Literature Review

The Influence of Frontal Lobe Tumors and Surgical Treatment on Advanced Cognitive
Functions
Shengyu Fang1, Yinyan Wang2, Tao Jiang1-3

Key words Brain cognitive functions affect patient quality of life. The frontal lobe plays a
- Brain tumor crucial role in advanced cognitive functions, including executive function, meta-
- Cognitive function
- Frontal lobe
cognition, decision-making, memory, emotion, and language. Therefore, frontal
- Surgical treatment tumors can lead to serious cognitive impairments. Currently, neurosurgical
treatment is the primary method to treat brain tumors; however, the effects of the
Abbreviations and Acronyms
surgical treatments are difficult to predict or control. The treatment may both
ACC: Anterior cingulate cortex
DLPFC: Dorsal lateral prefrontal cortex resolve the effects of the tumor to improve cognitive function or cause perma-
IFG: Interior frontal gyrus nent disabilities resulting from damage to healthy functional brain tissue. Pre-
LGG: Low-grade glioma vious studies have focused on the influence of frontal lesions and surgical
From the 1Beijing Neurosurgical Institute, Capital Medical
treatments on patient cognitive function. Here, we review cognitive impairment
University, Beijing; 2Department of Neurosurgery, Beijing caused by frontal lobe brain tumors.
Tiantan Hospital, Capital Medical University, Beijing; and
3
Beijing Institute for Brain Disorders, Brain Tumor Center,
Beijing, China
To whom correspondence should be addressed: tumors published between January 1978 medial frontal lobe results in an apathetic
Tao Jiang, M.D., Ph.D. and February 2016. A search of the state and a decrease in self-motivated ac-
[E-mail: [email protected]] PubMed database was conducted using tivities.4 Another recent report revealed
Shengyu Fang and Yinyan Wang are coefirst authors. the terms “frontal lobe,” “cognitive func- that not only the DLPFC but also
Citation: World Neurosurg. (2016) 91:340-346.
tion,” and “tumor.” The exclusion criteria subcortical structures including the
http://dx.doi.org/10.1016/j.wneu.2016.04.006 for publications were: 1) manuscripts not fronto-parietal circuit influence attention.5
Journal homepage: www.WORLDNEUROSURGERY.org in English, 2) manuscripts describing an- Meta-cognition is the capacity to eval-
Available online: www.sciencedirect.com
imal studies, and 3) studies that solely uate the success or failure of one’s own
focused on motor functions. A total of 97 cognitive processes.6 In other words, it
1878-8750/$ - see front matter ª 2016 Elsevier Inc. All
rights reserved. articles are included and are cited as ref- facilitates self-awareness and the self-
erences in this review. monitoring of cognitive activities.7
Patients with middle and lateral frontal
lobe damage exhibit meta-cognition defi-
Technological advances in brain tumor FRONTAL LOBE INVOLVEMENT IN cits. Transcranial magnetic stimulation
treatment have resulted in better patient ADVANCED COGNITIVE FUNCTION studies have shown that the DLPFC is also
prognoses and prolonged patient survival.
The frontal lobe appears relatively late in involved in meta-cognition.8,9 Functional
Furthermore, survival qualities have
brain development and is required for magnetic resonance imaging studies
become a useful index for the assessment
advanced cognitive functions, including indicate that multiple brain regions are
of treatment effects. Cognitive functions
executive function, meta-cognition, deci- involved in meta-cognition, including the
are an important standard for evaluating
sion-making, memory, emotion, and lan- DLPFC, middle prefrontal lobe, and
patient quality of life after treatment.
guage.1 Executive function facilitates the cingulate cortex.10,11
Indeed, numerous studies have investi-
generation and adaptation of a variety of Decision-making has a significant
gated the impact of frontal lobe tumors
behaviors. Although executive function impact on quality of life. Previous reports
and their surgical treatment on advanced
traditionally was believed to be have suggested that the bilateral prefrontal
cognitive functions. In this review, we
associated selectively with the frontal cortex as well as the bilateral orbitofrontal
summarize the available data on frontal
lobes, recent reports indicate that circuits lobe play an important role in decision-
lobe tumors and the effects of surgical
between the frontal lobe and other brain making.12-14
treatment on cognitive functions. This
regions also are involved in executive On the basis of function, memory can be
knowledge has the potential to improve
functions.2,3 The orbitofrontal lobe has divided into 2 subtypes: working memory
the ability of neurosurgeons to preserve
been associated with behavioral- and episodic memory.15 Previous studies
advanced cognitive brain functions by
emotional self-regulation, whereas the have shown that the prefrontal lobe, in
influencing their surgical decisions.
The present study reviewed original dorsal lateral prefrontal cortex (DLPFC) particular the DLPFC, plays an important
articles and literature reviews related to has been implicated primarily in attention, role in working memory.16,17 Many recent
cognitive impairment and frontal lobe information generation, organization, and studies also have found that the superior
planning. In addition, damage to the longitudinal fascicle, especially in the

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 LITERATURE REVIEW
SHENGYU FANG ET AL. FRONTAL LOBE TUMORS0 AFFECT ON COGNITIVE FUNCTIONS

context of the fronto-parietal pathway, is method to demonstrate that the ventral magnetic resonance imaging.46 Therefore,
crucial to the performance of working premotor cortex rather than the Broca area it is necessary for neurosurgeons to be
memory tasks.18-21 There also exist bilateral affect speech arrest, and that the IFG aware of the types of cognitive
differences in the neuroanatomical corre- rather than the area of Wernicke can affect impairments that can be caused by frontal
lates of working memory: interestingly, the anomia or paraphasia. This study also tumors.
left prefrontal lobe and its circuits are revealed the role of a supramodal network,
thought to be responsible for memory consisting of the frontal operculum, Impairment of Executive Function
encoding, whereas the right prefrontal lobe DLPFC, and posterior superior temporal Frontal tumors, in particular those in the
is thought to be responsible for memory cortex, in mediating language function. DLPFC, produce decreases in executive
recall.22 Patients with frontal lobe The fiber fascicles also participate in function.47 Among patients with LGGs or
impairments show poor performance on language function. On the basis of diffu- high-grade gliomas, executive response
episodic memory tests compared with sion tensor imaging, researchers have time is always prolonged, which suggests
healthy individuals.23 Some researchers identified a third subtype of the superior that frontal lobe gliomas also impair
believe that working memory is related to longitudinal fasciculus, which connects attention. Notably, greater glioma grades
decision-making; however, research on a the posterior IFG to the supramarginal have been associated with the severity of
component of working memory known as gyrus, in the phonological aspect of lin- attention impairment in patients.48
the phonological loop24 has indicated that guistic function.35 In a series of cortical Previous studies have shown that the
there is no relationship between the and subcortical stimulation studies, ACC also participates in executive
phonological loop and decision-making. Duffau et al.36-39 reported that many function.49,50 An evaluation of the
Emotional cognition refers to emotional components of the fronto-parietal circuit, executive functions of 2 patients with
self-awareness and the awareness of others’ which connects the frontal lobe to gliomas invading the frontal lobe
emotions. It includes intention, expecta- different parietal lobe sites, are involved in revealed that although single ACC lesions
tion, thinking, and faith.25 Emotional phonological and semantic functions. did not impair intelligence, memory,
cognition is thus part of the theory of Furthermore, Hickok and Poeppel40,41 language, or executive function, lesions
mind or mentalizing. Traditionally, the proposed the dual-route theory, which of the bilateral ACC produced mild
frontal lobe was considered to be less purports the involvement of the ventral decline in the function of the anterior
related to emotion than the anterior route and dorsal stream in language attention network.51 Because both
cingulate cortex (ACC), limbic system, or functions. The ventral route including A1, gliomas had invaded the frontal lobe in
bilateral temporal lobes26; however, many part of the IFG, and the anterior temporal this study, however, the patients also
studies on emotion have revealed that gyrus is responsible for semantic pro- showed executive dysfunction. These
impairment of the frontal lobe and cessing and comprehension. The dorsal findings suggest that although the ACC
especially the ventromedial prefrontal route including A1, the premotor cortex, does not play a core role in executive
cortex can negatively affect emotional the prefrontal cortex, and the planum function, it may synthesize cognitive
cognition.27 Many researchers also have temprolate is responsible for language processing and autonomic function in
identified roles for white matter structures perception. Recent studies also have the guidance of behavior. However, the
(e.g., the uncinate fasciculus) in the identified significant white matter areas of frontal lobes seem to play a larger role in
amygdala-ventromedial-prefrontal cortex the frontal lobe involved in speech executive function than the ACC.51
circuit in emotion.28,29 including the left frontal aslant tract,
Language cognition can be divided into 3 which connects the supplementary motor Meta-Cognitive Function Impairment
components: phonology, syntax, and sem- area and the Broca area.20,42,43 Frontal tumors can impair patient self-
anteme.30,31 The inferior frontal gyrus (IFG) awareness, which is a component of
in the dominant hemisphere is crucial for Frontal Tumors Impair Cognitive Function meta-cognition. Only a few reports,
verb generation but is not involved in Frontal lobe tumors have the potential to however, have described a mechanism for
semantic retrieval.32 Corticosubcortical damage a variety of cognitive functions the impairment of meta-cognition by
electrical stimulation is a useful method for (Figure 1). Mild cognitive impairment frontal tumors. One previous study re-
the evaluation of language function during attributable to frontal tumors is difficult ported the case of a 60-year-old woman
surgical procedures. Duffau et al.33 used for both patients and clinicians to detect. with multiple glioblastomas invading the
this method to identify differences in For this reason, epilepsy is usually the first prefrontal cortex. The patient’s primary
language performance during the symptom in patients with low-grade gli- symptom was pathological laughing; she
stimulation of different regions in the oma (LGG).44 In general, changes in would laugh every 3 minutes regardless of
dominant hemisphere and found that cognitive function precede the onset of whether or not it was relevant to her
stimulation of the ventral premotor cortex epilepsy. Conversely, if a patient with an environment. Moreover, although the
impaired word pronunciation. In contrast, LGG experiences changes in cognitive patient was unable to consciously control
dorsal premotor cortex stimulation resulted function, it indicates that the tumor is at her laughter, she did feel a sense of
in anomia. Stimulation of the pars an early stage.45 Studies have shown that embarrassment and a desire to control it.
opercularis and DLPFC induced speech assessing changes in cognition for the That is, although emotion and self-
arrest and semantic paraphasia, diagnosis of recurrent glioma is more control were not impaired, the patient’s
respectively. Tate et al.34 recently used this sensitive than computed tomography or self-awareness was damaged. After

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 LITERATURE REVIEW
SHENGYU FANG ET AL. FRONTAL LOBE TUMORS0 AFFECT ON COGNITIVE FUNCTIONS

Figure 1. Brain regions and corresponding symptoms related to DLPFC, dorsal lateral prefrontal cortex; IFG, inferior frontal
brain tumors in these regions. ACC, anterior cingulate cortex; gyrus.

surgical tumor removal, the pathological Memory Impairment addition, patients with frontal cortex
laughter resolved.52 In a study of 11 patients with left-sided gliomas demonstrate difficulty with the
frontal glioma (7 with gliomas located in accurate recognition of angry faces.57 A
the left IFG), working memory, assessed previous study reported that tumors in the
Decision-Making Impairment via the Digit Span Test, a traditional frontal lobe, ACC, and temporal lobe
Frontal lobe gliomas impair decision- measurement for working memory, was induce different emotional impairments.61
making, especially with regard to reaction impaired relative to control subjects. It Campanella et al.62 summarized 71 brain
time. The Iowa Gambling Task and Cam- was concluded that left frontal lobe gli- tumor patients’ pre- and postoperative
bridge Gambling Task have been used to omas damage working memory, likely due emotion test performances and concluded
evaluate patients’ decision-making ability to an impact on the phonological loop that tumors in the medial right prefrontal
in clinical trials. Clark et al.53 tested 46 located in the left IFG.54-57 Accordingly, lobe induce alexithymia, whereas tumors
patients with frontal lobe lesions (24/46 studies have shown that the phonological in the right lateral prefrontal cortex impair
right frontal lobe gliomas), however, and loop is a significant component of work- self-inhibition. Herbet et al.63 found that
concluded that the Iowa Gambling Task ing memory involved in both phonological gliomas in the right IFG damaged
was more sensitive than the Cambridge storage and the articulatory rehearsal patients’ mirror networks and decreased
Gamble Task for the detection of process. Indeed, left IFG damage impairs mentalizing. Subsequently, Herbet et al.64
impairments. Mattavelli et al.13 also used the articulatory rehearsal process in confirmed the disruption of empathy by
the Iowa Gambling Task successfully to patients.58,59 gliomas affecting the uncinate fasciculus or
evaluate 22 patients with left frontal LGGs the inferior fronto-occipital circuitry. Park
and concluded that dominant hemisphere Emotional Impairment et al.65 studied patients with intracranial
gliomas impair decision-making. A main Frontal tumors impair many aspects of arachnoids cysts and found that cysts
conclusion from these 2 studies was that emotion, and damage to different areas can located in the left frontal cortex were likely
patients with frontal lobe gliomas require produce variable emotional cognitive dys- to produce anxiety; indeed, the focal mass
more time to understand their own illness functions. Using the facial expression rather than the cysts themselves led to
and treatment, such that clinicians should recognition test, Botvinick et al.60 observed changes in patient mood as the result of
take more time to explain treatment that patients with ACC gliomas were effects on cerebral blood supply.
options and risks in these cases.13 unable to accurately recognize fear. In Unfortunately, there is a dearth of

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 LITERATURE REVIEW
SHENGYU FANG ET AL. FRONTAL LOBE TUMORS0 AFFECT ON COGNITIVE FUNCTIONS

additional direct evidence in support of the and the third circuit includes the left mentalizing, picture-naming, and verbal-
effect of frontal tumor masses on patient ventral, frontal, and posterior temporal visual tasks50 to monitor executive
emotions. In an autopsy study of patients cortices. When tumors grow into the left function, and the 2-back task20 to monitor
with depression, however, Drevets66 motor cortex, the first circuit is spatial working memory. Nonetheless, the
observed significant decreases in the overactivated, whereas the second and exploration of additional cognitive tests is
volume, thickness, and numbers of glial third circuits are overactivated by tumors required to optimize the monitoring of
cells in the frontal cortices. in the left inferior frontal triangle pars. advanced cognitive functions during the
Overall, frontal tumors lead to left IFG removal of brain tissue.
Language Impairment reorganization, and neural circuit over- In the postoperative stage, brain edema,
Frontal tumors damage language in 2 activation is a primary reason for compre- hemorrhage, or other complications can
ways: expression and syntax understand- hensive language dysfunction. create severe secondary and even life-
ing. Patients with tumors in the Broca threatening impairments. Therefore, it is
area exhibit different degrees of motor Default Mode Network Changing crucial for each neurosurgeon to predict
aphasia, and the mirror areas opposite to Even in the resting state, transmission intraoperative damage and treatment ef-
the Broca area in the dominant hemi- occurs between different brain regions. fects according to each patient’s situation.
sphere are forced to compensate.67 This This phenomenon is known as the default As mentioned previously, cognitive func-
compensation often is referred to as mode, and the pathways underlying this tion is an important criterion for the
functional plasticity, which occurs not phenomenon are known as default mode evaluation of patient quality of life.
only for the compensation of language networks. Upon reviewing studies of gli- Therefore, an understanding of how tu-
function but also for the compensation omas located in the dominant hemi- mor resection can potentially affect
of motor, sensory, and other sphere, we found that both LGGs and cognitive function is essential for optimal
neurological functions. Despite years of high-grade gliomas have been reported frontal lobe tumor treatment.
research on the topic of functional to impact default mode networks. Indeed,
plasticity, no clear mechanism has been higher tumor grades have been associated Tumor Resection and the Risk of Cognitive
reported. Southwell et al.68 hypothesized with more severe default mode network Dysfunction
a relationship between the degree of functional decline76; however, only LGGs Meta-Cognitive Impairment. A patient who
functional plasticity and glioma grade have been documented to induce underwent frontal lobe astrocytoma resec-
and volume. Alternatively, Duffau69,70 default mode network hemisphere tion developed postoperative anarchic hand
proposed that functional plasticity lateralization.77 The mechanism for this syndrome.83 This rare injury is characterized
occurs proximal to the primary lesion phenomenon is unknown but may be by hand conflicting behaviors and makes
and subsequently in the ipsilateral related to tumor invasiveness or the behavioral performance appear strange
region and contralateral hemisphere if degree of tumor cell differentiation. (obvious hand conflict and confrontation
the recruited components are between disuse and competition).84
insufficient. In a study of 7 patients with Unfortunately, it is unclear why this
gliomas in the Broca area, 5 did not EFFECTS OF TUMOR RESECTION ON
complication occurs, and so it is not
exhibit motor aphasia, suggesting that COGNITIVE FUNCTION AND RECOVERY
known how to minimize the risk of
compensation was nonspecific in these Surgery is the treatment of choice for most postoperative anarchic hand syndrome
patients.71 Other studies have concluded intracranial tumors. Tumor resection can during tumor resection.
that patients with frontal tumors are resolve brain tissue lesions, relieve focal
more likely to experience anomic oppression, and prevent the invasion of Memory Impairment. Not all patients with
aphasia.43,49,72 normal brain tissue. For neurosurgeons, it frontal lobe tumors exhibit memory
Patients with frontal tumors show is a challenge to resect as much tumor as dysfunction, but surgery may increase the
decreased language fluency performance possible without affecting important func- likelihood of functional memory impair-
relative to both healthy individuals and in- tional regions.78 Despite increasingly ments. A 5-year follow-up study of 18 pa-
dividuals with tumors in other positions.49 advanced technological methods for the tients with frontal lobe neurocytomas
Left IFG tumors can result in difficulty protection of cognitive function demonstrated a marked decline in mem-
understanding complex sentences.73,74 (e.g., preoperative functional magnetic ory after tumor resection. In addition,
Kinno et al.75 reported that language resonance imaging, neuronavigation, resection-related memory impairments
comprehension dysfunction in patients awake surgeries, and electrical stimulation were exacerbated with age.85 The reason
can occur as the result of the damage of 3 mapping), peripheral tissue impairment is for the decline in memory was likely
neural circuits: the first circuit includes often unavoidable.79-82 In addition to the related to damage to the frontal cortex
the opercula or the triangular parts of the monitoring linguistic functions during and blocked fiber connections between
left IFG, left intraparietal sulcus, awake resection, we have explored the use the frontal and temporal lobes.86
presupplementary motor areas, right of a handful of tasks during direct cortical
frontal regions, and right temporal stimulation for the monitoring of Emotional Control Disabilities. After the
regions; the second circuit includes the advanced cognitive functions. For resection of ventral prefrontal cortex tu-
left lateral premotor cortex, left angular instance, we have used the “reading the mors, patients are reported to experience
gyrus, lingual gyrus, and cerebellar nuclei; Mind in Eyes” task63 to monitor negative emotions such as anxiety,

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 LITERATURE REVIEW
SHENGYU FANG ET AL. FRONTAL LOBE TUMORS0 AFFECT ON COGNITIVE FUNCTIONS

depression, irritability, and fatigue.87 A CONCLUSION AND EXPECTATION 8. Pannu JK, Kaszniak AW, Rapcsak SZ. Meta-
memory for faces following frontal lobe damage.
previous analysis showed that these Frontal tumor location, volume, and J Int Neuropsychol Soc. 2005;11:668-676.
negative emotions were associated with morphology may induce different types and
damage to the heteromodals, which are a degrees of cognitive impairments. Several 9. Rounis E, Maniscalco B, Rothwell JC,
type of association cortex.88 Tumor studies have reported that alterations in
Passingham RE, Lau H. Theta-burst transcranial
magnetic stimulation to the prefrontal cortex
location and size can make it difficult to cognitive function can indicate the existence impairs metacognitive visual awareness. Cogn
avoid the loss of these structures during or recurrence of frontal lobe tumors. Neurosci. 2010;1:165-175.
surgery.89 As a result, tumor resection Cognitive symptoms, however, often are 10. Hoerold D, Pender NP, Robertson IH. Meta-
should be considered to negatively affect ignored by patients and doctors, cognitive and online error awareness deficits after
emotional control.87 especially in cases of mild manifestation.45 prefrontal cortex lesions. Neuropsychologia. 2013;51:
385-391.
Furthermore, unless symptoms are
improved after surgical resection, 11. Kikyo H, Ohki K, Miyashita Y. Neural correlates
Impairment of Language Function. Some
clinicians have a limited ability to attribute for feeling-of-knowing: an fMRI parametric anal-
patients who have undergone left frontal ysis. Neuron. 2002;36:177-186.
functional alterations to the lesion. The
lobe glioma resection have experienced
present review thus offers a list of the 12. Elliott R, Dolan RJ, Frith CD. Dissociable func-
language expression disabilities. Using
cognitive functions that should be assessed tions in the medial and lateral orbitofrontal cor-
damage function reconstruction technol- tex: evidence from human neuroimaging studies.
before and after surgery for frontal lesions.
ogy, we determined that a glioma resec- Cereb Cortex. 2000;10:308-317.
In the future, the identification of simple
tion resulting in language expression
and more sensitive diagnostic methods for 13. Mattavelli G, Casarotti A, Forgiarini M, Riva M,
disability had damaged a vast majority of
the evaluation of cognitive function during Bello L, Papagno C. Decision-making abilities in
the dorsal left frontal lobe and associated patients with frontal low-grade glioma.
surgery can improve postsurgical outcomes
white matter.90 In another study, J Neurooncol. 2012;110:59-67.
of tumor resection. In addition, clinical
Kinoshita et al.67 used diffusion tensor
trials exploring the impact of frontal 14. Shallice T, Burgess PW. Deficits in strategy
imaging and intraoperative cortical application following frontal lobe damage in man.
tumors on cognitive function are required.
stimulation to confirm that the frontal Brain. 1991;114(Pt 2):727-741.
The increasingly rapid development of
aslant tract plays a role in speech motor
imaging technologies will provide new 15. Rubin DC. The basic-systems model of episodic
control. Impairment the frontal aslant memory. Perspect Psychol Sci. 2006;1:277-311.
evidences to improve our understanding of
tract during tumor resection may
how frontal tumors impair advanced 16. McCarthy G, Blamire AM, Puce A, Nobre AC,
therefore be a reason for intractable
cognitive functions.96,97 Bloch G, Hyder F, et al. Functional magnetic
language expression disability.91 resonance imaging of human prefrontal cortex
activation during a spatial working memory task.
REFERENCES Proc Natl Acad Sci U S A. 1994;91:8690-8694.
1. Stuss DT, Alexander MP. Executive functions and
Tumor Resection for the Recovery of 17. Petrides M, Alivisatos B, Evans AC, Meyer E.
the frontal lobes: a conceptual view. Psychol Res.
Cognitive Functions 2000;63:289-298. Dissociation of human mid-dorsolateral from
Although tumor removal has a high like- posterior dorsolateral frontal cortex in memory
2. Kaufmann L, Koppelstaetter F, Delazer M, processing. Proc Natl Acad Sci U S A. 1993;90:
lihood of damaging cognitive function to 873-877.
Siedentopf C, Rhomberg P, Golaszewski S, et al.
some degree, surgery also can be per- Neural correlates of distance and congruity effects
formed to minimize cognitive impact or in a numerical Stroop task: an event-related fMRI 18. Belayachi S, Majerus S, Gendolla G, Salmon E,
help recover cognitive function, especially study. Neuroimage. 2005;25:888-898. Peters F, Van der Linden M. Are the carrot and the
stick the two sides of same coin? A neural exam-
in patients with language dysfunction. In 3. Wagner G, Koch K, Reichenbach JR, Sauer H, ination of approach/avoidance motivation during
patients with frontal lobe LGGs, language Schlosser RG. The special involvement of the cognitive performance. Behav Brain Res. 2015;293:
functions should recover to preoperative rostrolateral prefrontal cortex in planning abili- 217-226.
ties: an event-related fMRI study with the Tower
baselines within 1e2 weeks after tumor 19. Brooks JO 3rd, Vizueta N, Penfold C,
of London paradigm. Neuropsychologia. 2006;44:
resection.92 If the tumor volume is too 2337-2347. Townsend JD, Bookheimer SY, Altshuler LL. Pre-
large or cannot be removed in a single frontal hypoactivation during working memory in
4. Seniow J. Executive dysfunctions and frontal bipolar II depression. Psychol Med. 2015;45:
operation, excision in stages can be used
syndromes. Front Neurol Neurosci. 2012;30:50-53. 1731-1740.
to prevent language function from being
seriously affected.93 Surgical treatments 5. Arnsten AF, Rubia K. Neurobiological circuits 20. Kinoshita M, Nakajima R, Shinohara H,
have also been reported to improve the regulating attention, cognitive control, motiva- Miyashita K, Tanaka S, Okita H, et al. Chronic
tion, and emotion: disruptions in neuro- spatial working memory deficit associated with
decision-making abilities of patients with developmental psychiatric disorders. J Am Acad the superior longitudinal fasciculus: a study using
frontal lobe gliomas.13 Total functional Child Adolesc Psychiatry. 2012;51:356-367. voxel-based lesion-symptom mapping and intra-
recovery, however, always should be operative direct stimulation in right prefrontal
6. Fleming SM, Ryu J, Golfinos JG, Blackmon KE. glioma surgery [e-pub ahead of print]. J Neurosurg.
considered to be affected by the patient’s Domain-specific impairment in metacognitive 2016. http://dx.doi.org/10.3171/2015.10.JNS1591.
postoperative health and rehabilitation. accuracy following anterior prefrontal lesions.
Indeed, rehabilitative efforts such as Brain. 2014;137:2811-2822. 21. Yang J, Yu Y, Kunita A, Huang Q, Wu J,
Sawamoto N, et al. Tactile priming modulates the
training can significantly improve patient
7. Toglia J, Kirk U. Understanding awareness deficits activation of the fronto-parietal circuit during
memory and language skills following following brain injury. NeuroRehabilitation. 2000;15: tactile angle match and non-match processing: an
tumor resection.94,95 57-70. fMRI study. Front Hum Neurosci. 2014;8:926.

344 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.04.006

 LITERATURE REVIEW
SHENGYU FANG ET AL. FRONTAL LOBE TUMORS0 AFFECT ON COGNITIVE FUNCTIONS

22. Tulving E, Kapur S, Craik FI, Moscovitch M, premotor cortex in language: a study using 50. Plaza M, Gatignol P, Cohen H, Berger B,
Houle S. Hemispheric encoding/retrieval asym- intraoperative functional mapping in awake pa- Duffau H. A discrete area within the left dorso-
metry in episodic memory: positron emission to- tients. Neuroimage. 2003;20:1903-1914. lateral prefrontal cortex involved in visual-verbal
mography findings. Proc Natl Acad Sci U S A. 1994; incongruence judgment. Cereb Cortex. 2008;18:
91:2016-2020. 37. Duffau H, Capelle L, Denvil D, Sichez N, 1253-1259.
Gatignol P, Taillandier L, et al. Usefulness of
23. Andres P, Van der Linden M, Parmentier FB. intraoperative electrical subcortical mapping dur- 51. Baird A, Dewar BK, Critchley H, Gilbert SJ,
Directed forgetting in frontal patients’ episodic ing surgery for low-grade gliomas located within Dolan RJ, Cipolotti L. Cognitive functioning after
recall. Neuropsychologia. 2007;45:1355-1362. eloquent brain regions: functional results in a medial frontal lobe damage including the anterior
consecutive series of 103 patients. J Neurosurg. cingulate cortex: a preliminary investigation. Brain
24. Gozzi M, Papagno C. Is short-term memory 2003;98:764-778. Cogn. 2006;60:166-175.
involved in decision making? Evidence from a
short-term memory patient. J Neuropsychol. 2007;1: 38. Duffau H, Gatignol P, Denvil D, Lopes M, 52. Tsutsumi S, Yasumoto Y, Ito M. Pathological
115-129. Capelle L. The articulatory loop: study of the laughter caused by frontal glioblastoma: case
subcortical connectivity by electrostimulation. report. Neurol Med Chir (Tokyo). 2008;48:307-310.
25. Eslinger PJ. Neurological and neuropsychological Neuroreport. 2003;14:2005-2008.
bases of empathy. Eur Neurol. 1998;39:193-199.
53. Clark L, Manes F, Antoun N, Sahakian BJ,
39. Duffau H, Gatignol P, Mandonnet E, Peruzzi P,
26. Almairac F, Herbet G, Moritz-Gasser S, de Robbins TW. The contributions of lesion laterality
Tzourio-Mazoyer N, Capelle L. New insights into
Champfleur NM, Duffau H. The left inferior and lesion volume to decision-making impairment
the anatomo-functional connectivity of the
fronto-occipital fasciculus subserves language following frontal lobe damage. Neuropsychologia.
semantic system: a study using cortico-subcortical
semantics: a multilevel lesion study. Brain Struct 2003;41:1474-1483.
electrostimulations. Brain. 2005;128:797-810.
Funct. 2015;220:1983-1995.
54. Funahashi S. Prefrontal cortex and working
40. Hickok G, Poeppel D. The cortical organization of
27. Shamay-Tsoory SG, Tomer R, Goldsher D, memory processes. Neuroscience. 2006;139:251-261.
speech processing. Nat Rev Neurosci. 2007;8:
Berger BD, Aharon-Peretz J. Impairment in 393-402.
cognitive and affective empathy in patients with 55. Mu YG, Huang LJ, Li SY, Ke C, Chen Y, Jin Y, et al.
brain lesions: anatomical and cognitive correlates. 41. Hickok G, Poeppel D. Dorsal and ventral streams: Working memory and the identification of facial
J Clin Exp Neuropsychol. 2004;26:1113-1127. a framework for understanding aspects of the expression in patients with left frontal glioma.
functional anatomy of language. Cognition. 2004; Neuro Oncol. 2012;14(suppl 4):iv81-iv89.
28. Isaac L, Main KL, Soman S, Gotlib IH, Furst AJ,
92:67-99.
Kinoshita LM, et al. The impact of depression on 56. Smith EE, Jonides J. Working memory: a view
Veterans with PTSD and traumatic brain injury: a from neuroimaging. Cogn Psychol. 1997;33:5-42.
42. Kemerdere R, de Champfleur NM, Deverdun J,
diffusion tensor imaging study. Biol Psychol. 2015;
Cochereau J, Moritz-Gasser S, Herbet G, et al.
105:20-28.
Role of the left frontal aslant tract in stuttering: a 57. Woodward TS, Cairo TA, Ruff CC, Takane Y,
brain stimulation and tractographic study. Hunter MA, Ngan ET. Functional connectivity re-
29. Sobhani M, Baker L, Martins B, Tuvblad C, Aziz-
J Neurol. 2016;263:157-167. veals load dependent neural systems underlying
Zadeh L. Psychopathic traits modulate micro-
encoding and maintenance in verbal working
structural integrity of right uncinate fasciculus in a
43. Vassal F, Boutet C, Lemaire JJ, Nuti C. New memory. Neuroscience. 2006;139:317-325.
community population. Neuroimage Clin. 2015;8:
insights into the functional significance of the
32-38.
frontal aslant tract: an anatomo-functional study 58. Baddeley A. Working memory: looking back and
using intraoperative electrical stimulations com- looking forward. Nat Rev Neurosci. 2003;4:829-839.
30. Alexander MP, Stuss DT. Disorders of frontal lobe
bined with diffusion tensor imaging-based fiber
functioning. Semin Neurol. 2000;20:427-437.
tracking. Br J Neurosurg. 2014;28:685-687. 59. Muller NG, Knight RT. The functional neuro-
31. Poldrack RA, Wagner AD, Prull MW, Desmond JE, anatomy of working memory: contributions of
Glover GH, Gabrieli JD. Functional specialization 44. You G, Sha ZY, Yan W, Zhang W, Wang YZ, human brain lesion studies. Neuroscience. 2006;139:
for semantic and phonological processing in the Li SW, et al. Seizure characteristics and outcomes 51-58.
left inferior prefrontal cortex. Neuroimage. 1999;10: in 508 Chinese adult patients undergoing primary
15-35. resection of low-grade gliomas: a clinicopatho-
60. Botvinick MM, Braver TS, Barch DM, Carter CS,
logical study. Neuro Oncol. 2012;14:230-241.
Cohen JD. Conflict monitoring and cognitive
32. Thompson-Schill SL, Swick D, Farah MJ, control. Psychol Rev. 2001;108:624-652.
D’Esposito M, Kan IP, Knight RT. Verb generation 45. Ek L, Almkvist O, Wiberg MK, Stragliotto G,
in patients with focal frontal lesions: a neuropsy- Smits A. Early cognitive impairment in a subset of
61. Gu X, Gao Z, Wang X, Liu X, Knight RT, Hof PR,
chological test of neuroimaging findings. Proc Natl patients with presumed low-grade glioma. Neuro-
et al. Anterior insular cortex is necessary for
Acad Sci U S A. 1998;95:15855-15860. case. 2010;16:503-511.
empathetic pain perception. Brain. 2012;135:
2726-2735.
33. Duffau H, Leroy M, Gatignol P. Cortico-subcor- 46. Meyers CA, Hess KR. Multifaceted end points in
tical organization of language networks in the brain tumor clinical trials: cognitive deterioration
precedes MRI progression. Neuro Oncol. 2003;5: 62. Campanella F, Shallice T, Ius T, Fabbro F,
right hemisphere: an electrostimulation study in
89-95. Skrap M. Impact of brain tumour location on
left-handers. Neuropsychologia. 2008;46:3197-3209.
emotion and personality: a voxel-based lesion-
47. Yin X, Han Y, Ge H, Xu W, Huang R, Zhang D, symptom mapping study on mentalization pro-
34. Tate MC, Herbet G, Moritz-Gasser S, Tate JE,
et al. Inferior frontal white matter asymmetry cesses. Brain. 2014;137:2532-2545.
Duffau H. Probabilistic map of critical functional
regions of the human cerebral cortex: Broca’s area correlates with executive control of attention. Hum
revisited. Brain. 2014;137:2773-2782. Brain Mapp. 2013;34:796-813. 63. Herbet G, Lafargue G, Moritz-Gasser S,
Bonnetblanc F, Duffau H. Interfering with the
35. Makris N, Kennedy DN, McInerney S, 48. Fang D, Jiang J, Sun X, Wang W, Dong N, Fu X, neural activity of mirror-related frontal areas im-
Sorensen AG, Wang R, Caviness VS Jr, et al. et al. Attention dysfunction of postoperative pa- pairs mentalistic inferences. Brain Struct Funct.
Segmentation of subcomponents within the su- tients with glioma. World J Surg Oncol. 2014;12:317. 2015;220:2159-2169.
perior longitudinal fascicle in humans: a quanti-
tative, in vivo, DT-MRI study. Cereb Cortex. 2005;15: 49. De Witte E, Van Hecke W, Dua G, De 64. Herbet G, Lafargue G, Moritz-Gasser S, Menjot de
854-869. Surgeloose D, Moens M, Marien P. Atypical ce- Champfleur N, Costi E, Bonnetblanc F, et al.
rebral language dominance in a right-handed A disconnection account of subjective empathy
36. Duffau H, Capelle L, Denvil D, Gatignol P, patient: an anatomoclinical study. Clin Neurol impairments in diffuse low-grade glioma patients.
Sichez N, Lopes M, et al. The role of dominant Neurosurg. 2014;117:12-21. Neuropsychologia. 2015;70:165-176.

WORLD NEUROSURGERY 91: 340-346, JULY 2016 www.WORLDNEUROSURGERY.org 345

 LITERATURE REVIEW
SHENGYU FANG ET AL. FRONTAL LOBE TUMORS0 AFFECT ON COGNITIVE FUNCTIONS

65. Park YS, Eom S, Shim KW, Kim DS. Neuro- 78. Schulder M, Maldjian JA, Liu WC, Holodny AI, patients. Implications for a neurology of depres-
cognitive and psychological profiles in pediatric Kalnin AT, Mun IK, et al. Functional image- sion. Arch Gen Psychiatry. 1981;38:1344-1354.
arachnoid cyst. Childs Nerv Syst. 2009;25:1071-1076. guided surgery of intracranial tumors located in
or near the sensorimotor cortex. J Neurosurg. 1998; 90. Campanella F, Crescentini C, Mussoni A,
66. Drevets WC. Functional neuroimaging studies of 89:412-418. Skrap M. Refractory semantic access dysphasia
depression: the anatomy of melancholia. Annu Rev resulting from resection of a left frontal glioma.
Med. 1998;49:341-361. 79. Amiez C, Kostopoulos P, Champod AS, Neurocase. 2013;19:27-35.
Collins DL, Doyon J, Del Maestro R, et al. Pre-
67. Kinoshita M, de Champfleur NM, Deverdun J, operative functional magnetic resonance imaging 91. Fujii M, Maesawa S, Motomura K, Futamura M,
Moritz-Gasser S, Herbet G, Duffau H. Role of assessment of higher-order cognitive function in Hayashi Y, Koba I, et al. Intraoperative subcortical
fronto-striatal tract and frontal aslant tract in patients undergoing surgery for brain tumors. mapping of a language-associated deep frontal
movement and speech: an axonal mapping study. J Neurosurg. 2008;108:258-268. tract connecting the superior frontal gyrus to
Brain Struct Funct. 2015;220:3399-3412. Broca’s area in the dominant hemisphere of pa-
80. Chang EF, Wang DD, Perry DW, Barbaro NM, tients with glioma. J Neurosurg. 2015;122:1390-1396.
68. Southwell DG, Hervey-Jumper SL, Perry DW,
Berger MS. Homotopic organization of essential
Berger MS. Intraoperative mapping during repeat 92. Chainay H, Francois-Xaxier A, Alexandre K,
language sites in right and bilateral cerebral
awake craniotomy reveals the functional plasticity Hugues D, Laurent C, Emmanuelle V, et al. Motor
hemispheric dominance. J Neurosurg. 2011;114:
of adult cortex [e-pub ahead of print]. J Neurosurg. and language deficits before and after surgical
893-902.
2015. http://dx.doi.org/10.3171/2015.5.JNS142833. resection of mesial frontal tumour. Clin Neurol
81. Kho KH, Rutten GJ, Leijten FS, van der Schaaf A, Neurosurg. 2009;111:39-46.
69. Duffau H. Brain plasticity and tumors. Adv Tech
Stand Neurosurg. 2008;33:3-33. van Rijen PC, Ramsey NF. Working memory def-
icits after resection of the dorsolateral prefrontal 93. Kumabe T, Nakasato N, Suzuki K, Sato K,
70. Duffau H. The “frontal syndrome” revisited: les- cortex predicted by functional magnetic resonance Sonoda Y, Kawagishi J, et al. Two-staged resection
sons from electrostimulation mapping studies. imaging and electrocortical stimulation mapping. of a left frontal astrocytoma involving the oper-
Cortex. 2012;48:120-131. Case report. J Neurosurg. 2007;106:501-505. culum and insula using intraoperative neuro-
physiological monitoringecase report. Neurol Med
71. Meyer PT, Sturz L, Schreckenberger M, 82. Wager M, Du Boisgueheneuc F, Pluchon C, Chir (Tokyo). 1998;38:503-507.
Spetzger U, Meyer GF, Setani KS, et al. Preoper- Bouyer C, Stal V, Bataille B, et al. Intraoperative
ative mapping of cortical language areas in adult monitoring of an aspect of executive functions: 94. Miotto EC, Balardin JB, Vieira G, Sato JR, Martin
brain tumour patients using PET and individual administration of the Stroop test in 9 adult pa- Mda G, Scaff M, et al. Right inferior frontal gyrus
non-normalised SPM analyses. Eur J Nucl Med Mol tients during awake surgery for resection of activation is associated with memory improve-
Imaging. 2003;30:951-960. frontal glioma. Neurosurgery. 2013;72: ment in patients with left frontal low-grade gli-
ons169-ons180 [discussion: ons180-ons181]. oma resection. PLoS One. 2014;9:e105987.
72. Briganti C, Sestieri C, Mattei PA, Esposito R,
Galzio RJ, Tartaro A, et al. Reorganization of 83. Bakheit AM, Brennan A, Gan P, Green H, 95. Miotto EC, Savage CR, Evans JJ, Wilson BA,
functional connectivity of the language network in Roberts S. Anarchic hand syndrome following Martin MG, Balardin JB, et al. Semantic strategy
patients with brain gliomas. AJNR Am J Neuroradiol. resection of a frontal lobe tumor. Neurocase. 2013; training increases memory performance and brain
2012;33:1983-1990. 19:36-40. activity in patients with prefrontal cortex lesions.
Clin Neurol Neurosurg. 2013;115:309-316.
73. Kinno R, Muragaki Y, Hori T, Maruyama T, 84. Sarva H, Deik A, Severt WL. Pathophysiology and
Kawamura M, Sakai KL. Agrammatic compre- treatment of alien hand syndrome. Tremor Other 96. Duffau H. Awake surgery for nonlanguage map-
hension caused by a glioma in the left frontal Hyperkinet Mov (N Y). 2014;4:241. ping. Neurosurgery. 2010;66:523-528 [discussion:
cortex. Brain Lang. 2009;110:71-80. 528-529].
85. Shi ZF, Sun DL, Song JP, Yao Y, Mao Y. Emotion
74. Mohr JP, Pessin MS, Finkelstein S, 97. Wang X, Wang YY, Jiang T, Wang YZ, Wu CX.
and cognitive function assessment of patients
Funkenstein HH, Duncan GW, Davis KR. Broca Direct evidence of the left caudate’s role in bilin-
with central neurocytoma resection through
aphasia: pathologic and clinical. Neurology. 1978; gual control: an intra-operative electrical stimu-
transcortical frontal approach: a 5-year post-
28:311-324. lation study. Neurocase. 2013;19:462-469.
operative follow-up study. Chin Med J (Engl). 2011;
124:2593-2598.
75. Kinno R, Ohta S, Muragaki Y, Maruyama T,
Sakai KL. Differential reorganization of three
86. Williams R. The human connectome: just another Conflict of interest statement: The authors declare that the
syntax-related networks induced by a left frontal
glioma. Can J Neurol Sci. 2014;137:1193-1212. ’ome? Lancet Neurol. 2010;9:238-239. article content was composed in the absence of any
commercial or financial relationships that could be construed
76. Harris RJ, Bookheimer SY, Cloughesy TF, Kim HJ, 87. Irle E, Peper M, Wowra B, Kunze S. Mood as a potential conflict of interest.
Pope WB, Lai A, et al. Altered functional con- changes after surgery for tumors of the cerebral Received 20 November 2015; accepted 2 April 2016
nectivity of the default mode network in diffuse cortex. Arch Neurol. 1994;51:164-174.
Citation: World Neurosurg. (2016) 91:340-346.
gliomas measured with pseudo-resting state
88. Hyvarinen J. Regional distribution of functions in http://dx.doi.org/10.1016/j.wneu.2016.04.006
fMRI. J Neurooncol. 2014;116:373-379.
parietal association area 7 of the monkey. Brain Journal homepage: www.WORLDNEUROSURGERY.org
77. Esposito R, Mattei PA, Briganti C, Romani GL, Res. 1981;206:287-303.
Available online: www.sciencedirect.com
Tartaro A, Caulo M. Modifications of default-
mode network connectivity in patients with cere- 89. Ross ED, Rush AJ. Diagnosis and neuroanatom- 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All
bral glioma. PLoS One. 2012;7:e40231. ical correlates of depression in brain-damaged rights reserved.

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