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Johnstone, B., Cohen, D., Bryant, K. R., Glass, B., & Christ, S. E. (2014, November 17).
Functional and Structural Indices of Empathy: Evidence for Self-Orientation as a
Neuropsychological Foundation of Empathy. Neuropsychology. Advance online publication.
http://dx.doi.org/10.1037/neu0000155
Neuropsychology
2014, Vol. 29, No. 1, 000
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University of Missouri
Objective: To evaluate a model that hypothesizes that empathy is associated with decreased right parietal
lobe (RPL)-related self-orientation (i.e., increased selflessness), which allows individuals to more easily
empathize with others. Methods: Participants: Thirty one individuals with documented neuroradiological
abnormalities due to traumatic brain injury (TBI) referred for clinical evaluations. Measures: Cerebral
integrity was measured with both functional (i.e., neuropsychological tests) and structural indices (i.e.,
MRI). Participants were administered comprehensive neuropsychological tests associated with general
bilateral frontal, temporal, and parietal lobe functioning, a self-report measure of empathy (i.e., Penners
Prosocial Personality Battery), and an objective measure of empathy (i.e., Prisoners Dilemma). Twenty
participants also completed structural MRI analysis of the bilateral frontal, temporal, parietal, and insular
cortices measured in terms of volume. Results: Pearson correlations indicated that empathy was related
to increased neuropsychological indices of RPL and frontal lobe (primarily left frontal) functioning. The
only MRI indices associated with empathy were the bilateral insula. Neither functional nor structural
cerebral indices were significantly related to objective measures of empathy. Conclusions: Contrary to
hypotheses, empathy appears to be associated with increased RPL functioning. It is suggested that to
incorporate the experiences of others into the experience of the self (i.e., to be empathetic), one must have
an intact sense of the self.
Keywords: affective empathy, cognitive empathy, self-orientation, right parietal lobe, neuropsychology
Neuroanatomy of Empathy
There has been growing interest in determining the neuroanatomical and neuropsychological foundations of empathy (hereby
defined as the action of understanding, being aware of, being
sensitive to, and vicariously experiencing the feelings, thoughts,
and experience of another). A meta-analysis of empathy research
concluded that empathy is a complex construct that is related to
multiple neurologic networks and cognitive and emotional abilities
(Zaki & Ochsner, 2012). Specifically, empathy has been shown to
be related to the inferior parietal lobe, temporoparietal junction,
anterior insula, posterior superior temporal sulcus, temporal pole,
premotor cortex, posterior cingulate cortex, anterior cingulate cortex, medial prefrontal cortex, insula, right temporoparietal region,
and various regions of the frontal lobes (Banissy, Kanai, Walsh, &
Rees, 2012; Decety & Jackson, 2004; Decety & Jackson, 2006;
Eslinger, 1998; Grattan, Bloomer, Archambault, & Eslinger, 1994;
Grattan & Eslinger, 1989; Grattan & Eslinger, 1992; Mutschler,
Reinbold, Wankerl, Seifritz, & Ball, 2013; Preston & de Waal,
2002; Shamay-Tsoory, Tomer, Goldsher, Berger, & Aharon-
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Neuropsychology of Empathy
In addition to identifying the cerebral areas associated with
empathy, research has also focused on determining the specific
affective and cognitive components of empathy. Empathy has been
conceptualized as relating to numerous cognitive processes including attention, memory, perspective taking, theory of mind, abstract
reasoning, cognitive flexibility, generational fluency, and set shifting (Rankin et al., 2005). More concisely, empathy is generally
conceptualized as involving two primary neuropsychological processes including the ability to cognitively take the perspective of
others (i.e., cognitive empathy) and the ability to feel the emotions
of others as if they were ones own (i.e., affective empathy;
Shamay-Tsoory et al., 2009; Shamay-Tsoory, 2011). Studies of
empathy involving persons with brain dysfunction have primarily
focused on the associations between empathy and cognitive flexibility (Grattan et al., 1994; Shamay-Tsoory et al., 2009; Grattan &
Eslinger, 1989), with suggestions that increased cognitive flexibility allows individuals to take the perspective of others. Other
studies suggest that empathy is related to declarative memory
(Beadle & Tranel, 2013), as well as empathetic concern (Rankin et
al., 2005; Rankin et al., 2006).
Methods
Participants
The sample included 31 individuals with TBI referred for outpatient neuropsychological evaluations at a Midwestern university.
All participants had abnormal clinical radiologic evaluations of the
brain. Neuropsychological tests and self-report measures of empathy were completed by all 31 participants. MRI data for 20
participants was obtained and analyzed for research purposes. Data
were unavailable for the remaining participants due to either
preexisting counterindications (e.g., metal in body; n 7) or
technical problems at the time of testing (n 4). Chi-square and
t tests conducted between the 20 participants with and 11 participants without MRI scanning indicated there were no significant
differences in neuropsychological, demographic, or outcome measures between the groups, other than marital status (with the group
not receiving MRI having a higher percentage of divorce).
The average age of the sample was 34.6 years (SD 16.2; range
17 87). The mean Wechsler Adult Scale of Intelligence III, Full Scale
IQ (WAIS-3 FSIQ) of the sample was in the average range (WAIS-3
FSIQ 93.4; SD 15.9; Wechsler, 1997a). The WAIS-3 FSIQ was
not significantly correlated with any measure of empathy. Demographic characteristics of the entire sample are presented in Table 1.
TBI injury severity characteristics are presented in Table 2.
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Procedure
All participants were referred for clinical neuropsychological
evaluations and had evidence of abnormal neuroradiological evaluations at the time of their injuries. They were administered
measures of the functional integrity of the brain including intelligence, memory, language, visual-spatial skills, attention, and
sensory-motor skills by psychometricians (see Table 3). Participants provided informed consent and completed subjective measures of empathy (see Table 4). Participants were then scheduled
for MRIs (i.e., measures of the structural integrity of the brain),
where they were screened for contraindications to scanning and
also completed an objective measure of empathy. Participants were
Table 2
Sample Brain Injury Characteristics
Loss of Consciousness
Yes
No
Unknown/Missing
Retrograde Amnesia
Yes
No
Unknown/Missing
Posttraumatic Amnesia
Yes
No
Unknown/Missing
Effected Brain Regions on Imaging
Left Frontal
Right Frontal
Left Temporal
Right Temporal
Left Parietal
Right Parietal
Occipital
Percent
18
5
8
58.1
16.1
25.8
9
0
22
29.0
0.0
71.0
14
0
17
45.2
0.0
54.8
9
7
7
7
6
4
2
29.0
22.6
22.6
22.6
19.4
12.9
6.5
compensated $100. The present study was approved by the universitys research review board.
Measures of Empathy
Table 1
Sample Demographics
Gender
Male
Female
Handedness
Right
Left
Ethnicity
White
African American
Biracial
Marital Status
Married
Divorced
Separated
Single
Education
Some HS
HS Diploma
Some College
Bachelors Degree
Masters Degree
PhD/JD/MD
Employment Status
Currently Employed
Student
Unemployed, not on disability
Unemployed, on disability
Retired
Annual Income
$20,000
$20,001$40,000
$40,001$60,000
$60,001$80,000
$80,000
Percent
21
10
67.7
32.3
28
3
90.3
9.7
28
1
2
90.0
3.2
6.5
9
5
1
16
29.0
16.1
3.2
51.6
Table 3
Neuropsychological Measure Descriptive Statistics
4
13
7
3
3
1
12.9
41.9
22.6
9.7
9.7
3.2
12
5
12
1
1
38.7
16.1
38.7
3.2
3.2
25
3
1
1
1
80.6
9.7
3.2
3.2
3.2
TMT (z score)
WMS-3 LM I
(scaled score)
BVMT-R Delay
(t score)
JOLO (z score)
Letter Fluency
(scaled score)
Agnosia RH
(errors)
Agnosia LH
(errors)
Min.
Max.
Mean
SD
31
19.52
1.18
3.58
4.86
31
2.00
13.00
7.35
3.01
30
31
20.00
1.75
66.00
1.08
46.27
0.02
13.77
0.86
31
3.00
19.00
8.42
3.85
30
0.70
1.06
30
0.37
0.56
trial. The total score is the amount of money earned over all trials.
Higher dollar amounts are indicative of higher levels of cooperation (and theoretically empathy).
Table 4
Subjective and Objective Empathy Measures
Descriptive Statistics
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Min.
Max.
Mean
SD
31
31
31
31
20
32
10
12
3
61
46
22
19
12
79
39.93
17.32
15.61
7.0
71.50
3.79
2.91
2.08
2.56
4.35
Neuropsychological Tests
The following neuropsychological tests were administered as
indices of the general functional integrity of each of the following
cerebral lobes. Specifically, the tests were not used as indicators of
specific cognitive functions, but rather to infer the functional
integrity of the cerebral lobe that is generally associated with the
test (i.e., finger agnosia tests used as indices of parietal lobe
functioning, rather than measures of tactile sensitivity; Lezak,
Howieson, & Loring, 2004). However, it is acknowledged that
only general relationships could be inferred regarding empathy and
neuroanatomical foundations, which was determined to be appropriate given the unclear nature of the neurological foundations of
empathy (Zaki & Ochsner, 2012). For all tests, higher scores
indicate more intact ability, other than for the finger agnosia tests
(i.e., higher scores equal worse performance). Age was controlled
for by calculating standard scores for all tests based on age, other
than for finger agnosia.
RPL. The Judgment of Line Orientation (JOLO; Benton,
Hamsher, Varney, & Spreen, 1983) and left-hand finger agnosia
tests were used to infer RPL functioning. The JOLO is a measure
of spatial perception with the total score equaling the number
correct of the 30 total items. For this study, the score is presented
as a z-score calculated according to normative data published in
the test manual, with higher z -scores indicative of better performance. The JOLO, and similar measures of the perception of
angulation, have been associated with right hemisphere and particularly RPL functioning (Benton, Hannay, & Varney, 1975;
Lezak, Howieson, & Loring, 2004; Meador et al., 1993). Leftsided finger agnosia is a measure of tactile perception that is
associated with the RPL (Lezak et al., 2004). On this test, each of
the five fingers is touched four times and identified by the participant, with the score equaling the total number of errors. More
agnosia errors suggest greater RPL dysfunction.
Left parietal lobe. Right-sided finger agnosia is a measure of
tactile perception associated with the left parietal lobe (Lezak et
al., 2004), during which each of the five fingers is touched four
times and identified by the participant, with the score equaling the
total number of errors. More agnosia errors suggest greater left
parietal dysfunction.
Right temporal lobe. The Brief Visuospatial Memory Test
Revised (BVMT-R; Benedict, 1997) is a test of visual memory that
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has been associated with right temporal lobe functioning (Tranel &
Damasio, 2002). It involves presenting the participant with three
trials during which they are visually exposed to six geometric
figures for 10 s, after which they are asked to draw the figures from
memory. The score is the total number of details recalled for all
three trials, which is presented as a t score based on age-related
normative data (average t score 50, SD 10).
Left temporal lobe. The Wechsler Memory Scale III
(WMS-3) Logical Memory (LM) I subtest (Wechsler, 1997b) is a
measure of verbal memory that has been associated with left
temporal functioning (Tranel & Damasio, 2002). It involves reading two narrative stories to the participant that they are asked to
remember and repeat immediately after presentation. The score is
the standard score according to age-related norms (i.e., M 10,
SD 3).
Left frontal lobe. The Delis Kaplan Executive Function System Letter Fluency Test (DKEFS; Delis & Kaplan, 2001) is a
measure of verbal fluency that has been associated with left frontal
lobe functioning (Johnstone, Leach, Hickey, Frank, & Rupright,
1995). On this measure, participants state as many words as
possible in a 1-min period for three different letters. The total score
is the total number of words generated over the three trials, which
is expressed as a scaled score based on age-related normative data
(M 10, SD 3).
Frontal lobe. The Trail Making Test Part B (Reitan, 1992)
has been associated with general frontal lobe functioning (Johnstone et al., 1995). It is a measure of divided attention (also
described as cognitive flexibility) that involves the participant
completing a connect-the-dot test, alternating between a series of
numbers and letters (i.e., 1 to A, A to 2, 2 to B, B to 3, etc.). The
result is based on time to complete the measure. For this study, the
score is presented as a z score according to normative data (Heaton, Miller, Taylor, & Grant, 2004), with higher z scores indicative
of better performance.
MRI
Data acquisition. A 3T Siemens Trio MRI scanner with a
standard eight-channel head coil was used to obtain highresolution (1 mm3) T1-weighted structural images of the brain.
Images were collected using a standard T1-weighted pulse sequence (MP-RAGE sequence: repetition time [TR] 1,920 ms,
echo time [TE] 4 ms, flip angle 8, number of slices 160,
resolution 1 mm3).
Data processing and analysis. Data processing and analysis
was carried out using a surface-based approach as implemented
within BrainVoyager QX software (Brain Innovation, Maastricht,
The Netherlands). (For a more extensive description of the BrainVoyager processing pipeline, see http://support.brainvoyager.com
or Geuze et al., 2008.) First, the structural MRI data for each
participant was rotated into anterior-posterior commissures (ACPC) coordinates. The skull and dural tissue were then removed by
manually deleting voxels containing non-neural tissue. Next, a
Sigma filter and BrainVoyagers automatic intensity inhomogeneity correction tool (IIHC) were applied to enhance grey/white
matter (GM/WM) tissue contrast and correct for spatial intensity
inhomogeneities, respectively. Noncortical structures (e.g., ventricles, subcortical nuclei) were then removed, and the resulting
image was upsampled from 1 to 0.5 mm3 using sinc interpolation
Table 5
MRI Cortical Volume Descriptive Statistics
Left Hemisphere
Left Temporal
Left Frontal
Left Parietal
Left Insula
Right Hemisphere
Right Temporal
Right Parietal
Right Frontal
Right Insula
Min.
Max.
Mean
SD
20
20
20
20
30,628.05
41,317.70
23,028.63
6,319.09
53,710.81
79,798.30
37,681.60
9,724.08
42,241.44
59,528.84
31,215.89
8,121.69
5,425.12
8,539.29
3,722.84
900.11
19
20
20
20
30,052.48
44,251.37
23,802.39
8,123.95
47,168.65
81,739.61
34,333.18
11,413.30
40,602.12
62,146.05
28,024.57
9,915.95
4,330.72
8,641.45
3,026.48
894.49
Table 6
Correlation Analyses Among Neuropsychological Indices and
Empathy Measures
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Neuropsychological
Total
Left Temporal
WMS-3 LM I
0.24
Left Frontal
DKEFS Letter Fluency
0.52
Left Parietal
Right Finger Agnosia
0.07
Right Temporal
BVMT-R total
0.03
Right Parietal
JOLO
0.04
Left Finger Agnosia
0.21
Frontal
Trail Making Test
0.35
EC
0.16
0.42
Prisoners
Dilemma
PT
PD
0.36
0.14
0.28
0.42 0.08
0.04
0.11
0.06
0.08
0.30
0.24
0.09
0.12
0.07
0.49
0.37
0.20
0.15
0.31
0.16
0.38
0.12
0.37 0.27
0.01
0.39
Note. Total Penner Prosocial Personality Total score; EC Empathetic Concern; PT Perspective Taking; PD Personal Distress; Prisoners Dilemma Prisoners Dilemma Total Earnings; WMS-3 LM I
Wechsler Memory Scale III Logical Memory I; BVMT-R Benton Visual
Memory Test Revised; DKEFS Delis Kaplan Executive Function
Scales; JOLO Judgment of Line Orientation.
p .05.
Results
Neuropsychological Indices
Contrary to hypotheses, the results suggest that empathy is
generally related to increased functional integrity of the RPL.
Specifically, measures of increased RPL functioning (i.e., JOLO
and left-hand finger agnosia tests) were significantly correlated
with both increased affective empathy and less personal distress.
Measures associated with frontal lobe functioning, and particularly the left frontal lobe (i.e., Trail Making Test and DKEFS
Letter Fluency subtest), were significantly and positively correlated with cognitive empathy.
A measure of left temporal lobe functioning (i.e., WMS-3 LM I
scale) was significantly and positively associated with cognitive
empathy.
No neuropsychological measures were related to Prisoners Dilemma scores.
related to increased rather than decreased RPL functional integrity. The process of being empathetic apparently is not associated
with a decreased focus on the self, which allows for an increased
focus on others. Instead, it appears that to empathize with others
that it is necessary to have an intact and relatively strong sense of
the self. That is, if one does not have an intact sense of the self,
then one cannot fully understand and emotionally relate to the
experiences of others. As stated by Cozolino:
empathy is an attempt to experience the inner life of another while
retaining objectivity. In other words, we hold our own perspective in
mind while simultaneously imagining what it is like to be the other. In
order to have empathy, we need to maintain an awareness of our inner
world as we imagine the inner world of others. (Cozolino, 2006, p.
203)
Table 7
Correlation Analysis Among MRI Cortical Volume and
Empathy Measures
MRI Indices
Right and left insular cortices were the only cerebral structures
shown by MRI to be significantly related to subjective measures of
empathy (i.e., Total Empathy, Personal Distress). No MRI indices
of cerebral integrity were significantly related to Prisoners Dilemma scores.
Total
EC
PT
PD
Prisoners
Dilemma
Left Hemisphere
Left Temporal
Left Frontal
Left Parietal
Left Insula
Right Hemisphere
Right Temporal
Right Frontal
Right Parietal
Right Insula
Note. Total Total Empathy; EC Empathetic Concern; PT Perspective Taking; PD Personal Distress; Prisoners Dilemma Prisoners Dilemma Total Earnings.
p .05.
Discussion
0.32
0.12
0.33
0.48
0.18
0.08
0.27
0.06
0.19
0.13
0.25
0.25
0.05
0.20
0.04
0.46
0.04
0.11
0.04
0.15
0.12
0.15
0.02
0.43
0.10
0.17
0.04
0.18
0.13
0.23
0.02
0.29
0.26
0.03
0.07
0.56
0.07
0.12
0.12
0.04
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to perceptual judgment and left-sided tactile sensitivity. If conceptualized in this manner, it can then be inferred that other RPL
functions, such as general self-orientation processes (Austin, 2009;
Decety & Sommerville, 2003; Leigh et al., 2013; Lou et al., 2004;
Uddin et al., 2006; Feinberg & Keenan, 2005b, 2005a; McGlynn &
Schacter, 1989; Mesulam, 2000) are also likely to be diminished.
Of note, the results also indicated that decreased RPL functioning (i.e., JOLO, left-sided finger agnosia) is associated with higher
levels of personal distress. That is, less intact RPL functioning
(and inferentially the sense of self) is associated with a decreased
ability to keep composure under stressful situations (e.g., I tend to
lose control during emergencies; When I see someone who
badly needs help in an emergency, I go to pieces). This suggests
that a stronger sense of the self allows individuals to retain composure in stressful situations and increase their ability to focus on
others. This finding is consistent with beliefs that one must have a
strong sense of the self to empathize with others (Cozolino, 2006).
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Further research regarding the expression of increased and decreased self-orientation processes is also warranted given the multiple studies that suggest that decreased RPL functioning (as measured by the JOLO and/or finger agnosia tests) is associated with
increased transcendence (Johnstone et al., 2012; Johnstone &
Glass, 2008) and increased willingness to forgive (Johnstone et al.,
2012; Johnstone et al., 2014), but decreased empathy (Grattan et
al., 1994; current study). Future research may benefit from determining how increased and decreased self-orientation may be related to other human experiences (e.g., altruism, antisocial personality, etc.), as well as the manner in which self- and other-oriented
neuropsychological processes interact in different human experiences/relationships (Austin, 2009; Fox et al., 2005; Ochsner et al.,
2004).
A primary limitation of the current study is the relatively small
sample size, as the use of a larger sample may lead to a more clear
understanding of the specific nature of empathy (e.g., allow for
investigation of more specific brain regions). The results are further limited in that the current sample included persons with TBI,
which is an injury that typically involves generalized impairment
throughout the brain (Lezak et al., 2004). As a result, only general
inferences can be drawn regarding the neuroanatomical and neuropsychological bases of empathy. Relatedly, the current study is
limited as the MRI data involving cortical volume was viewed by
examining large regions as a whole (i.e., left frontal lobe) rather
than examining more specific regions within each brain region that
have been suggested to be implicated in different dimensions of
empathy (Eslinger, 1998; Shamay-Tsoory et al., 2009). Not focusing on more specific brain regions may have decreased the strength
of the observed relationships and may have contributed to the
insignificant MRI findings.
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