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Impairments in proverb interpretation following focal frontal
lobe lesions
$
Patrick Murphy
a
, Tim Shallice
b,c
, Gail Robinson
a,d
, Sarah E. MacPherson
a,e
,
Martha Turner
a,b
, Katherine Woollett
a,b
, Marco Bozzali
g
, Lisa Cipolotti
a,f,
n
a
National Hospital for Neurology and Neurosurgery, Box 37 Queen Square, London WC1N 3BG, UK
b
Institute of Cognitive Neuroscience, University College, London, UK
c
International School for Advanced Studies (SISSA), Trieste, Italy
d
School of Psychology, University of Queensland, St. Lucia, Brisbane, Australia
e
Department of Psychology, University of Edinburgh, Scotland, UK
f
Dipartimento di Psicologia, University of Palermo, Italy
g
Neuroimaging Laboratory, Santa Lucia Foundation, Rome 00179, Italy
article info
Article history:
Received 24 October 2012
Received in revised form
16 May 2013
Accepted 29 June 2013
Available online 11 July 2013
Keywords:
PFC
Proverbs
Executive function
Fluid intelligence
abstract
The proverb interpretation task (PIT) is often used in clinical settings to evaluate frontal “executive”
dysfunction. However, only a relatively small number of studies have investigated the relationship
between frontal lobe lesions and performance on the PIT. We compared 52 patients with unselected focal
frontal lobe lesions with 52 closely matched healthy controls on a proverb interpretation task.
Participants also completed a battery of neuropsychological tests, including a fluid intelligence task
(Raven’s Advanced Progressive Matrices). Lesions were firstly analysed according to a standard left/right
sub-division. Secondly, a finer-grained analysis compared the performance of patients with medial, left
lateral and right lateral lesions with healthy controls. Thirdly, a contrast of specific frontal subgroups
compared the performance of patients with medial lesions with patients with lateral frontal lesions. The
results showed that patients with left frontal lesions were significantly impaired on the PIT, while in
patients with right frontal lesions the impairments approached significance. Medial frontal patients were
the only frontal subgroup impaired on the PIT, relative to healthy controls and lateral frontal patients.
Interestingly, an error analysis indicated that a significantly higher number of concrete responses were
found in the left lateral subgroup compared to healthy controls. We found no correlation between scores
on the PIT and on the fluid intelligence task. Overall our results suggest that specific regions of the frontal
lobes contribute to the performance on the PIT.
& 2013 The Authors. Published by Elsevier Ltd. All rights reserved.
1. Introduction
1.1. Abstraction and the frontal lobes
The selective impairment of abstract thought processes as a
result of neurological disease has long been known of; at least
since such an impairment was held to reflect the loss of an abstract
attitude (Goldstein, 1936, 1944). More specifically, it has been
associated with lesions to the frontal cortex. Thus, Luria (1966,
p. 285) concluded that the difficulties of frontal patients with
abstraction emerged from their “lapse into irrelevant connections”
when constructing abstract mental representations. As far as
specific experimental results are concerned, Cicerone, Lazar, and
Shapiro (1983) reported an abstract thought impairment in a
group of frontal lobe patients who were shown to be unable to
generate hypotheses regarding the underlying patterns in a visual
learning task. Other studies showed that frontal lobe damage led
to difficulties in abstracting rules in temporal and spatial patterns
(Burgess & Shallice, 1996; Reverberi, Lavaroni, Gigli, Skrap, &
Shallice, 2005; Villa, Gainotti, De Bonis, & Marra, 1990). More
recently, using functional imaging, increased cerebral activity has
been observed in prefrontal areas alongside increased “chunking”
of specific visual sequences into abstract shapes during a spatial
memory task (Bor, Duncan, Wiseman, & Owen, 2003).
Analogical reasoning is a further aspect of abstract reasoning
that has also implicated the prefrontal cortex. In the non-verbal
domain, fMRI studies have shown increased PFC activation when
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/neuropsychologia
Neuropsychologia
0028-3932/$ - see front matter & 2013 The Authors. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.neuropsychologia.2013.06.029
☆
This is an open-access article distributed under the terms of the Creative
Commons Attribution-Non Commercial-No Derivative Works License, which per-
mits non-commercial use, distribution, and reproduction in any medium, provided
the original author and source are credited.
n
Corresponding author at: National Hospital for Neurology and Neurosurgery,
Box 37 Queen Square, London WC1N 3BG, United Kingdom.
Tel.: +44 20 3448 4793/44 20 3448 4793; fax: +44 20 7813 2516.
E-mail address: l.cipolotti@ucl.ac.uk (L. Cipolotti).
Neuropsychologia 51 (2013) 2075–2086
assessing the relationships between pairs of visual stimuli (Bunge,
Helskog, & Wendelken, 2009; Krawczyk, Michelle McClelland, &
Donovan, 2011), when deriving and applying rules from visual
patterns (Hampshire, Thompson, Duncan, & Owen, 2011; Watson
& Chatterjee, 2012) and when comparing the characteristics
shared by pairs of people ( Cho et al., 2010). In adolescents, a
higher level of cortical maturity in prefrontal areas was found to
reflect a better performance on a scene analogy task (Krawczyk
et al., 2010). In the verbal domain, imaging studies have shown
raised left prefrontal cortex activity when evaluating the relation-
ships between semantic relationships (Bunge, Wendelken, Badre,
& Wagner, 2005; Green, Fugelsang, Kraemer, Shamosh, & Dunbar,
2006; Green, Kraemer, Fugelsang, Gray, & Dunbar, 2010 ; Green,
Kraemer, Fugelsang, Gray, & Dunbar, 2012). Event-related poten-
tials have been used to find increased prefrontal activity for both a
semantic analogical reasoning task (Maguire, McClelland,
Donovan, Tillman, & Krawczyk, 2012) and a graphemic analogical
reasoning task (Qiu, Li, Chen, & Zhang, 2008). However, despite
this evidence, the specific localisation of processes supporting
abstraction within the frontal lobes remains debated.
1.2. Proverbs and the frontal lobes
One of the most regularly used frontal lobe tasks tapping
abstraction is proverb interpretation (see Gorham, 1956; Delis,
Kaplan, & Kramer, 2001). As an aspect of figurative language,
proverbs are familiar, fixed, sentential expressions that express
well-known truths, social norms or moral concerns (Gibbs & Beitel,
1995). Common examples are Rome wasn′t built in a day and All that
glitters is not gold . Proverb tasks assess the ability to interpret the
proverbial statement in an abstract or metaphorical rather than a
concrete sense, as the proverb’s meaning must be generalised to
more scenarios than are reflected literally in the proverb itself (Delis
et al., 2001, p. 205; Gibbs & Beitel, 1995). Impaired interpretations of
proverbs have been regarded as an indicative of dysfunction in
higher-level thinking processes linked with the frontal lobes. For
example, Zeigarnik (1927), quoted by Luria, 1966 found evidence
that patients with frontal lobe damage were unable to connect the
literal and the metaphorical meanings of proverbs. Thus, one
patient was noted as choosing the literal, rather than the correct
abstract interpretation of the proverbs in a multiple-choice trial.
Impaired proverb interpretation has been reported in other condi-
tions affecting the frontal lobes such as Parkinson’s disease (
Levin,
Llabre, & Weiner, 1989). An increased tendency to interpret pro-
verbs in a concrete sense in older people was found to be associated
with decreased frontal executive skills (Albert, Wolfe, & Lafleche,
1990; Uekermann, Thoma, & Daum, 2008).
Despite their popularity as an assessment tool, relatively few
studies have investigated the effects of focal cortical lesions on the
ability to interpret proverbs. In an older study, where the basis for
the classification of lesion location was not clear, Benton (1968)
found that patients with bilateral frontal damage were significantly
impaired in interpreting proverbs relative to those with unilateral
damage. There was a trend towards a stronger performance in the
left frontal group compared to the right frontal group with notable
percentages of patients from each group (left frontal: 20%, right
frontal: 25%, bilateral: 71%) performing in the impaired range.
In a more recent study, McDonald, Delis, Kramer, Tecoma, and
Iragui (2008) compared patients with frontal lobe epilepsy (FLE),
temporal lobe epilepsy (TLE) and healthy controls (HC’s) on a
proverb interpretation task (PIT). To our knowledge, this is the
only study where a systematic analysis of the errors made by
frontal lobe patients on a PIT was undertaken. On an overall test
score, FLE patients differed significantly from HC’s, but not from
TLE patients in terms of proverb interpretation. In a multiple-
choice trial, only FLE patients showed an increased tendency to
choose concrete interpretations of the proverb. A further contrast
based on the lateralisation of seizures showed that patients with
left-sided FLE showed significantly poorer abstraction relative to
the right-sided FLE patients.
Roca et al. (2010) reported data on a PIT from frontal lobe
patients as part of a wider study of the nature of executive
function deficits. The authors found that the frontal group as a
whole was significantly impaired on proverb interpretation rela-
tive to HC’s. In a further group comparison, no difference was
found between four different frontal subgroups: superior medial,
inferior medial, left lateral and right lateral. Although a significant
correlation was found between performance on the PIT and a test
of fluid intelligence, patients and controls still differed on the PIT
following adjustment for fluid intelligence. This indicates that
proverb interpretation could not be entirely explained by a deficit
in fluid intelligence. A subsequent lesion analysis examined the
performance of six patients who performed the worst on five tests,
including the PIT, where fluid intelligence did not account entirely
for differences between patients and controls. This indicated that
anterior (particularly right) frontal cortex was associated with the
remaining deficits on these tests once the variance associated with
fluid intelligence was accounted for. The authors suggested that
lesions to this area may have damaged a “common processing
theme” linking performance on these five tests.
1.3. Figurative language and the frontal lobes
The interpretation of proverbs, which undoubtedly requires the
understanding of metaphor (Gibbs & Beitel, 1995), can be viewed
as a part of the broader area of figurative language processes.
Studies of brain damaged patients have provided evidence for
frontal lobe involvement in such processes. Impaired idiom
comprehension has been demonstrated following frontal lobe
damage (Cacciari et al., 2006; Papagno, Curti, Rizzo, Crippa, &
Colombo, 200 6). This impairment has been shown to be associated
with executive function deficits in Alzheimer’s disease (Papagno,
Lucchelli, Muggia, & Rizzo, 2003). A reversed-concreteness effect
was found for idiom comprehension in a patient with temporal
lobe damage and a spared PFC (Papagno & Cacciari, 2010). In this
study, interpretation of unambiguous and thus less figurative
idioms was selectively impaired, with ambiguous idiom compre-
hension unimpaired. Impairments in metaphor processing have
been associated with decreased activity in the left inferior frontal
gyrus in patients with traumatic brain injury (Yang, Fuller,
Khodaparast, & Krawczyk, 2010) and patients with schizophrenia
(Kircher, Leube, Erb, Grodd, & Rapp, 2007), a condition linked with
deficits in frontal executive functions (Minzenberg, Laird, Thelen,
Carter, & Glahn, 2009).
In healthy subjects, neuroimaging studies have found associa-
tions between idiom comprehension and activity in left superior
medial frontal gyrus and left inferior frontal gyrus (Romero Lauro,
Tettamanti, Cappa, & Papagno, 2008), bilateral inferior frontal gyri
(Zempleni, Haverkort, Renken, & Stowe, 2007), and left ventral
dorsolateral PFC (Hillert & Buračas, 2009). One study utilising
transcranial magnetic stimulation has indicated that left and right
dorsolateral PFC is involved in idiom comprehension (Rizzo,
Sandrini, & Papagno, 2007). Reading of metaphors has been
associated with left inferior frontal gyrus activity (Rapp, Leube,
Erb, Grodd, & Kircher, 2004; Stringaris, Medford, Giampietro,
Brammer, & David, 2007).
There is ongoing debate regarding the role of left and right
hemispheres in figurative language processing. Influential
accounts have accorded a crucial role for right hemisphere regions
through suppressing literal interpretations of figurative language
or by processing less salient meanings (e.g. Bookheimer, 20 02;
Giora, Zaidel, Soroker, Batori, & Kasher, 2000; Stringaris et al.,
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–20862076
2006; Tompkins & Lehman, 1998). However, these results are
challenged by studies noting no effect of laterality on metaphor
processing tasks (Rapp et al., 2004), greater deficits in pragmatics
tasks in left-sided brain injury when compared to right-sided
brain injury (Soroker et al., 2005) and an effect of congruity but
not figurativeness on right-hemisphere processing of metaphors
(Diaz & Hogstrom, 2011).
1.4. Aims
Findings from the literature support the view that the frontal
lobes play an important role in proverb interpretation and in
figurative language. However, questions remain regarding the
localisation of processes within the frontal lobes that underpin
the interpretation of proverbs. This study investigated this issue in
a population of patients with unselected frontal lobe lesions
performing a proverb interpretation task. Our primary goal was
to examine if focal lesions to specific frontal lobe areas would have
a differential effect on performance on the PIT and the pattern of
errors made by patients. Following from Roca et al. (2010),we
sought to establish if such deficits resulting from damage to
specific frontal lobe areas could be explained by a deficit in fluid
intelligence. A secondary goal was to establish if the performance
of our patient group could shed further light on the role of right
and left hemispheres in figurative language processes.
2. Materials and methods
2.1. Participants
Eighty-one patients with focal unilateral frontal lobe lesions were recruited
from the National Hospital for Neurology and Neurosurgery (London, UK) and
assessed in the Neuropsychology Department. The inclusion criteria for the study
were: (i) age≤77 years, (ii) absence of psychiatric disorders, (iii) absence of other
previous neurological disorders, (iv) absence of aphasia, (v) a score above the 5th
percentile on a test of nominal functions, the Graded Naming Test (see below) and
(vi) presence of a unilateral lesion confined to the frontal lobe documented by MRI
or CT scan. Additionally (vii), patients were excluded if lesions were not localised to
medial, orbital or left or right lateral areas of the frontal lobes as per the criteria
outlined in Section 2.2 below. Fifty-two patients (N¼52) met these criteria. Details
of the aetiology of the lesions were available for N¼48 patients, details of which
are shown in Appendix A. The lesions were primarily the result of cerebrovascular
accidents or tumour resections. Note that the data from these patients were
gathered as part of a larger study of frontal lobe lesions. Patients from this study
have been included in previous studies of frontal lobe dysfunction (MacPherson,
Turner, Bozzali, Cipolotti, & Shallice, 2010; MacPherson et al., 2008; Robinson,
Shallice, Bozzali, & Cipolotti, 2010, 2012; Turner, Cipolotti, Yousry, & Shallice, 2007).
Each patient was matched with a healthy control (HC) for age, gender and full-
scale IQ as estimated by the National Adult Reading Test (NART). Fifty-two HC’s
were included in the study from a group of 107 initially assessed. Both left and right
frontal groups and left lateral, right lateral and medial frontal subgroups were
compared with HC’s in terms of age, gender, NART full-scale IQ and performance on
the Graded Naming Test. No significant differences were found (see Tables 1 and 2
for a summary of group and subgroup demographic details). The latter result
indicates that there was no difference between the groups in terms of their pre-
morbid intellectual functioning.
All participants gave informed consent according to the Declaration of Helsinki
1991. Our study was approved by the National Hospital for Neurology and
Neurosurgery and the Institute of Neurology Joint Research Ethics Committee
(UK). Other aspects of the performance of the participants in this study have been
reported previously (MacPherson et al., 2008, 2010; Robinson et al., 2010, 2012;
Turner et al., 2007).
2.2. MRI and lesion analysis
A neurologist who was blind to the history of each patient reviewed the hard
copies of MRI scans (or CT scan where MRI was unavailable). Brain MRI was
obtained on systems operated on a 1.5 T machine and included the acquisition of an
axial dual-echo and an axial and coronal T1-weighted scan. CT scans were all
obtained using a spiral CT system. Both MRI and CT data were used, as the main
goal of the current study was to enable the recruitment of a large number of
patients. The exclusion criteria and lesion assessment guidelines were based on
detailed anatomical localisation using standard atlases (Duvernoy, 1991). The lesion
localisation method is described in detail in Robinson et al. (2012). Briefly, each
frontal patient was coded for the presence of lesion in each hemisphere in the
Table 1
Demographic characteristics—left and right frontal groups and HC’s.
Left frontal N¼ 29
mean (SD)
Right frontal N¼ 23
mean (SD)
HC N¼ 52
mean (SD)
Group comparison
F-value
Age (years) 46.48 (11.26) 45.61 (15.76) 47.35 (14.59) 0.128 (p¼ 0.880)
Gender (male/female) 17/12 11/12 25/27 0.944
a
(p¼0.624)
No. months between surg/VA/neuropsy
b
18.16 (26.05) 22.77 (34.22) N/A 0.286 (p¼ 0.595)
No. of brain regions damaged 3.11 (2.35) 2.70 (1.66) N/A 0.500 (p ¼0.486)
GNT (no. correct/30) 20.76 (3.99) 22.35 (3.97) 22.77 (3.96) 2.438 (p¼ 0.092)
NART IQ 106.10 (15.12) 111.48 (8.95) 110.85 (9.83) 1.990 (p¼ 0.142)
SD, standard deviation; HC, healthy controls; no., number; surg, surgery; VA, vascular accident; neuropsy, neuropsychological assessment; N/A, non applicable; GNT, Graded
Naming Test; NART, National Adult Reading Test. All significant comparisons in bold.
a
Chi-squared analysis.
b
Number of cases missing (left frontal¼3).
Table 2
Demographic characteristics—three prefrontal subgroups and HC's.
Medial N¼ 17
mean (SD)
Left lateral N¼ 16
mean (SD)
Right lateral N¼13
mean (SD)
HC N¼ 46
mean (SD)
Group comparison
F-value
Age (years) 42.29 (10.04) 47.44 (12.78) 46.46 (14.74) 48.38 (14.41) 0.560 (p¼ 0.643)
Gender (male/female) 7/10 10/6 6/7 20/26 2.006
a
(p¼0.571)
No. months between surg/VA/neuropsy
b
32.71 (39.84) 18.27 (27.71) 11.27 (18.94) N/A 1.849 (p¼0.171)
No. of brain regions damaged 2.36 (1.66) 4.06 (2.74) 3.23 (2.28) N/A 2.366 (p¼ 0.106)
NART IQ 109.18 (11.21) 104.31 (17.81) 112.00 (8.803) 110.64 (9.22) 1.459 (p ¼0.231)
GNT (no. correct/30) 22.59 (4.39) 19.94 (3.70) 22.15 (3.46) 22.50 (3.84) 2.074 (p¼ 0.109)
SD, standard deviation; HC, healthy controls; no., number; surg, surgery; VA, vascular accident; neuropsy, neuropsychological assessment; N/A, non applicable. All significant
comparisons in bold.
a
Chi-squared analysis.
b
Number of cases missing (medial¼ 1/left lateral ¼1).
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–2086 2077
anterior and posterior portions of nine left and right frontal regions (18 areas in
total) (see Figs. 1 and 2). An area was only coded as damaged if at least 25% of the
area was affected.
Two types of lesion analyses were carried out. The first analysis aimed at
assessing the lateralisation effect by collapsing the nine left and right brain regions
and dividing the patients into two groups, i.e., left and right frontal, according to
which hemisphere was damaged.
In the second analysis, a more refined anatomical sub-division was employed,
similar to that used in previous studies (e.g. MacPherson et al., 2010; Robinson
et al., 2010, 2012; Turner et al., 2007). The prefrontal regions were collapsed in
order to define three main subgroups of patients: medial, left lateral and right
lateral.
For these subgroups, primary damage to the respective cortical areas was
defined as either (a) damage that was restricted to the cortical regions that defined
the subgroup or (b) damage that affected at least three cortical regions that defined
the subgroup and no more than one other region that defined an adjacent
subgroup. The medial subgroup (N ¼17) consisted of patients with unilateral
primary damage to the left (Fig. 1, panel B) or right (panel D) cingulate gyrus
(anterior/posterior), and/or the left (panel B) or right (panel D) medial superior
frontal gyrus (anterior/posterior). These areas consist of or overlap with Brodmann
areas 6, 8, 9, 10, 23, 24, 32 and 33. The lateral subgroups consisted of patients with
primary damage to the left (N¼ 16; panel C) or right (N¼13; panel A) lateral part of
the superior frontal gyrus (anterior/posterior), and/or the left (panel C) or right
(panel A) middle frontal gyrus (anterior/posterior) and/or the left (panel C) or right
(panel A) inferior frontal gyrus (anterior/posterior). These areas consist of or
overlap with Brodmann areas 6, 8, 9, 38, 44, 45, 46 and 47. See Fig. 3 for percentage
of patients from each group with damage to specified areas and Fig. 2 for depiction
of Brodmann areas contained within subgroups of interest. A further group of
patients with primary damage to the left (panels B and C) or right (panels A and D)
orbital cortex (blue areas, Brodmann areas 10 and 11) were excluded from the
analysis due to the small number of patients in the group (N¼ 6) and the lack of
error data available (half of the sample). However, a qualitative description of the
orbital patients will be provided.
We found no difference between left and right hemisphere groups and
between the medial, left lateral and right lateral subgroups in terms of the number
of frontal regions damaged (see Tables 1 and 2). The lesion analysis also revealed
that the lesions of 10 of our patients resulted in basal ganglia damage. The
likelihood of basal ganglia damage did not differ across the frontal subgroups,
χ
2
(3, N¼ 46)¼ 2.500, p¼0.287.
2.3. Neuropsychological investigation—baseline cognitive tests
The battery comprised well-known clinical tests with published standardised
normative data collected from large control samples. The National Adult Reading
Test (NART) was administered to estimate pre-morbid optimal levels of functioning
(Nelson & Willison, 1991). Raven’s Advanced Progressive Matrices (RAPM, Raven,
1976), an untimed, relatively culture-fair, non-verbal test, was used to assess
abstract reasoning. The Graded Naming Test (GNT, McKenna & Warrington, 1980)
was used to assess nominal functions. Executive functions were assessed using two
tests known to be sensitive to frontal lobe dysfunction, namely the Stroop test
(Trenerry, Crosson, DeBoe, & Leber, 1989) and the Trail Making Test (Reitan, 1958).
For the Stroop test we recorded the number of words or the number of colours
named in 2 min. For the Trail Making Test we report the results of Part B, known to
be sensitive to executive dysfunction (Stuss et al., 2001).
Superior Frontal gyr (anterior)
Superior Frontal gyr (posterior)
Middle Frontal gyr (anterior)
Middle Frontal gyr (posterior)
Inferior Frontal gyr (anterior)
Inferior Frontal gyr (posterior)
Orbito-frontal cortex
Cingulate (anterior)
Cingulate (posterior)
Fig. 1. Frontal lobe areas used to partition patients into subgroups of interest.
Fig. 2. Depiction of Brodmann areas contained within subgroups of interest.
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–20862078
2.4. Proverbs test (PIT)
The PIT was adapted from the the D-KEFS Proverb Test (Delis et al., 20 01). The
PIT contains eight metaphoric proverbs (see Supplementary material, Appendix A),
used in the English (UK) language. Each proverb is read aloud to the subject, who
provides an explanation of the meaning of the proverb. The participants’ responses
are recorded by the clinician. This task assesses the ability to interpret a statement
more in an abstract rather than a concrete sense, as the proverb’s meaning must be
generalised to more scenarios than are reflected literally in the proverb itself (Delis
et al., 2001, p. 205). For example, for the proverb “Rome wasn′t built in a day”,a
generalised understanding is that any great achievement (“Rome”) takes patience and
time to complete (“wasn′tbuiltinaday”). A concrete or literal (i.e. less generalised)
understanding of the proverb may refer to the length of time it takes to complete
buildings or infrastructure or the time it took to establish the Roman Empire.
The first analysis assessed the accuracy of interpretation of the proverb (or “free
enquiry”, see Delis et al., 20 01). Each oral response to an item on the PIT was scored
out of 2. Participants were given 2 points for a fully accurate, abstract interpretation
of the proverb in which all aspects of the proverb were covered. A 1 point was given
for a partially accurate abstract interpretation. A 1 point was also given for an
accurate explanation that was somewhat concrete/literal. No points were given for
inaccurate interpretations. Fifteen patients and 15 HC’s completed an abbreviated
form of the PIT consisting of four proverbs (items 1, 3, 5, and 7, see Appendix A).
Thus, to facilitate comparisons, each subject’s raw score on the PIT was converted
to a percentage correct score.
The second analysis, the error analysis, examined the errors made by the
subjects to probe their abstraction ability. Transcripts of the responses of 31 patients
and 46 HC’s were retrieved. Errors were divided into three mutually exclusive
categories; a partially accurate and abstract response, an accurate or inaccurate
concrete response and a non-concrete inaccurate response. Table 3 provides an
example from each category of response for one of the proverbs in the PIT. Note here
that concrete interpretations could score 1 or 0 depending on the accuracy.
To facilitate categorisation of errors, criteria for concrete responses for each
item were created. For example, for the proverb “the grass is always greener on the
other side” a response was considered concrete if it contained references to another
person’s garden or property, the colour of other items or if it was a restatement of
the proverb or a single example. These criteria were used to categorise each
subject’s responses by the named author (P.M.), who was blind to the presence/
absence of a brain lesion for each subject. A random sample (N¼15) of these
categorisations were checked by the named author (K.W.) to assess fidelity with
the criteria for concreteness. For each subject the percentage of responses (out of
the total number of items on PIT) that fell into each of the three error categories
was calculated.
2.5. Statistical analysis
The neuropsychological data were screened to ascertain if they were normally
distributed and to identify any outliers. We also checked the data for homogeneity
of variance. Since error variances differed significantly between the groups for the
Trails B Test we transformed these data using a natural log transformation. For the
demographic variables in Table 1 we used an ANOVA (age, years of education,
months between surgery and assessment, NART IQ) or a chi-square analysis
(gender, handedness) to test for a significant group difference. For the data in
Tables 4– 6b (baseline cognitive tests and accuracy of interpretation of proverbs) an
ANCOVA was used for each variable. NART score was entered as a covariate of no
interest for the data in Tables 4–6a. Age and NART score were entered as covariates
Fig. 3. Damage to frontal lobe regions for each frontal patient subgroup. Shading describes percentage of patients from each group with damage to specified area.
Table 3
Scoring examples for “Rome wasn′t built in a day” proverb.
Sample response Score
“It takes patience and time to complete a great, worthwhile project” (Fully accurate and abstract)2
“Things take time, but you will get there in the end” (Partially accurate and abstract)
“Any great city or empire, like Rome, will not be completed overnight” (Accurate concrete)
1
“Quit while you are ahead” (Non-concrete inaccurate) “Rome is a beautiful city” (Inaccurate concrete) Don′t know 0
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–2086 2079
Table 4
Performance on baseline cognitive tests—left and right frontal groups and HC's.
Left frontal N¼ 29
mean (SD)
Right frontal N¼ 23
mean (SD)
HC N¼ 52
mean (SD)
Group comparison
F-value
RAPM (number correct/12)
a
8.00 (2.69) 8.83 (2.08) 9.28 (1.66) 2.116 (p ¼0.126)
Trails B—time in msec
b
109.96 (99.44)
n
(p¼0.009)
y
90.46 (68.26) (p¼0.109) 66.45 (21.48) 3.881 (p ¼0.026)
Stroop word—no. words
c
206.62 (70.64)
n
(p¼ 0.013)
y
224.07 (50.30) (p¼0.145)
y
244.07 (48.96) 3.402 (p¼ 0.037)
Stroop colour—no. colours
d
80.12 (39.78)
n
(p¼ 0.003)
y
95.60 (36.43) (p¼ 0.168)
y
106.74 (23.72) 4.027 (p¼0.010)
SD, standard deviation; HC, healthy controls; no., number. All significant comparisons in bold.
y
Probability value from post hoc test (patient subgroup versus HC’s).
n
po 0.05 (significant group difference between patient group and HC’s).
a
Number of cases missing (HC¼ 2).
b
Number of cases missing (left frontal¼2/HC¼ 5).
c
Number of cases missing (left frontal¼2/right frontal¼1/HC¼1).
d
Number of cases missing (left frontal¼6/right frontal¼2/HC¼1).
Table 5
Performance on baseline cognitive tests—three prefrontal subgroups and HC's.
Medial N¼ 17
mean (SD)
Left lateral N¼16
mean (SD)
Right lateral N¼ 13
mean (SD)
HC N¼ 46
mean (SD)
Group difference
F-value
RAPM (number correct/12)
a
9.00 (2.76) 7.63 (2.60) 8.46 (2.30) 9.36 (1.63) 1.898 (p¼ 0.136)
Trails B—time in msec
b
85.26 (56.90)
n
(p¼ 0.026)
y
129.88 (125.00)
n
(p¼ 0.001)
y
102.59 (83.75)
n
(p¼0.012)
y
66.62 (21.44) 6.005
n
(p¼0.001)
Stroop word—no. words
c
221.52 (53.58) (p¼ 0.200)
y
193.27 (74.14)
n
(p¼ 0.007)
y
214.74 (47.56) (p¼ 0.108)
y
248.59 (57.10) 2.928
n
(p¼ 0.038)
Stroop colour—no. colours
d
101.61 (30.49) 80.50 (44.63) 85.22 (41.63) 105.95 (23.46) 2.371 (p¼0.077)
SD, standard deviation; HC, healthy controls; GNT, Graded Naming Test; no., number; msec, milliseconds; RAPM, Raven’s Advanced Progressive Matrices. All significant
comparisons in bold.
y
Probability value from post hoc test (patient subgroup versus HC’s).
n
po 0.05 (significant group difference between patient group and HC’s).
a
Number of cases missing (healthy controls¼2).
b
Number of cases missing (left lateral¼ 2/healthy controls¼5).
c
Number of cases missing (medial¼ 1/left lateral¼1/right lateral¼ 1/healthy controls¼ 1).
d
Number of cases missing (medial¼ 2/left lateral¼4/right lateral¼ 1/healthy controls¼ 1).
Table 6a
Proverb interpretation task accuracy—comparison of left and right frontal groups and frontal subgroups with HC’s.
Lateralisation analysis
a
Left frontal N¼ 27
mean (SD)
Right frontal N¼ 23
mean (SD)
HC N¼ 52
mean (SD)
Group difference
F-value
Score on proverbs task
(% score)
b
53.02 (23.18 )
n
(p¼ 0.003)
y
57.34 (19.46)
c
(p¼0.059)
y
65.50 (15.60) 3.400
n
(p¼0.020)
Finer-grained analysis Medial N¼ 17 mean (SD) Left lateral N¼ 16 mean (SD) Right lateral N¼ 13 mean (SD) HC N¼46 mean (SD) Group difference F-value
Score on proverbs task
(% score)
b
48.53 (16.76)
n
(p¼ 0.001)
y
56.25 (23.27) (p¼ 0.195)
y
59.62 (24.02) (p¼ 0.154)
y
66.71 (15.60) 4.220
n
(p¼ 0.008)
SD, standard deviation; HC, healthy controls. All significant comparisons in bold.
y
Probability value from post hoc test (patient subgroup versus HC’s).
n
po 0.05 (significant group difference between patient group and HC’s).
a
Orbital patients and their matched HC’s included.
b
Fifteen healthy controls and 15 patients were administered four items on the proverbs task, all others were administered eight items. Score represents the patient’s
score on the proverbs task expressed as a percentage. See text for guide to method of scoring.
c
Approaching significance (p¼ 0.059).
Table 6b
Proverb interpretation task accuracy—comparison of medial and lateral frontal subgroups.
Medial N¼ 29 mean (SD) Lateral frontal N¼29 mean (SD ) Group difference F-value
Score on proverbs task (% score)
a
48.53 (16.76) 57.76 (23.25) 4.296
n
(p¼0.044)
SD, standard deviation. All significant comparisons in bold.
n
po 0.05 (significant group difference between patient group and HC’s).
a
Eighteen healthy controls and 22 patients were administered four items on the proverbs task, all others were administered eight items. Score represents the patient’s
score on the proverbs task expressed as a percentage. See text for guide to method of scoring.
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–20862080
of no interest for the data in Table 6b. When an ANOVA/ANCOVA produced a
significant group effect, the between-subjects tests were employed to ascertain the
source of the significance. The Dunnett test with a threshold of p o 0.05 was
employed for post hoc analyses. Given the non-parametric nature of the data in
Tables 8–10 (error analysis), a Kruskal–Wallis or Mann–Whitney test was used for
each variable to test for a significant group difference. Where a significant effect
was found a between-subjects Mann–Whitney post hoc test with Bonferroni
correction was used to ascertain the source of significance.
Three analyses for grouping frontal patients based on lesion location were
carried out.
In the lateralisation analysis, left frontal and right frontal groups were contrasted
with controls. This analysis sought to investigate the lateralisation of processes
involved in proverb interpretation and figurative language processing. The neu-
ropsychological measures, scores on the PIT and category of error on the PIT were
the dependent variables.
A finer-grained analysis contrasted left lateral versus right lateral versus medial
versus HC’s. This analysis investigated the localisation of the processes under-
pinning proverb interpretation within the frontal cortex. It mirrored those used in
previous studies (Reverberi et al., 2005; Robinson et al., 2012; Stuss & Alexander,
2005; Stuss et al., 1998, 2000), allowing comparison to be made with previous
behavioural analyses of frontal lobe dysfunction. A comparison of models of
cognitive process organisation within the prefrontal cortex (e.g. Duncan, 1995;
Stuss & Alexander, 2000) was also possible following this analysis. The orbital
group and their respective matched controls were omitted from this analysis due to
the small number of patients in the orbital group (n ¼6). Once again, the
neuropsychological measures, scores on the PIT and category of error on the PIT
were the dependent variables.
A third analysis, a contrast of specific frontal subgroups, was based on the
procedure of Alexander, Stuss, Picton, Shallice, and Gillingham (2007). This analysis
was carried out if and only if a group difference was found on the finer-grained
analysis. This analysis examined the specificity of any effects found in areas of the
frontal cortex. If a frontal group (left or right) or subgroup (left lateral, right lateral
or medial) were found to differ significantly from HC’
s, then this group was
compared with the frontal patients from the subgroup or subgroups that did not
differ significantly from HC’s. Scores on the PIT and category of error on the PIT
were the dependent variables.
Table 7
Pearson’s r coefficients for correlations of performance on the PIT with the performance on baseline cognitive measures.
All frontal patients Left frontal Right frontal Left lateral Right lateral Medial
RAPM 0.170 (p¼ 0.229) 0.244 (p¼ 0.203) 0.016 (p¼0.942) 0.316 (p¼0.233) 0.092 (p¼ 0.764) 0.321 (p¼ 0.209)
Trails B—time in msec 0.271 (p¼ 0.057) 0.396
n
(p¼0.041) 0.022 (p¼0.921) 0.475 (p ¼0.086) 0.027 (p¼ 0.931) 0.318 (p¼ 0.213)
Stroop word—no. words 0.106 (p ¼0.469) 0.255 (p¼ 0.200) 0.247 (p¼0.267) 0.269 (p¼0.332) 0.295 (p ¼0.352) 0.146 (p¼ 0.590)
Stroop colour—no. colours 0.311
n
(p¼ 0.040) 0.383 (p¼ 0.072) 0.182 (p¼0.429) 0.415 (p¼ 0.180) 0.338 (p¼ 0.283) 0.619
n
(p¼ 0.014)
Graded Naming Test 0.344
n
(p¼ 0.012) 0.365 (p¼ 0.051) 0.285 (p¼ 0.187) 0.441 (p¼0.087) 0.275 (p ¼0.363) 0.586
n
(p¼ 0.013)
n
po 0.05 (significant correlation).
Table 8
Category of errors
a
made by left frontal and right frontal patients and HC's.
Left frontal N¼ 16
mean (SD)
Right frontal N¼ 15
mean (SD)
HC N¼ 37
mean (SD)
χ
2
(p-value)
Concrete errors as % of total errors 36.11 (38.10)
*
(p¼ 0.009)
y
13.17 (22.24) (p¼0.224)
y
8.31 (19.65) 9.365
*
(p¼0.001)
Partial errors as % of total errors 40.48 (32.78)
*
(p¼ 0.001)
y
59.60 (36.21) (p¼ 0.066)
y
79.25 (25.64) 14.371
*
(p¼ 0.006)
Non-concrete incorrect errors as % of total errors 17.16 (19.19) 20.56 (26.82) 12.44 (18.90) 1.376 (p ¼0.503)
All significant comparisons in bold.
y
Probability value from post hoc test (patient subgroup versus HC’s).
n
po 0.05 (Bonferroni corrected for comparisons between individual patient groups and HC’s).
a
See Materials and methods section for complete explanation of response categories.
Table 9
Category of errors
a
made by left lateral, right lateral and medial frontal patients and healthy controls.
Medial N¼ 8
mean (SD)
Left lateral N¼ 11
mean (SD)
Right lateral N¼9
mean (SD)
HC N¼ 33
mean (SD)
χ
2
(p-value)
Concrete errors as % of total errors 24.46 (8.71) (p¼ 0.062)
y
44.92 (41.73)
n
(p¼ 0.001)
y
12.25 (20.32) (p¼ 0.526) 7.59 (20.11) 11.841
n
(p¼ 0.008)
Partial errors as % of total errors 42.89 (29.27)
n
(p¼0.002)
y
34.90 (34.23)
n
(p¼0.007)
y
61.60 (36.00) (p¼ 0.355) 80.22 (24.81) 16.232
n
(p¼ 0.001)
Non-concrete incorrect errors as % of total errors 35.74 (29.27) (p¼ 0.024) 11.09 (14.63) (p ¼0.979) 15.04 (20.39) (p¼ 0.763) 12.19 (19.03) 6.408 (p¼ 0.093)
All significant comparisons in bold.
y
Probability value from post hoc test (patient subgroup versus HC’s).
n
po 0.05 (Bonferroni corrected for comparisons between individual patient groups and HC’s).
a
See Materials and methods section for complete explanation of response categories.
Table 10
Category of errors
a
made by medial and lateral frontal subgroups.
Medial N¼ 8
mean (SD)
Lateral frontal N¼20
mean (SD)
Z (p-value)
Concrete errors as % of total errors 21.38 (24.64) 30.22 (36.99) 0.215 (p¼ 0.830)
Partial errors as % of total errors 42.89 (29.27) 46.91 (36.72) 0.051 (p¼0.980)
Non-concrete incorrect errors as % of total errors 35.74 (29.27) 12.87 (17.08) 2.065 (p¼ 0.049)
a
See Materials and methods section for complete explanation of response categories.
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–2086 2081
2.6. Procedure
Each participant completed the neuropsychological tests, which were adminis-
tered by experienced clinical neuropsychologists as part of a larger set of tests. All
patients underwent an MRI or a CT scan.
3. Results
3.1. Baseline cognitive tests
3.1.1. Lateralisation analysis
Table 4 details the performance of the three groups on the
baseline cognitive measures. There was no main effect of group on
performance on the RAPM, with no significant difference between
the left and right frontal groups and HC’s. Neither was a significant
group effect found on the GNT (see Table 1). For the Stroop Test,
group effects were found on the word-reading trial and the colour-
naming conflict condition. In both cases left frontal patients alone
performed worse than HC’s. A group effect was also found on the
Trails B test. Left frontal patients took significantly more time to
complete the test than HC’s.
3.1.2. Finer-grained analysis
Table 5 details the performance of the three patient subgroups
on the baseline cognitive measures along with the HC’s. As
detailed above the orbital subgroup was omitted from each
analysis and NART score was included as a covariate.
No significant group effect was found on performance on the
RAPM or the Stroop colour-naming conflict condition. Neither was
a significant group effect observed for GNT (see Table 2). Group
effects were found for the Stroop test word-reading condition.
Here, the left lateral subgroup alone performed significantly worse
than HC’s. A group effect was also found on the Trails B test, with
medial, left lateral and right lateral subgroups all significantly
slower than HC’s at completing this test.
3.2. Proverbs test (PIT)—accuracy of interpretation
3.2.1. Lateralisation analysis
Comparison of left frontal, right frontal and HC groups on the
PIT revealed a significant group effect (see Table 6a). Post hoc
comparisons revealed that the left frontal group performed
significantly worse than controls on the PIT. The right frontal
group narrowly missed out on significance, showing a trend
towards a poorer performance on the PIT.
3.2.2. Finer-grained analysis
Comparison of medial, left lateral, right lateral and HC groups
on the PIT revealed a significant group effect, with post hoc
comparisons revealing that the medial subgroup performed sig-
nificantly worse than HC’s. Left lateral and right lateral subgroups
did not differ significantly from HC’s. An additional comparison of
left medial and right medial patients found no difference in terms
of their performance on the PIT (F(1, 15) ¼0.177;
p¼0.681).
3.2.3. Contrast of specific frontal subgroups
The finer-grained analysis revealed a significant difference
between the medial subgroup and HC’s. In contrast, no difference
was found between the two lateral subgroups and HC ’s. We
investigated how specific to the medial subgroup the difficulty
interpreting proverbs was by comparing their performance on the
PIT with the two lateral groups combined. An ANCOVA was used to
test for a group effect with age and NART score entered as a
covariate. A group effect was observed, with the means indicating
that the medial subgroup performed significantly worse on the PIT
than the other lateral patients (orbital patients excluded, see
Table 6b).
3.2.4. Orbitofrontal subgroup
The orbitofrontal subgroup was excluded from the analysis due
to the low number of patients (n¼6). Qualitatively, it was noted
that the mean performance of this subgroup on the PIT was
comparable to that of the non-impaired subgroups (orbital group,
mean: 59.38% sd: 24.29%; HC’s, mean: 65.50%, sd: 15.60%), with
two of the six orbital patients scoring more than 1.5 standard
deviations below the mean of the control group.
3.2.5. Correlations with baseline cognitive tests
Given the results above, it is of interest if cognitive dysfunction
as revealed by the baseline cognitive tests may predict perfor-
mance on the PIT. A correlational analysis between PIT perfor-
mance and each baseline test was carried out to this end for each
group and subgroup. The results of each correlation are shown in
Table 7. No significant correlations were observed between the
performance on the PIT and the RAPM for any patient group or
subgroup. Scores on the GNT and the Stroop colour-naming
conflict condition correlated significantly with PIT performance
for the patients as a whole and for the medial subgroup. On the
Trail Making Test Part B, a significant correlation was observed for
the left frontal group only. No correlation was noted between the
performance on the Stroop word-reading condition and the
performance on the PIT for any patient group or subgroup.
3.2.6. Fluid intelligence
Given our interest in the relationship between the performance
on the PIT and fluid intelligence, we compared the performance
within patient subgroups on the measure of fluid intelligence
(RAPM). Although PIT score was seen to be significantly worse in
the medial patients compared to lateral patients (see above), they
did not differ from lateral patients significantly in terms of
performance on the RAPM (F(1, 43) ¼0.556; p¼0.460). In fact,
none of the three frontal subgroups were found to differ from each
other on this measure (F(2, 42) ¼ 0.282; p¼
0.756).
3.3. Proverbs test (PIT)—error analysis
Here we investigated if there were differences in terms of
abstraction or concreteness in the type of responses given by our
patient sample and HC’s. For this purpose, errors were categorised
into three mutually exclusive categories as detailed above (see
Table 3 ). Results of group comparisons on these variables are as
follows.
3.3.1. Lateralisation analysis
Comparing left frontal, right frontal and HC groups, a signifi-
cant group effect was found for both concrete responses as a
percentage of total errors and partially correct responses as a
percentage of total errors. No difference was found between the
left frontal, right frontal and HC groups in terms of non-concrete
incorrect responses as a percentage of total errors (see Table 8).
Breaking down these effects using post hoc analyses with
Bonferroni corrections, it was found that a higher percentage of
the left frontal group’s errors were concrete when compared with
the HC group. Right frontal patients and HC’s did not differ from
each other in terms of the percentage of errors that were concrete.
A significantly lower percentage of the left frontal patients’ errors
were partial errors compared to HC’s. No difference was found
between right frontal patients and HC’s in terms of the percentage
of errors that were partial errors.
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–20862082
3.3.2. Finer-grained analysis
Repeating this analysis of errors for the frontal subgroups,
significant group differences were found for the percentage of
errors that were concrete responses and partially correct
responses (see Table 9 and Fig. 4).
Using post hoc analyses with Bonferroni correction, it was
found that for the left lateral subgroup alone, a significantly higher
percentage of their errors were concrete responses when com-
pared with HC’s. Medial and right lateral subgroups did not differ
significantly from HC’s in this respect. As depicted in Fig. 4, the left
lateral group was almost twice as likely as medial patients and
more than three times more likely than right lateral patients to
make a concrete response when making an error. This result is
further emphasised if one examines the likelihood of 50% or more
of errors being concrete responses. The three patient groups
differed in this regard (χ
2
(2, N¼28)¼0.049), with a post hoc
Fisher’s exact test demonstrating that the left lateral patients were
significantly more likely than the other two subgroups to make
concrete responses on 50% or more of their errorful responses
(p¼0.029).
For the left lateral and medial subgroups, a significantly lower
percentage of their errors were partially correct when compared
with HC’s with no significant difference found between the right
lateral subgroup and HC’s in this regard.
3.3.3. Contrast of specific frontal subgroups
Here we examined if the patterns of concrete, partial and non-
concrete incorrect errors in the Medial subgroup would differ from
the other two frontal subgroups. Right and left lateral subgroups
were combined for this analysis and compared with the medial
subgroup based on the three categories of error (see Table 10 ). No
group difference was observed for percentage of concrete
responses, partially correct responses, or non-concrete incorrect
responses.
3.3.4. Orbitofrontal subgroup
Qualitatively, it was noted that none of the three of six
orbitofrontal subgroup patients for whom error data were avail-
able made a concrete error on the PIT. Only one patient made a
single non-concrete incorrect error. The percentage of errors made
by the orbital group that were partial errors was comparable to
controls (orbital group, mean: 86.77%, sd: 22.91%; HC’s, mean:
79.25%, sd: 25.64%).
4. Discussion
4.1. Summary of results
To our knowledge, this is the first study to investigate the
performance of a large number of non-aphasic patients with focal
frontal lesions on a proverb interpretation task (PIT). The PIT
requires an abstract interpretation of proverbs that relates to a
wide variety of contexts, as opposed to a literal, concrete inter-
pretation. Our samples of frontal patients and healthy controls
(HC’s) were matched for age and on a measure of estimated pre-
morbid intellectual ability. They did not differ from controls in
terms of gender or performance on a test of nominal skills. Also,
the patient groups and subgroup did not differ in terms of the
number of frontal regions damaged, the time between injury and
assessment and the likelihood of subcortical damage. However,
significant differences were found on tasks sensitive to executive
dysfunction, as well as on a fluid intelligence task. The patients’
performance on the PIT was analysed as follows.
4.1.1. Lateralisation analysis
This provides data relevant to previous studies investigating
the role of the left and right frontal lobes in proverb interpretation.
This analysis showed a significant impairment on the PIT for the
left frontal patients and a trend towards impairment in the right
frontal group. Previous studies have reported impairment in
proverb interpretation following lesions to either the left or right
frontal lobes (Benton, 1968; Roca et al., 2010).
4.1.2. Finer-grained analysis
This provides a potential theoretical interpretation for the data. It
focussed on the role of medial and lateral frontal areas in proverb
interpretation. This analysis showed that only patients with
medial frontal lobe damage were significantly impaired on the
PIT relative to HC’s.
4.1.3. Contrast of specific subgroups
This compared directly the performance of the medial frontal
subgroup with the lateral subgroups combined. Quite strikingly,
the medial frontal subgroup performed significantly worse on the
PIT than the lateral patients combined.
4.1.4. Error analysis
We analysed the patients’ and HC’s responses in terms of the
percentage of their errors that were concrete, partially correct and
non-concrete incorrect. We found that:
1. For the left lateral patients alone, a significantly higher percen-
tage of their errors were concrete when compared to HC’s.
2. For the medial and left lateral patients, a lower percentage of
their errors were partially correct when compared to HC’s.
In addition to these results, none of our patient groups or
subgroups performed worse than HC’s on a measure of fluid
intelligence (RAPM). Moreover, fluid intelligence did not correlate
with the performance on the PIT in any of our patient groups or
subgroups.
4.2. Proverb interpretation and the medial frontal lobe
Patients with medial frontal lesions were significantly impaired
on the PIT compared to HC’s and lateral patients. This finding
suggests that medial frontal areas play a significant role in proverb
interpretation. This is in line with previous imaging findings. For
example, Wallentin et al. (2005) reported higher medial frontal
Fig. 4. Percentage of total errors made by patient subgroups that were concrete
errors.
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–2086 2083
activity during the comprehension of more abstract sentences
rather than concrete sentences. Moreover, increased activity in
medial frontal areas has been shown to be associated with verbal
analogical reasoning, which, as outlined in the introduction, shares
many of the features of proverb interpretation (Green et al., 2010,
2012).
One possible explanation for the medial effect is in line with
the interpretation of Romero Lauro et al. (2008). In this study the
authors suggested that when comprehending idioms, two inter-
pretations of the sentence are available, idiomatic and literal.
According to the authors, the anterior medial prefrontal cortex is
involved in selecting the less natural interpretation (i.e. the
idiomatic interpretation). However, the anterior medial prefrontal
region activated in the Romero Lauro et al. study (4, 54, 32) is
very close to that area found by Gilbert, Frith, and Burgess (20 05)
to be more activated in stimulus-oriented rather than stimulus-
independent processes, which makes this interpretation some-
what less plausible; the less natural interpretation is presumably
not the result of a more stimulus-oriented process.
An alternative possibility is derived from the hypothesis that the
medial frontal cortex plays a key role in attentional “energ isa tio n”.
This is a top-down process that acts to initiate and sustain one
specific type of thought process or behaviour rather than another
(Stuss & Alexander, 2007), particularly in situations where the
responses are not over-learned (Shallice et al., 2008). Proverb
interpretation requires generation of not over-learned responses. T o
make a correct interpretation a proverb will activate abstract as well
as concrete interpretations. Howeve r, correct responses on the PIT
would requir e one to select a weaker abstract interpretation over a
more dominant concrete one. Given this, the difficulty shown by our
medial patients on the PIT may reflect an energisation difficulty .
4.3. Proverb interpretation and the left lateral frontal lobe
Our left lateral subgroup did not differ from HC’s in terms of
their overall level of performance on the PIT. However, of the
errors they made a significantly higher percentage were concrete
errors, accounting for 44.92% of their total errors. This is in
contrast to the other frontal subgroups, for whom 24.46% (medial)
and 12.25% (right lateral) of their errors were concrete. This result
is consistent with McDonald et al.’s (2008) findings, where left
frontal lesions were associated with poorer abstraction compared
to right frontal lesions. We will argue later that concrete errors are
at least as sensitive a measure of frontal “executive” impairment as
overall performance.
Left lateral frontal areas have previously been linked with
figurative language processes in imaging studies with the main
emphasis being on the left inferior frontal gyrus (Rapp et al., 2004;
Romero Lauro et al., 2008; Stringaris et al., 2007; Yang et al., 2010).
It has been suggested that this region is involved in selection
between competing verbal responses (see e.g. Robinson, Blair, &
Cipolotti, 1998; Thompson-Schill et al., 1997). A related although
more general hypothesis is that the left inferior frontal gyrus is
involved in “difficult” semantic operations per se (e.g. Yang et al.,
2010). Neither of these hypotheses explains why, unlike the medial
impairment, the left lateral impairment of our patients does not
manifest itself in an overall poorer performance but specifically in
a higher rate of concrete errors. This result suggests a third
possible explanation related to a hypothesis put forward by
Shallice and Cooper (2011, submitted for publication) for abstract
words. This hypothesis suggests that the left inferior frontal gyrus
is involved in constructing or storing abstract representations.
Damage to this region would leave only the literal interpretation
available to the patient. However, further investigations are
required to disambiguate between these three types of
explanation.
We would like to argue that the performance of the left lateral
subgroup has implications for the clinical use of the PIT. Our left
lateral patients were on average 2 standard deviations worse than
HC’s in terms of the percentage of errors that were concrete. The
medial subgroup was on an average more than 1 standard devia-
tion worse. By contrast, only the medial subgroups were more
than 1 standard deviation worse than HC’s in terms of their overall
performance on the PIT. Thus, large differences were found
between two subgroups and HC’s in terms of concrete errors,
whereas only the medial subgroup differed significantly from HC’s
in terms of overall performance on the PIT. Therefore, in clinical
scenarios it would appear that concrete responses on the PIT
rather than overall performance are likely to represent a more
sensitive measure of frontal executive dysfunction.
4.4. Lateralisation of figurative language processing
Studies of figurative language processes have provided some-
what inconclusive evidence regarding the lateralisation of anato-
mical substrates involved in figurative language processes. Thus,
some studies suggested that bilateral frontal areas are crucial for
idiom (e.g. Rizzo et al., 2007; Zempleni et al., 2007; see Thoma &
Daum, 2006 for review) and proverb interpretation (Benton,
1968). Other studies have suggested that left frontal areas are
critical for this process (e.g. Cacciari et al., 2006; Hillert & Buračas,
2009; Papagno et al., 2006; Romero Lauro et al., 2008). Several
other authors have ascribed a crucial role for right hemisphere
regions in figurative language processes or in suppressing literal
interpretations of figurative language (e.g. see Bookheimer, 2002
for review; Tompkins & Lehman, 1998). Recently, Roca et al. (2010)
found some evidence for right anterior frontal involvement in
proverb interpretation. Unfortunately, the types of errors made by
their patients were not reported.
Our fi
nding that patients with left and right medial frontal lobe
lesions were significantly impaired on the PIT seems to provide
some limited support for the suggestion that the frontal lobes
bilaterally are implicated in the processing of figurative language.
With regards to a right-hemisphere advantage in processing
figurative language, we failed to find evidence for increased
numbers of concrete responses following right frontal lobe lesions.
Indeed, our error analysis differentiated left frontal patients, but
not right frontal patients, from HC’s.
Our results are therefore in conflict with the hypothesis that
the right hemisphere has a particular role in figurative language
processes (e.g. Bookheimer, 2002; Giora et al., 2000; Stringaris
et al., 2006; Tompkins & Lehman, 1998). Instead, our data suggest
that an impaired performance on the PIT is associated with
bilateral medial frontal lobe lesions and that an increased number
of concrete responses are associated with the damage to left
lateral areas of the frontal lobes. Our data also suggest that
separate areas of the frontal lobes may contribute differentially
to figurative language processing.
4.5. Fluid intelligence and proverb interpretation
The performance of our frontal patients on the PIT did not
correlate with the performance on a fluid intelligence test (RAPM).
Roca et al. (2010) found this correlation, but only when combining
patient and control groups as a whole. However, the authors found
that this correlation could not entirely explain performance on the
PIT in their frontal sample, which is corroborated by our study.
Indeed, Roca et al. also examined the mean of the residual deficits
not accounted for by fluid intelligence deficits on five tasks,
including the PIT. They reported that right anterior frontal lesions
were associated with the mean of the residual deficits. Further-
more; Roca et al. did not find a difference in performance on the
P. Murphy et al. / Neuropsychologia 51 (2013) 2075–20862084
PIT when comparing their four frontal subgroups. In contrast, the
only group impaired relative to HC’s in our study (medials) was
also impaired relative to the other two frontal subgroups (left and
right laterals).
There are some notable differences between our study and that
of Roca et al. Whereas Roca et al. had 15 frontal lobe patients
completing their version of the PIT, of which less than five were
medial patients, our study had 52 frontal patients of whom 17
were medial. Our increased numbers of patients would be
expected to lead to a more sensitive study. Secondly, the inclusion
of patients and healthy controls in the correlations in Roca et al.
(2010) is a possible source of divergent findings. There were also
some important differences between the scoring procedures
adopted to analyse responses on the PIT in Roca et al.’s study
and in our study. Roca et al. scored responses as correct, an
example and incorrect whereas we have used a more differen-
tiated scoring procedure. It is possible that our scoring criteria
were more stringent and therefore may have highlighted difficul-
ties in frontal patients that were not revealed by Roca et al. This is
supported by the observation that the mean performance for the
HC’s in our study (65.50%) is lower than that of the HC’s tested in
Roca et al.’s study (91.33%).
One weakness of our study was the small number of patients
with orbitofrontal cortex damage, which led to their exclusion
from the finer-grained analysis. Functional imaging studies have
linked this area of the frontal lobes with analogical verbal reason-
ing, a cognitive process sharing many of the features of proverb
interpretation (Bunge et al., 2005; Green et al., 200 6). Future
studies could examine proverb interpretation in larger numbers of
orbitofrontal patients. A second weakness was that for our retro-
spective study additional data from language tasks other than
nominal tasks were not available. This has prevented us from
investigating whether the impairments in frontal patients on the
PIT could be linked with other broader language processes.
A third weakness of our study was the information available on
lesion extent for our patient sample. Although we found no
difference between the frontal subgroups in terms of the number
of frontal regions damaged, we were unable to compare each
group in terms of the overall volume of cortex damaged by the
lesions. To obtain a large enough sample, 12 years of patient
referrals needed to be included and in the earlier patient referrals
the clinical scans available were not suitable for VBM or VLSM
procedures. It is therefore possible that subgroups differed in
terms of total lesion volume, which may have contributed to the
differences reported between the groups on the PIT.
Our results show for the first time that medial and left lateral
areas play a crucial role in proverb interpretation. We have also
demonstrated that medial frontal lesions impair performance on
the PIT, with left lateral lesions giving rise to significantly
increased levels of concrete errors compared with HC’s. Our results
do not support the view that deficits in the PIT following focal
frontal lobe lesions reflect a deficit in fluid intelligence. Our
findings also fail to support accounts that stress a specific role
for the right frontal lobe in figurative language processing. Instead,
our results seem to support the notion that proverb interpretation
engages a set of specialised cognitive processes underpinned by
medial and left lateral areas.
Acknowledgements
This research was supported by a grant provided by the Well-
come Trust, Grant no. WT089231AIA.
Gail Robinson is supported by an Australian Research Council
Discovery Early Career Researcher Award (DE120101119).
Appendix A
See Table A1.
Appendix B
Proverbs test.
1. Don′t cry over spilt milk.
2. Rome wasn′t built in a day.
3. Where there′s a will there’saway.
4. Strike while the iron is hot.
5. The grass is always greener on the other side.
6. Let sleeping dogs lie.
7. All that glitters is not gold.
8. Too many cooks spoil the broth.
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