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Neuropsychology

Functional and Structural Indices of Empathy: Evidence


for Self-Orientation as a Neuropsychological Foundation
of Empathy
Brick Johnstone, Dan Cohen, Kirk R. Bryant, Bret Glass, and Shawn E. Christ
Online First Publication, November 17, 2014. http://dx.doi.org/10.1037/neu0000155

CITATION
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

2014 American Psychological Association


0894-4105/14/$12.00 http://dx.doi.org/10.1037/neu0000155

Functional and Structural Indices of Empathy: Evidence for


Self-Orientation as a Neuropsychological Foundation of Empathy
Brick Johnstone, Dan Cohen, Kirk R. Bryant, Bret Glass, and Shawn E. Christ

This document is copyrighted by the American Psychological Association or one of its allied publishers.
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

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

Peretz, 2004; Zaki & Ochsner, 2012). Considered together, these


studies implicate most of the brain in empathy, which is not
surprising given its complexity. This variability in findings is
likely related to the lack of clear definitions of empathy, methodological weaknesses inherent in neuroradiological scanning (Logothetis, 2008), and other methodological issues (e.g., use of selfreport vs. objective measures of empathy; artificiality of
objective empathy measures; structural vs. functional measures of
cerebral integrity; use of clinical and nonclinical samples; Zaki &
Ochsner, 2012).
The majority of research on the neurology of empathy has
involved neuroradiological evaluation of nonclinical populations
engaged in objective computer-based tasks. However, determining
associations between empathy and cerebral regions is complicated
given the numerous other cognitive processes that are engaged
during objective tasks of empathy (e.g., attending to stimuli, listening to instructions, perceiving stimuli, cognitively processing
economic games commonly used in empathy research, etc.; Logothetis, 2008). As a result, the neuroanatomical basis of empathy
has been difficult to determine. An alternative research method has
involved the investigation of populations with brain dysfunction in
which persons with various lesions/disorders are compared with
one another (e.g., persons with left vs. right frontal lobe lesions),
or to healthy control groups, in terms of empathy (Beadle &
Tranel, 2013; de Sousa et al., 2010; Eslinger, 1998; Grattan et al.,
1994; Grattan & Eslinger, 1989; Grattan & Eslinger, 1992; Rankin,
Kramer, & Miller, 2005; Rankin et al., 2006; Shamay-Tsoory et
al., 2004; Shamay-Tsoory, Aharon-Peretz, & Perry, 2009). Using
this method, empathy can be associated with different cerebral
areas (i.e., damage to areas associated with empathy will be

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-

Brick Johnstone, Department of Health Psychology, University of Missouri;


Dan Cohen, Department of Religious Studies, University of Missouri; Kirk R.
Bryant, Department of Health Psychology, University of Missouri; Bret Glass,
Department of Psychological Sciences, University of Missouri; Shawn E.
Christ, Department of Psychological Sciences, University of Missouri.
Correspondence concerning this article should be addressed to Brick Johnstone, Department of Health Psychology, University of Missouri, DC116.88,
Columbia, MO 65212. E-mail: johnstoneg@health.missouri.edu
1

JOHNSTONE, COHEN, BRYANT, GLASS, AND CHRIST

indicative of decreased empathy). However, a weakness in such


research is that only general relationships can be inferred given the
diffuse nature of most brain disorders. Whereas the first method
may lead to overidentification of the cerebral areas/functions specifically associated with empathy, the latter one can only be used
to make general inferences regarding brain-empathy relationships.
In fact, it has been suggested that the two methodologies are
appropriate complements to one another (Rorden & Karnath,
2004).

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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).

Right Hemisphere, Self-Orientation, and Empathy


Empathy has been hypothesized to be related to self/other
differentiation and self/other overlap (Zaki & Ochsner, 2012).
However, the specific nature of such self/other neuropsychological
processes has not been fully elaborated. Recent research on other
complex human experiences/traits (i.e., transcendence, forgiveness) suggests that empathy may have its neuropsychological
foundations in decreased self-orientation associated with the right
hemisphere, and particularly the right parietal lobe (RPL). Research indicates that persons with increasing RPL dysfunction,
from either brain injuries or tumors, report increased spiritual
transcendence (Johnstone, Bodling, Cohen, Christ, & Wegryzn,
2012; Johnstone & Glass, 2008; Urgesi, Aglioti, Skrap, & Fabbro,
2010). This increased transcendence is hypothesized to be related
to decreased self-orientation, or what can be termed increased
selflessness. These studies are further supported by singlephoton emission computed tomography (SPECT) research on Buddhist monks and Franciscan nuns who demonstrate decreased RPL
activity during advanced spiritual practices while reporting increased feelings of selflessness (Newberg, Alavi, Baime, Mozley,
& dAquili, 1997; Newberg et al., 2001; Newberg, Pourdehand,
Alavi, & dAquili, 2003).
Two recently published studies suggest that decreased RPL
functioning is also related to increased willingness to forgive in
populations with both traumatic brain injury (TBI; Johnstone et al.,

2012) and seizures (Johnstone et al., 2014). These studies suggest


that to forgive, one must be willing to decrease focus on the
perceived wrong to the self.
Based on these studies, it is hypothesized that empathy may also
be related to decreased RPL-related self-orientation. Specifically,
it is suggested that one must be selfless to experience spiritual
transcendence, be willing to forgive, and to be empathetic. This
hypothesis is also based on studies that indicate that the right
hemisphere, and particularly the RPL, is primarily related to processing information that is related to the self (Austin, 2009;
Northoff et al., 2006). Numerous studies have consistently demonstrated that the right hemisphere is related to several selfreferential processes, such as recognizing pictures of ones self and
processing autobiographical information/memories (Decety &
Sommerville, 2003; Keenan, McCutcheon, & Pascual-Leone,
2001; Keenan, Nelson, OConnor, & Pascual-Leone, 2001; Leigh
et al., 2013; Lou et al., 2004; Platek, Wathne, Tierney, & Thomson, 2008; Uddin, Molnar-Szakacs, Zaidel, & Iacoboni, 2006).
The relationship between the RPL and self-orientation is also
supported by research with individuals with RPL dysfunction.
They often experience disorders of the self, including anosagnosia and left-sided neglect, in which they have difficulties
creating/processing a coherent sense of the physical and/or
psychic self (Feinberg & Keenan, 2005b; Feinberg & Keenan,
2005a; McGlynn & Schacter, 1989; Mesulam, 2000). When
considered together, these studies suggest that decreased RPLrelated self-orientation (which can be conceptualized as increased selflessness) may also allow individuals to more
easily understand and relate to the experiences of others (i.e., to
be empathetic).

Rationale for Current Study


It was hypothesized that decreased integrity of the RPL (which
is associated with decreased self-orientation) would be related to
increased empathy. To address weaknesses in empathy research to
date, empathy was measured by subjective and objective measures,
and cerebral integrity was measured in terms of both functional
and structural indices. Although the focus of the study was on the
relationship between the RPL and empathy, relationships among
empathy and indices of other cerebral areas were also investigated
to assist in clarifying the neurologic and neuropsychological foundations of empathy.

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

SELF-ORIENTATION AND EMPATHY

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

Penner Prosocial Personality Battery (Penner, Fritzsche,


Craiger, & Freifeld, 1995). This measure was used to assess
several dimensions of empathy and has been used in several
peer-reviewed studies (Finkelstein, Penner, & Brannick, 2005;
Penner, 2002; Penner & Finkelstein, 1998; Skoe, Cumberland,
Eisenberg, Hansen, & Perry, 2002). The Empathy scale assesses
the ability to feel responsibility for and concern about the welfare
of others. This scale is divided into four different scores, including
a total empathy score, as well as individual scores for each of the
following three dimensions of empathy: Empathetic Concern, Perspective Taking, and Personal Distress. All questions are rated on

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

Note. TMT Trail Making Test Part B; WMS-3 LM I Wechsler


Memory Scale III Logical Memory I; BVMT-R Benton Visual Memory
Test Revised; JOLO Judgment of Line Orientation; RH right hand;
LH left hand.

JOHNSTONE, COHEN, BRYANT, GLASS, AND CHRIST

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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Prosocial Personality Battery


Total Empathy
Perspective Taking
Empathic Concern
Personal Distress
Prisoners Dilemma Total Score

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

a five point scale, from 1 (strongly disagree) to 5 (strongly agree).


The score for each scale is the total number endorsed for each
respective scale. The Total Empathy score is the sum of each of the
following three subscales.
Empathetic concern. This subscale includes four questions
and assesses the degree to which individuals are emotionally
concerned with the well-being of others. It includes questions such
as: When I see someone being taken advantage of, I feel kind of
protective toward them; I am often quite touched by things that
I see happen. To be consistent with the terminology of previous
studies, Empathetic Concern is conceptualized as affective empathy. Higher scores suggest more empathetic concern. Cronbachs
alpha for the measure was .67 for the original sample (Penner,
2002; n 1,111).
Perspective taking. This subscale includes five questions and
assesses the degree to which individuals can take the perspective
of others. It includes questions such as: I sometimes try to
understand my friends better by imagining how things look from
their perspective; When I am upset at someone, I usually try to
put myself in their shoes for a while. To be consistent with the
terminology from previous studies, Perspective Taking is conceptualized as cognitive empathy. Higher scores suggest a greater
capacity to take others perspective. Cronbachs alpha for the
measure was .66 for the original sample (Penner, 2002; n
1,111).
Personal distress. This subscale includes three questions and
assesses the degree to which individuals have difficulties dealing
with stressful situations. Example questions include: I tend to lose
control during emergencies; I am usually pretty effective in
dealing with emergencies; and When I see someone who badly
needs help in an emergency, I go to pieces. Higher scores suggest
a higher degree of distress. Cronbachs alpha for the measure was
.77 for the original sample (Penner, 2002; n 1,111).
Prisoners Dilemma task. This computer task that has been
used as an objective measure of empathy/altruism (Batson &
Moran, 1999). Participants are engaged in a task in which they are
told they can cooperate with, or not cooperate with (i.e., defect),
another person (i.e., the same confederate face on the computer
screen for each trial), not knowing if the confederate will themselves cooperate or defect. If the participant and confederate both
choose to cooperate, then they both earn $5. If the participant
defects but the confederate cooperates, then the participant earns
$6 and the confederate $1. If the participant cooperates but the
confederate defects, then the participant earns $1 and the confederate $6. The participants are administered 15 trials twice, and the
participant is informed of the confederates response after each

Functional and Structural Indices of Cerebral


Integrity
The current study evaluated both the functional and structural
integrity of gross cerebral structures that have been shown to be
related to empathy (i.e., bilateral frontal, temporal, parietal, insular
cortices). Both structural and functional indices of cerebral integrity were used given that neuropsychological tests can provide
different information than neuroradiological techniques (Gomar et
al., 2011; Schmand et al., 2014). For example, cerebral abnormalities were detected in only 18% of MRI scans of persons with TBI,
compared with 40% of SPECT scans and 86% of magnetoencephalography evaluations (Lewine et al., 2007).

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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SELF-ORIENTATION AND EMPATHY

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

(the upsampling is required for use of BrainVoyagers advanced


segmentation tools). BrainVoyagers built-in segmentation process, which uses local intensity histograms and computed gradient
fields to adaptively calculate WM, GM, and cerebrospinal fluid
(CSF) boundaries, was then applied. Importantly, before proceeding, the resulting segmentations were visually inspected (slice-byslice) for accuracy and manually corrected where necessary. Cortical thickness measurements were calculated using a Laplace
method (Jones, Buchbinder, & Aharon, 2000) as implemented
within BrainVoyager. For the current study, cortical volume was
chosen as an index of structural cerebral integrity (i.e., cortical
thickness surface area), consistent to other neuroradiological
studies of empathy (Banissy et al., 2012; see Table 5).
Output from the previously described segmentation process was
also utilized to create cortical surface reconstructions of each
hemisphere for each participant. Anatomical alignment of these
surface representations (and thereby the aforementioned cortical
thickness measurements) across participants was accomplished
using BrainVoyagers automatic cortex-based alignment (CBA)
process (Fischl, Sereno, Tootell, & Dale, 1999; Goebel, Esposito,
& Formisano, 2006). CBA represents an iterative adaptive process
whereby curvature information (representing gyral and sulcal folding patterns) is used to align macroanatomical structures (gyri and
sulci) of each participants brain to a standard reference brain
provided in BrainVoyager. Following alignment, average cortical
thickness, surface area, and volume measurements were extracted
for each major cortical region (frontal, parietal, temporal, insular)
of each hemisphere (left, right) of each participant.
Analyses. Pearson productmoment correlations were conducted among the neuropsychological measures and the Penner
Prosocial Personality Battery Empathy scales, and the Prisoners
Dilemma total score (see Table 6). It is noted that age was
accounted for in the analyses through the use of age-corrected
normative data for the neuropsychological measures, other than for
finger agnosia measures. Partial-correlations using age as a covariate were conducted among MRI-derived measures of cortical
volume and the Penner scores, and the Prisoners Dilemma total
score (see Table 7). Statistical significance was set at 0.05, acknowledging weaknesses inherent in using the relatively small
sample size.

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

JOHNSTONE, COHEN, BRYANT, GLASS, AND CHRIST

Table 6
Correlation Analyses Among Neuropsychological Indices and
Empathy Measures

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This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

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)

Although the results were contrary to those hypothesized, they


support others studies that suggest that relatively stronger right
hemisphere functioning, and particularly RPL functioning, is related to increased empathy (Decety & Batson, 2009; Grattan &
Eslinger, 1989; Shamay-Tsoory et al., 2004; Shamay-Tsoory et al.,
2009). For example, Shamay-Tsoory and colleagues (2004) reported that individuals with RPL lesions, but not left parietal lobe
lesions, demonstrated significantly decreased empathy. Similarly,
Grattan and Eslinger (1989) found that the JOLO (i.e., the same
measure used in the current study to infer RPL dysfunction) was
significantly and positively related to empathy in a sample of
individuals with brain dysfunction (r .30 vs. r .38 in the
current study). However, they conceptualized this test as a measure
of perceptual judgment and did not mention this finding in the
abstract given the focus of their study was on the frontal lobes. In
contrast, in the current study, the JOLO was used to infer the
functional integrity of the RPL. Whereas Grattan and Eslinger
concluded that impairments in visual-spatial perception could
potentially be a shared variable among the flexibility and empathy
measures, it is suggested that it may be more appropriate to
interpret these tests as indicators of general RPL functional integrity. Based on this premise, it can then be inferred that empathy is
significantly related to two measures of RPL integrity (i.e., JOLO,
left finger agnosia), rather than suggesting that empathy is related

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.

MRI Brain Region

Total

EC

PT

PD

Prisoners
Dilemma

Empathy and the RPL

Left Hemisphere
Left Temporal
Left Frontal
Left Parietal
Left Insula
Right Hemisphere
Right Temporal
Right Frontal
Right Parietal
Right Insula

The primary goal of the study was to determine if decreased


RPL functioning was related to increased empathy. Contrary to the
hypothesis, the results suggest that certain aspects of empathy are

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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SELF-ORIENTATION AND EMPATHY

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).

Empathy and Other Cerebral


Structures/Neuropsychological Functions
In the current study, empathy (i.e., affective, cognitive, total)
was associated with frontal lobe functioning (and particularly the
left frontal lobe), consistent with several other studies (Decety &
Batson, 2009; Decety & Jackson, 2004; Grattan et al., 1994;
Grattan & Eslinger, 1989; Grattan & Eslinger, 1992; Rankin et al.,
2005; Rankin et al., 2006; Shamay-Tsoory et al., 2004; ShamayTsoory et al., 2009). In general, current and previous results
consistently suggest that cognitive flexibility associated with frontal lobe functioning is necessary for individuals to take the cognitive perspective of others.
The results also support previous studies that indicate that the
temporal lobes are involved in empathy (Decety & Batson, 2009;
Leigh et al., 2013; Rankin et al., 2006). It has been suggested that
empathy may be related to the emotional processing that has been
shown to be related to both the temporal lobes and limbic system,
given their close neural connectivity (Lee & Siegle, 2012; Lezak et
al., 2004; Rankin et al., 2005). However, somewhat unexpectedly,
in the current study, cognitive empathy was associated with increased left temporal lobe functioning, whereas affective empathy
was not. If anything, it could be hypothesized that affective empathy would be related to temporal lobe functioning. The rationale
for this finding is unclear.

Empathy and Structural Indices of Cerebral Integrity


The results indicate that the bilateral insular cortices were the
only structural indices that were significantly associated with
empathy (i.e., Total Empathy and Personal Distress). This finding
is generally consistent with several other studies that implicate the
insula in the experience of empathy (Banissy et al., 2012;
Mutschler et al., 2013). It is speculated that the insula may be
related to empathy given that it has been associated with emotional
processing (and particularly negative emotions such as personal
distress), awareness of internal bodily states (i.e., self-orientation
of internal states), and connecting physiological states of the body
with social emotions such as empathy (Craig, 2009; Critchley,
Wiens, Rotshtein, Ohman, & Dolan, 2004; Karnath, Baier, &
Ngele, 2005).

The lack of significant findings between empathy and other


cerebral areas does not suggest that empathy is solely based in the
insula. The lack of findings is more likely related to the fact that
many individuals with even severe TBI have normal neuroradiological findings (Brasure et al., 2012; Lobato et al., 1986). This
suggests that quantitative structural MRI data may help differentiate groups with brain dysfunction for comparison (e.g., frontal vs.
nonfrontal lesions; Grattan, Bloomer, Archambault, & Eslinger
1994), but may not be appropriate for correlational analyses such
as those conducted in the current study. Regardless, the current
results clearly suggest that future empathy research will benefit
from focusing on the role of the insula.

Self-Report Versus Objective Measures of Empathy


The results indicate that self-report measures of empathy (i.e.,
Penners Prosocial Personality measure) were significantly related
to neuropsychological indices of cerebral integrity, although the
objective measure (i.e., Prisoners Dilemma) was not. This finding
may be reflective of the artificiality associated with using experimental tasks to measure empathy (Zaki & Ochsner, 2012), and
particularly for persons with TBI. Although subjective and objective measures of a construct may frequently be administered together to assure the construct validity of an attribute (e.g., empathy), in this case the constructs measured by the Penner Prosocial
Personality Measure and Prisoners Dilemma appear to be different.

Limitations and Future Directions


It is acknowledged that empathetic processes are much more
complicated from neuroanatomical and neuropsychological perspectives than the conclusions presented in this article. However,
given the weaknesses in empathy research to date (Zaki &
Ochsner, 2012), the current results can provide suggestions for
future research, and particularly how self-orientation relates to
empathy. The current study suggests that different neuropsychological processes associated with different neurological networks
interact in the experience of empathy (e.g., RPL-related selforientation; frontal lobe-related cognitive flexibility; temporal
lobe-related emotional processing; insula-related processing of
internal physical states and social emotions).
To date researchers have generally conceptualized empathy as
involving processes such as self/other discrimination, selfreflection, self/other overlap, and theory of mind (ShamayTsoory et al., 2009; Zaki & Ochsner, 2012). However, these terms
are relatively nonspecific and such terminology may not best
explain the manner by which individuals incorporate the experiences of others into the experience of the self. A more nuanced
explanation for the manner by which specific dimensions of selforientation relate to empathy is needed. Just as language can be
used as a general umbrella term for other more specific communication skills (e.g., expression, comprehension, semantics, syntax,
etc.), self-orientation may be best conceptualized as a general
umbrella descriptor for more specific self-oriented processes (e.g.,
autobiographical memory, body schema perception, selfawareness, self-recognition, self-evaluation, etc.). In fact, a general
model of self-orientation has been proposed, with suggestions that
the self can be conceptualized in terms of a physical self, mental
self, and autobiographical self (Northoff et al., 2006).

JOHNSTONE, COHEN, BRYANT, GLASS, AND CHRIST

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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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Received March 7, 2014


Revision received July 24, 2014
Accepted September 22, 2014

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