexibility and empathy after cerebral lesions. Neuropsychology.
ropsychol. 1987;3:81-89. 1989;3:175-185.
28. Welsh MC, Pennington BF. Assessing frontal lobe functioning in chil- 63. Grattan LM, Eslinger PJ. Differential representation of deficits in cog-
dren. Dev Neuropsychol. 1988;4:199-230. nitive flexibility and interpersonal behavior within the frontal lobe. J Clin Exp
29. Diamond A, Doar B. The performance of human infants on a measure Neuropsychol. 1990;12:79.
of frontal cortex function, the delayed response task. Dev Psychobiol. 1989; 64. Goldman PS, Galkin TW. Prenatal removal of frontal association cor-
22:271-294. tex in the fetal rhesus monkey: anatomical and functional consequences in
30. Levin HS, Culhane KA, Hartmann J, et al. Developmental changes in postnatal life. Brain Res. 1978;152:451-485.
performance on tests of purported frontal lobe functioning. Dev Neuropsy- 65. Kolb B, Gibb R. Anatomical correlates of behavioral change after neo-
chol. 1991;7:377-395. natal prefrontal lesions in rats. In: Uylings HBM, van Eden, De Bruin JPC, Corner
31. Finger S. Brain damage, development and behavior: early findings. MA, Feenstra MGP, eds. Progress in Brain Research. Amsterdam, the Nether-
Dev Neuropsychol. 1991;7:261-274. lands: Elsevier Science Publishers; 1990;85:241-256.
32. Chelune GJ, Edwards P. Early brain lesions: ontogenetic-

DownloadedViewFrom:
publicationhttp://jamanetwork.com/
stats by a Penn State Milton S Hershey Med Ctr User on 09/09/2014