Functional and Structural Indices of Empathy

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Neuropsychology

Functional and Structural Indices of Empathy: Evidencefor Self-Orientation as a Neuropsychological Foundationof EmpathyBrick 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


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Functional and Structural Indices of Empathy: Evidence forSelf-Orientation as a Neuropsychological Foundation of Empathy

Brick Johnstone, Dan Cohen, Kirk R. Bryant, Bret Glass, and Shawn E. ChristUniversity 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

toincreasedneuropsychological indices of RPL and frontal lobe (primarily left frontal) functioning. The

only MRI indices associated with empathy were the bilateral insula. Neither functional nor structuralcerebral 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 neuroanat-

omical 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 cor-

tex, 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-

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, method-

ological weaknesses inherent in neuroradiological scanning (Logo-

thetis, 2008), and other methodological issues (e.g., use of self-

report 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, lis-

tening to instructions, perceiving stimuli, cognitively processing

economic games commonly used in empathy research, etc.; Logo-

thetis, 2008). As a result, the neuroanatomical basis of empathyhas 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

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 John-

stone, Department of Health Psychology, University of Missouri, DC116.88,

Columbia, MO 65212. E-mail: [email protected]

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Neuropsychology 2014 American Psychological Association2014, Vol. 29, No. 1, 000 0894-4105/14/$12.00 http://dx.doi.org/10.1037/neu0000155

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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 spe-

cifically 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 areappropriate complements to one another (Rorden & Karnath,

2004).

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 includ-

ing attention, memory, perspective taking, theory of mind, abstract

reasoning, cognitive flexibility, generational fluency, and set shift-

ing (Rankin et al., 2005). More concisely, empathy is generally

conceptualized as involving two primary neuropsychological pro-

cesses 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 flex-

ibility (Grattan et al., 1994; Shamay-Tsoory et al., 2009; Grattan &

Eslinger, 1989), with suggestions that increased cognitive flexibil-

ity 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, forgive-

ness) suggests that empathy may have its neuropsychological

foundations in decreased self-orientation associated with the right

hemisphere, and particularly the right parietal lobe (RPL). Re-

search 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 single-

photon emission computed tomography (SPECT) research on Bud-

dhist monks and Franciscan nuns who demonstrate decreased RPL

activity during advanced spiritual practices while reporting in-

creased 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. Thishypothesis is also based on studies that indicate that the right

hemisphere, and particularly the RPL, is primarily related to pro-

cessing information that is related to the self (Austin, 2009;

Northoff et al., 2006). Numerous studies have consistently dem-

onstrated that the right hemisphere is related to several self-

referential 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, & Thom-

son, 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 anosag-

nosia 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 RPL-

related self-orientation (which can be conceptualized as in-

creased 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 (whichis 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 foun-

dations of empathy.

Methods

ParticipantsThe sample included 31 individuals with TBI referred for out-

patient neuropsychological evaluations at a Midwestern university.

All participants had abnormal clinical radiologic evaluations of the

brain. Neuropsychological tests and self-report measures of empa-

thy 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

ttests conducted between the 20 participants with and 11 partic-

ipants without MRI scanning indicated there were no significant

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differences in neuropsychological, demographic, or outcome mea-

sures 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

1787). 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 wasnot significantly correlated with any measure of empathy. Demo-

graphic characteristics of the entire sample are presented in Table 1.

TBI injury severity characteristics are presented in Table 2.

Procedure

All participants were referred for clinical neuropsychological

evaluations and had evidence of abnormal neuroradiological eval-

uations at the time of their injuries. They were administered

measures of the functional integrity of the brain including intelli-

gence, memory, language, visual-spatial skills, attention, and

sensory-motor skills by psychometricians (see Table 3). Partici-

pants provided informed consent and completed subjective mea-

sures of empathy (see Table 4). Participants were then scheduledfor 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 werecompensated $100. The present study was approved by the uni-

versitys research review board.

Measures of Empathy

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 assessesthe 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, Per-

spective Taking, and Personal Distress. All questions are rated on

Table 1

Sample Demographics

N Percent

GenderMale 21 67.7Female 10 32.3

HandednessRight 28 90.3Left 3 9.7

EthnicityWhite 28 90.0African American 1 3.2Biracial 2 6.5

Marital StatusMarried 9 29.0Divorced 5 16.1Separated 1 3.2Single 16 51.6

EducationSome HS 4 12.9HS Diploma 13 41.9Some College 7 22.6Bachelors Degree 3 9.7Masters Degree 3 9.7PhD/JD/MD 1 3.2

Employment StatusCurrently Employed 12 38.7Student 5 16.1Unemployed, not on disability 12 38.7Unemployed, on disability 1 3.2Retired 1 3.2

Annual Income$20,000 25 80.6$20,001$40,000 3 9.7$40,001$60,000 1 3.2$60,001$80,000 1 3.2$80,000 1 3.2

Table 3

Neuropsychological Measure Descriptive Statistics

N Min. Max. Mean SD

TMT (z score) 31 19.52 1.18 3.58 4.86WMS-3 LM I

(scaled score) 31 2.00 13.00 7.35 3.01BVMT-R Delay

(tscore) 30 20.00 66.00 46.27 13.77JOLO (z score) 31 1.75 1.08 0.02 0.86Letter Fluency

(scaled score) 31 3.00 19.00 8.42 3.85Agnosia RH

(errors) 30 0 4 0.70 1.06Agnosia LH

(errors) 30 0 2 0.37 0.56

Note. TMT Trail Making Test Part B; WMS-3 LM I WechslerMemory Scale III Logical Memory I; BVMT-R Benton Visual MemoryTest Revised; JOLO Judgment of Line Orientation; RH right hand;LH left hand.

Table 2

Sample Brain Injury Characteristics

N Percent

Loss of ConsciousnessYes 18 58.1

No 5 16.1Unknown/Missing 8 25.8Retrograde Amnesia

Yes 9 29.0No 0 0.0Unknown/Missing 22 71.0

Posttraumatic AmnesiaYes 14 45.2No 0 0.0Unknown/Missing 17 54.8

Effected Brain Regions on ImagingLeft Frontal 9 29.0Right Frontal 7 22.6Left Temporal 7 22.6Right Temporal 7 22.6Left Parietal 6 19.4Right Parietal 4 12.9

Occipital 2 6.5

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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 empa-

thy. 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 concep-tualized 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 them-

selves 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 confed-

erate $6. The participants are administered 15 trials twice, and the

participant is informed of the confederates response after each

trial. The total score is the amount of money earned over all trials.

Higher dollar amounts are indicative of higher levels of coopera-

tion (and theoretically empathy).

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 integ-

rity were used given that neuropsychological tests can provide

different information than neuroradiological techniques (Gomar et

al., 2011; Schmand et al., 2014). For example, cerebral abnormal-

ities were detected in only 18% of MRI scans of persons with TBI,

compared with 40% of SPECT scans and 86% of magnetoen-

cephalography evaluations (Lewine et al., 2007).

Neuropsychological Tests

The following neuropsychological tests were administered as

indices of thegeneralfunctional 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 appro-

priate 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, otherthan 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 perfor-

mance. The JOLO, and similar measures of the perception of

angulation, have been associated with right hemisphere and par-

ticularly RPL functioning (Benton, Hannay, & Varney, 1975;

Lezak, Howieson, & Loring, 2004; Meador et al., 1993). Left-

sided 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 partic-

ipant, 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

Table 4

Subjective and Objective Empathy Measures

Descriptive Statistics

N M in. Max. Mean SD

Prosocial Personality Battery

Total Empathy 31 32 46 39.93 3.79Perspective Taking 31 10 22 17.32 2.91Empathic Concern 31 12 19 15.61 2.08Personal Distress 31 3 12 7.0 2.56

Prisoners Dilemma Total Score 20 61 79 71.50 4.35

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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 tscore based on age-related

normative data (average tscore 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 read-

ing 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 Sys-

tem 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 (John-

stone 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 (Hea-

ton, Miller, Taylor, & Grant, 2004), with higherz 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 high-

resolution (1 mm3) T1-weighted structural images of the brain.

Images were collected using a standard T1-weighted pulse se-

quence (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 Brain-

Voyager 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 (AC-

PC) 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 inhomogene-

ity 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., ventri-

cles, 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 pro-

cess, which uses local intensity histograms and computed gradient

fields to adaptively calculate WM, GM, and cerebrospinal fluid

(CSF) boundaries, was then applied. Importantly, before proceed-

ing, the resulting segmentations were visually inspected (slice-by-

slice) for accuracy and manually corrected where necessary. Cor-tical 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 fold-

ing 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 con-

ducted 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 cova-

riate 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, ac-

knowledging weaknesses inherent in using the relatively small

sample size.

Table 5

MRI Cortical Volume Descriptive Statistics

N Min. Max. Mean SD

Left HemisphereLeft Temporal 20 30,628.05 53,710.81 42,241.44 5,425.12Left Frontal 20 41,317.70 79,798.30 59,528.84 8,539.29Left Parietal 20 23,028.63 37,681.60 31,215.89 3,722.84Left Insula 20 6,319.09 9,724.08 8,121.69 900.11

Right HemisphereRight Temporal 19 30,052.48 47,168.65 40,602.12 4,330.72Right Parietal 20 44,251.37 81,739.61 62,146.05 8,641.45Right Frontal 20 23,802.39 34,333.18 28,024.57 3,026.48Right Insula 20 8,123.95 11,413.30 9,915.95 894.49

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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 particu-

larly the left frontal lobe (i.e., Trail Making Test and DKEFS

Letter Fluency subtest), were significantly and positively corre-

lated 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 Di-

lemma scores.

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 Di-

lemma scores.

Discussion

Empathy and the RPL

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

related to increased rather than decreasedRPL functional integ-

rity. 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 theexperiences 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 re-

lated 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) re-ported 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 empathymeasures, it is suggested that it may be more appropriate to

interpret these tests as indicators of general RPL functional integ-

rity. 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 Brain Region Total EC PT PDPrisonersDilemma

Left HemisphereLeft Temporal 0.32 0.18 0.19 0.05 0.04Left Frontal 0.12 0.08 0.13 0.20 0.11Left Parietal 0.33 0.27 0.25 0.04 0.04Left Insula 0.48 0.06 0.25 0.46 0.15

Right HemisphereRight Temporal 0.12 0.10 0.13 0.26 0.07Right Frontal 0.15 0.17 0.23 0.03 0.12Right Parietal 0.02 0.04 0.02 0.07 0.12Right Insula 0.43 0.18 0.29 0.56 0.04

Note. Total Total Empathy; EC Empathetic Concern; PT Per-spective Taking; PD Personal Distress; Prisoners Dilemma Prison-ers Dilemma Total Earnings. p .05.

Table 6

Correlation Analyses Among Neuropsychological Indices and

Empathy Measures

Neuropsychological Total EC PT PDPrisonersDilemma

Left TemporalWMS-3 LM I 0.24 0.16 0.36 0.14 0.28Left Frontal

DKEFS Letter Fluency 0.52 0.42 0.42 0.08 0.04Left Parietal

Right Finger Agnosia 0.07 0.11 0.06 0.08 0.30Right Temporal

BVMT-R total 0.03 0.24 0.09 0.12 0.07Right Parietal

JOLO 0.04 0.38 0.12 0.49 0.20Left Finger Agnosia 0.21 0.37 0.27 0.37 0.15

FrontalTrail Making Test 0.35 0.01 0.39 0.31 0.16

Note. Total Penner Prosocial Personality Total score; EC Empa-thetic Concern; PT Perspective Taking; PD Personal Distress; Pris-oners Dilemma Prisoners Dilemma Total Earnings; WMS-3 LM I

Wechsler Memory Scale III Logical Memory I; BVMT-R Benton VisualMemory Test Revised; DKEFS Delis Kaplan Executive FunctionScales; JOLO Judgment of Line Orientation. p .05.

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to perceptual judgment and left-sided tactile sensitivity. If concep-

tualized 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 function-ing (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 com-

posure 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 FunctionsIn 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; Shamay-

Tsoory et al., 2009). In general, current and previous results

consistently suggest that cognitive flexibility associated with fron-

tal lobe functioning is necessary for individuals to take the cogni-

tive 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 thatempathy 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 in-

creased left temporal lobe functioning, whereas affective empathy

was not. If anything, it could be hypothesized that affective em-

pathy 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 neuroradio-

logical findings (Brasure et al., 2012; Lobato et al., 1986). This

suggests that quantitative structural MRI data may help differen-

tiate 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 ex-

perimental tasks to measure empathy (Zaki & Ochsner, 2012), andparticularly for persons with TBI. Although subjective and objec-

tive measures of a construct may frequently be administered to-

gether to assure the construct validity of an attribute (e.g., empa-

thy), in this case the constructs measured by the Penner Prosocial

Personality Measure and Prisoners Dilemma appear to be differ-

ent.

Limitations and Future Directions

It is acknowledged that empathetic processes are much more

complicated from neuroanatomical and neuropsychological per-

spectives 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 forfuture research, and particularly how self-orientation relates to

empathy. The current study suggests that different neuropsycho-

logical processes associated with different neurological networks

interact in the experience of empathy (e.g., RPL-related self-

orientation; 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, self-

reflection, self/other overlap, and theory of mind (Shamay-

Tsoory 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 experi-

ences of others into the experience of the self. A more nuanced

explanation for the manner by which specific dimensions of self-

orientation relate to empathy is needed. Just as language can be

used as a general umbrella term for other more specific commu-

nication 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, self-

awareness, 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).

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Further research regarding the expression of increased and de-

creased self-orientation processes is also warranted given the mul-

tiple studies that suggest that decreased RPL functioning (as mea-

sured by the JOLO and/or finger agnosia tests) is associated with

increased transcendence (Johnstone et al., 2012; Johnstone &

Glass, 2008) andincreasedwillingness to forgive (Johnstone et al.,

2012; Johnstone et al., 2014), but decreasedempathy (Grattan etal., 1994; current study). Future research may benefit from deter-

mining how increased and decreased self-orientation may be re-

lated to other human experiences (e.g., altruism, antisocial person-

ality, etc.), as well as the manner in which self- and other-oriented

neuropsychological processes interact in different human experi-

ences/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 fur-

ther limited in that the current sample included persons with TBI,

which is an injury that typically involves generalized impairmentthroughout the brain (Lezak et al., 2004). As a result, only general

inferences can be drawn regarding the neuroanatomical and neu-

ropsychological 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 focus-

ing 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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Functional and Structural Indices of Empathy