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Neural responses to perceiving suffering in humans

and animalsRobert G. Franklin Jr.

a , Anthony J. Nelson

b , Michelle Baker

b , Joseph E. Beeney

b ,

Theresa K. Vesciob , Aurora Lenz-Watson

b & Reginald B. Adams Jr.

b

a Department of Psychology, Brandeis University, Waltham, MA, USA

b Department of Psychology, The Pennsylvania State University, University Park, PA, USA

Version of record first published: 13 Feb 2013.

To cite this article: Robert G. Franklin Jr. , Anthony J. Nelson , Michelle Baker , Joseph E. Beeney , Theresa K. Vescio ,

Aurora Lenz-Watson & Reginald B. Adams Jr. (2013): Neural responses to perceiving suffering in humans and animals, SocialNeuroscience, DOI:10.1080/17470919.2013.763852

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SOCIAL NEUROSCIENCE, 2013http://dx.doi.org/10.1080/17470919.2013.763852

Neural responses to perceiving suffering in humansand animals

Robert G. Franklin Jr.1 , Anthony J. Nelson2 , Michelle Baker 2 , Joseph E. Beeney2 ,

Theresa K. Vescio2 , Aurora Lenz-Watson2 , and Reginald B. Adams Jr.2

1Department of Psychology, Brandeis University, Waltham, MA, USA2Department of Psychology, The Pennsylvania State University, University Park, PA, USA

The human ability to perceive and understand others’ suffering is critical to reinforcing and maintaining our social

bonds. What is not clear, however, is the extent to which this generalizes to nonhuman entities. Anecdotal evidence

indicates that people may engage in empathy-like processes when observing suffering nonhuman entities, but

psychological research suggests that we more readily empathize with those to whom we are closer and more

similar. In this research, we examined neural responses in participants while they were presented with pictures of

human versus dog suffering. We found that viewing human and animal suffering led to large overlapping regions

of activation previously implicated in empathic responding to suffering, including the anterior cingulate gyrus

and anterior insula. Direct comparisons of viewing human and animal suffering also revealed differences such

that human suffering yielded significantly greater medial prefrontal activation, consistent with high-level theory of

mind, whereas animal suffering yielded significantly greater parietal and inferior frontal activation, consistent with

more semantic evaluation and perceptual simulation.

Keywords: Empathy; Emotion; Mentalizing; Anthropomorphism.

Perceiving suffering in others can elicit powerfulresponses in observers. We readily empathize with

the suffering of others, feeling their pain as our own.

Anecdotal evidence suggests that this extends to ani-

mals as well, as images of animal suffering evoke

strong responses in humans. Stories of animal suffer-

ing and abuse capture media headlines as do stories

of human suffering. For example, in the midst of

the devastating earthquake and tsunami in Japan in

March 2011, a video of a dog staying with another

suffering dog captured as much international atten-

tion as any story of human suffering. Additionally,

animal rights groups often present explicit photos of

abused animals in an attempt to effect change in animal

treatment policies. Even fictitious images of animal

Correspondence should be addressed to: Robert G. Franklin, Jr., Department of Psychology, Brandeis University, 415 South Street, Mailstop

062, Waltham, MA 02454, USA. E-mail: [email protected] and Reginald B. Adams, Jr., Department of Psychology, 464 Moore Building,

University Park, PA 16802, USA. E-mail: [email protected]

This research was supported by a Social Science Research Institute grant, Penn State University, to R. B. A., Jr. We acknowledge Amanda

Gearhart and David Pennell for their help with data collection and Jasmine Boshyan for her helpful comments on an earlier version of this

article.

suffering can produce horror and outrage in viewers.Director Francis Ford Coppola said of The Godfather ,

“Thirty people were shot in the movie, but people

only talked about ‘cruelty to animals,’ ” which was a

response to the severed horse head found in a char-

acter’s bed (as quoted in Kohn, 1990). Anecdotal

evidence suggests that animal suffering arouses similar

responses as human suffering (e.g., Kennedy, 1992);

however, some psychological research indicates that

thinking about human mental states is distinct from

thinking about animal states (e.g., Caramazza &

Shelton, 1998). This points to an intriguing question;

namely, do images of suffering in humans and animals

elicit similar empathy-related processes at the neural

level?

© 2013 Taylor & Francis

mailto:[email protected]

mailto:[email protected]



2 FRANKLIN ET AL.

SUFFERING IN HUMANS ANDANIMALS

A large social and political movement decries human-

caused animal suffering, calling for the end of the

use of animals for food, as beasts of burden, and forsport (Singer, 1975). This movement is largely based

on the philosophical and ethical premise that animal

suffering is morally equivalent to human suffering

(Singer, 1974). Despite anecdotal evidence and ethi-

cal appeals suggesting the equivalency of human and

animal suffering, research on how humans perceive

suffering has almost exclusively examined responses

to other humans. This is partly because humans are

assumed to have a set of mental experiences that are

distinct from those that animals possess (Kennedy,

1992). This is also partly due to the fact that we pro-

cess our knowledge of humans in different, and neu-

rally dissociable, cognitive substrates compared with

knowledge of nonhuman beings or inanimate objects

(Caramazza & Shelton, 1998). For instance, judging if

a word describes a possible action of a human agent

yields greater activation in medial prefrontal regions,

whereas judging if a word describes an action a dog

can perform leads to greater activation in more tem-

poral regions (Mason, Banfield, & Macrae, 2004).

This suggests that thinking about humans and thinking

about animals recruit qualitatively different processes.

In the context of this study, the aforementioned

findings suggest that processing suffering in humans

may lead to greater activation of networks involvedin understanding others’ mental states. Several mental

processes are necessary to understand others’ suffer-

ing. These include the ability to decode what another

is thinking, represent an individual’s mental and/or

emotional state, take that person’s perspective, reg-

ulate emotions generated through identification with

another’s suffering, and maintain awareness of the

boundaries between self and others (Decety, 2007).

These processes elicit activation in a variety of brain

regions, three of which are particularly relevant to the

present research.

First, viewing others in pain consistently activates

the dorsal anterior cingulate (dACC) and the ante-rior insula (AI). These regions are part of a network

involved in alerting organisms of threats and dan-

gers in their environment and representing one’s own

emotional states. Specifically, the anterior cingulate

and AI are part of a network involved with rep-

resentations of self and others’ affective states and

are important in homeostatic regulation (Craig, 2002;

Singer, Critchley, & Preuschoff, 2009). The dACC is

involved in error detection and performance monitor-

ing (Holroyd et al., 2004). In regard to perceiving

threats in the environment and empathy more specifi-

cally, the dACC is thought to be akin to a neural alarm

system, active when something is “off” physiologi-

cally (Eisenberger & Lieberman, 2004). In addition,

the dACC is involved in emotion regulation (Davidson,

Putnam, & Larson, 2000). The AI is involved withintegrating somatic and emotional information and is

active when witnessing others in pain, as well as being

active in situations evoking disgust and a sense of

unfairness (Ostrowsky et al., 2002). These regions are

consistently found in studies of empathy for pain and

are thought to reflect a core network involved with

perceiving the suffering of others, whether this knowl-

edge is based on actually perceiving someone in pain

or if a person is told that another is suffering (Lamm,

Decety, & Singer, 2011). Further, shared activation in

these regions supports the hypothesis that the vicarious

experience of pain involves some of the same neural

processes as directly experiencing pain (Singer et al.,2004).

Second, brain regions involved with decoding what

others are thinking are involved in empathy for the suf-

fering of others. The medial prefrontal cortex (mPFC)

is important to mentalizing, or understanding the

behaviors of oneself or others in terms of mental

states, and is active in many studies involving decod-

ing what another is feeling (Amodio & Frith, 2006).

More apropos to perceiving suffering in others, learn-

ing a close other is in pain leads to mPFC activation

(Singer et al., 2004), perspective taking, and empathy

arousal (Cheng, Chen, Lin, Chou, & Decety, 2010).

In regard to empathy, mPFC activation may reflect

the importance of self-awareness and taking the per-

spective of others, as lesions of the ventral mPFC

and orbitofrontal cortex lead to deficits in empathy

(Eslinger, 1998; Rankin et al., 2006; Sturm, Rosen,

Allison, Miller, & Levenson, 2006) and these regions

are involved in taking another’s emotional perspec-

tive (Hynes, Baird, & Grafton, 2006). Additionally,

the ventral mPFC is involved with processing intero-

ceptive information important for understanding the

affective significance of stimuli (Decety & Michalska,

2010).

Third, another region implicated in understand-ing others is the inferior frontal gyrus (IFG). The

IFG is part of a set of regions involved with action

understanding and its role in empathy may be in

predicting and understanding action sequences. The

IFG is thought to be part of empathy in regard to

emotional contagion processes, possibly due to simu-

lating others’ emotional states and feeling those same

emotions (Preston & de Waal, 2002; Shamay-Tsoory,

Aharon-Peretz, & Perry, 2009). In addition, the IFG is

important in attentional processes. The IFG, especially



NEURAL RESPONSES TO SUFFERING 3

right-lateralized, is active in attentional tasks involving

detecting important stimuli (Hampshire, Chamberlain,

Monti, Duncan, & Owen, 2010). The IFG along with

the inferior parietal cortex was more active for empa-

thy when it was elicited via pictures of suffering rather

than cues indicating another was suffering (Lammet al., 2011) and is also active in tasks involving

mentalizing based on perceptual information (e.g.,

Adams et al., 2010), which indicates the importance

of this region in empathy tasks based on perceiv-

ing another’s suffering. In addition, IFG activation is

higher when watching closer friends suffer, mediat-

ing the relationship between friendship and empathy-

related responses in the dACC, which may indicate the

importance of the IFG in greater levels of empathy

for those with whom we are closer (Beeney, Franklin,

Levy, & Adams, 2011).

Despite the fact that almost all of the prior research

on empathy has examined empathy for human suffer-ing, there is some work that has examined empathy

for suffering for animals. Plous (1993, 2003) has

examined human responses to suffering in animals,

especially how it is relevant to whether humans use

animals for human gain. In this research, Plous (1993)

found that the degree to which people perceive similar-

ity with an animal species affects how much empathy

is attributed to suffering animals. Animals consid-

ered more similar to humans were judged as being

more capable of perceiving pain. Further, when par-

ticipants viewed suffering animals, those animals who

were judged as more similar to humans elicited greater

skin conductance responses, indicating that perceiving

suffering in those animals aroused more anxiety in par-

ticipants than perceiving suffering in animals judged to

be less similar to humans.

To our knowledge, only one prior study has com-

pared neural differences in the perception of suffering

in animals and humans. Filippi et al. (2010) exam-

ined responses of vegans, vegetarians, and omnivores

perceiving negatively valenced images of injured and

dead animals in food processing contexts comparing

these to threatening images of violence in humans. For

human suffering, more activation was apparent in the

middle temporal gyrus and precuneus, while animalsuffering led to more activation in the IFG. The ACC

was involved in perceiving suffering in both humans

and animals. Vegetarians and vegans also had greater

responses to animal suffering in several areas involved

with empathy, including the ACC, mPFC, and amyg-

dala. This study examined empathy for animals in

the context of explicit pictures of physical suffering

involving food processing and dietary preferences and

thus could reflect highly charged beliefs and regula-

tory processes due to complicity in the suffering of

animals involved in food processing. In the present

study, we attempted to control for these by examining

whether different neural responses are engaged when

viewing the suffering of humans and dogs, which are

animals we typically engage in a social rather than

dietary manner.

The present research

In our study, we examined neural differences while

people viewed images of humans and dogs suffering.

We chose to use dogs because people are regularly

exposed to dogs and tend to assume that dogs have

greater cognitive abilities than many other animals

(Serpell, 1986). In many ways, humans anthropomor-

phize dogs, extending processes used in understanding

other people to how they understand dogs. People

show high consensus when rating how well Big Five

personality traits apply to pictures of dogs, suggesting

shared implicit knowledge as to how they are assess-

ing dogs’ personalities (Gosling, Kwan, & John, 2003;

Kwan, Gosling, & John, 2008). Further, people also

extend appearance stereotypes found in humans to

their perceptions of dogs, rating more attractive dogs

as having more positive traits and rating more baby-

ish appearing dogs as being more childlike (Zebrowitz

et al., 2011). Dogs may also have a unique abil-

ity among animals to understand humans as well,

as there is evidence that the domestication of dogs

led them to better read human affective states (Hare,Brown, Williamson, & Tomasello, 2002). Darwin even

ascribed human affective states to his dog—such as

joy, guilt, and disappointment—and did not doubt the

“communication and empathy” present between him

and his dog (see Buck & Ginsburg, 1997). Based on

human familiarity and beliefs about the cognitive abili-

ties of dogs, we believed that perceiving dogs suffering

would likely evoke the most powerful responses of

empathy in humans compared to other animals, partic-

ularly those that are commonly associated with dietary

consumption in this culture.

In this study, we examined contrasting predictions

regarding whether the perception of suffering animalsand humans would elicit similar or distinct neural

responses related to empathy. On the one hand, anec-

dotal evidence and anthropomorphism suggests that

we show high levels of empathy for animals, which

leads to the prediction that little difference would be

found in the empathic responses elicited in people who

are viewing animals and human suffering. On the other

hand, empathy research suggests that the degree to

which people empathize with others varies as a func-

tion of perceived similarity they have to the self, which



4 FRANKLIN ET AL.

might lead one to expect that empathizing with other

humans would activate different neural networks than

when viewing suffering animals.

In addition, one possible reason for differences

in empathy in perceiving suffering in animals and

humans is the possibility that animals elicit greaterempathy due to their perceived helplessness. Empathy-

related responses, such as providing help, are related

to the perceived helplessness of a suffering victim

(Batson et al., 1997; Weiner, 1980). It is possible that

suffering dogs may be seen as more helpless than suf-

fering humans, who by their very nature may be more

responsible for the situations that place them in suffer-

ing. We examined empathy-related neural activation to

suffering children and adults along with suffering adult

dogs and puppies in order to examine this question,

under the supposition that suffering children would be

seen as helpless victims and if helplessness is respon-

sible for differences in neural activation in perceivingsuffering in humans versus animals, these differences

would be weaker in comparisons between children and

puppies than in comparisons between adult dogs and

humans.

To investigate these questions, we examined neu-

ral responses of participants as they perceived images

of suffering humans and dogs. We predicted that per-

ceiving suffering for humans would elicit activation

in brain regions previously implicated in empathy

for the suffering of others, particularly the ACC and

AI. However, as mentioned above, we had compet-

ing predictions as to whether these responses would

extend to animals. Further, we predicted that viewing

suffering in humans compared to animals would acti-

vate regions involved in understanding others’ men-

tal states, including the mPFC (Mason et al., 2004),

whereas perceiving empathy in animals compared

to humans would more likely involve activation in

regions involved in perceptual simulation, such as the

IFG, as was previously found (Filippi et al., 2010).

METHOD

Participants

Seventeen White participants (9 women, 8 men) partic-

ipated for course credit. Participants were either under-

graduate or graduate students, right-handed, under

25 years of age, had normal or corrected to normal

vision, and were free of any history of neurological

problems. Two other participants were dropped for

excess movement in the scanner (>6 mm over the run

while all other participants had <2 mm of movement

over the run). Participants provided informed consent

before completing the study and all study procedures

were approved by the Pennsylvania State University

Institutional Review Board.

Stimuli

One hundred and twenty images of suffering were

selected, with 80 images of humans and 40 images of

dogs suffering. Forty of the images of humans suffer-

ing were of White individuals while 40 images were of

Black individuals.1 Images were selected from Internet

sources and included a wide variety of potential sit-

uations involving suffering, including an equal repre-

sentation of depictions of starvation, physical pain, or

apparent affective suffering across conditions. Further,

images were selected to be free of explicit displays of

blood or gore to avoid responses due to the images

being highly arousing or disgust responses due to vio-

lent displays. We ensured that each group was matchedon how much the individuals looked toward or away

the camera and how near the bodies of the individ-

uals were to the camera. Further, half of the images

were of mature adult humans and dogs and half were

of immature children and puppies.2

Images were pre-rated by an independent sample

of 17 undergraduates (7 female, 10 male) recruited

from the same participant population. Ratings were

made on how much the target in each picture appeared

to be suffering using a seven point scale, with end-

points defined as 1 = not much suffering to 7 = very

much suffering. Responses ranged from a minimum of

2.72 and maximum of 6.56 ( M = 4.51, SD = 0.76).

There were no significant differences in the ratings

of humans and animals in the images selected for the

fMRI participants t (101) = 1.10, p > .27.

Design and procedure

Participants completed one run of the fMRI task where

they viewed images of suffering humans, and dogs.

Participants were instructed that they would see a

series of blocks of images and to merely pay attention

to the images, with no other instructions given about

1 We included same-race and other-race individuals here in order

to examine if any human-specific empathy responses generalized to

other-race individuals. Research examining infrahumanization indi-

cates that humans may not attribute human-like emotional states to

outgroup individuals (e.g., Leyens et al., 2000), thus suggesting that

empathy foroutgroup sufferingmay be more comparable to empathy

for nonhuman entities.2 In addition to the analysis reported here, we compared neural

responses for perceiving suffering in White individuals versus dogs

and Black individuals versus dogs. In these analyses, we found the

same results as reported here, with activations in all the same areas

reported at the threshold we use for this analysis.




the images. Participants passively viewed 35 blocks,

10 blocks each of Black individuals, White individ-

uals, and dogs, and 5 blocks of 16 second baseline

fixation. Human images were blocked by race in order

to explore the potential of any cross-race effects. For

each group, five blocks showed mature humans or dogssuffering and five blocks showed immature humans

or dogs suffering. Each block consisted of four pho-

tos, each shown for 3.5 seconds, with a 0.5 second

inter-trial fixation dividing each of the four stimuli.

Thus, each of the 120 images were shown only once

during the entire paradigm. Photos were shown in

random order within blocks for each participant and

blocks were shown sequentially with no time between

blocks. The order of the blocks was pseudo-randomly

determined in order to ensure that the same condi-

tions were not repeated from block to block, with

nine participants viewing one order, and the remain-

ing eight viewing the reverse order. The total run timewas 9 minutes and 20 seconds.

Scanning parameters and analysis

Functional data were collected using a 3T Siemens

Tim-Trio (Siemens AG, Munich, Germany) using

echo-planar imaging with 1 run of 280 T2∗ images

(TR, 2000 ms; TE, 25 ms; 38 interleaved slices; trans-

verse orientation; 3.5 mm slice thickness; 0.5 mm

gap; and voxel size 3.5 mm3). We used SPM8 soft-

ware to process data (Wellcome Institute, London,

UK) using standard six-parameter realignment, coreg-istration of the mean functional image to each subject’s

T1 anatomical image, segmentation of the anatom-

ical image, normalization of functional images to

the Montreal Neurological Institute (MNI) template

using parameters derived from segmentation, and then

smoothing using an 8 mm FWHM Gaussian kernel.

We analyzed functional data using a mass-

univariate general linear model (GLM) approach. For

each subject, we generated first-level fixed-effects con-

trasts for each of the various conditions minus base-

line activation. These first-level contrast images were

then used as the basis for a second-level random-

effects analysis. Second-level random-effects analysesproduced t -statistic maps which were thresholded at

p < .05 false-discovery rate (FDR) corrected, five

voxel cluster extent.

RESULTS

Overlapping activation

In order to assess whether there were regions that

were mutually active for perceiving both human and

animal suffering, we conducted a conjunction analysis

examining activation that was commonly associated

with both human and animal suffering. In order to

examine the overlap between these two conditions, we

computed a conjunction analysis using each of the con-

trasts to baseline (see Friston, Holmes, Price, Büchel,

& Worsley, 1999). However, in order to ensure thatthe areas significant in the conjunction analysis were

significantly active in each condition separately (i.e.,

human minus baseline fixation as well as dog minus

baseline fixation), we created an inclusive mask for

the conjunction analysis for areas that were significant

for both human and animal suffering. To create this

mask, we generated SPM maps of active voxels at the

threshold of p < .05 FDR corrected, five voxel extent

for human suffering minus baseline activation and ani-

mal suffering minus baseline activation and created a

mask of the union of areas significant for both of these

analyses.

This analysis revealed activation in three criticalareas relevant to empathy. First, we found activation

of the bilateral AI and anterior cingulate in both con-

ditions, as well as in the posterior cingulate and cere-

bellum (see Table 1 and Figure 1). This is consistent

with the notion that perceiving animal suffering elicits

empathy-related responses in a similar way as perceiv-

ing human suffering. Second, we found activation of

the mPFC and the IFG. These are regions of the brain

thought to be involved in mentalizing and shown to be

activated in perception of pain in humans. Importantly,

here, we find these areas to be activated when people

perceive pain in both animals and humans. Although

we found differences in the recruitment of these two

areas for human versus animal suffering in the compar-

isons reported above, their conjunction here suggests

that they reflect predominant, though still overlapping

responses.

Differences between humans and dogs

In order to examine differences in suffering between

humans and animals, we conducted a three (type

of sufferer: Black individual, White individual, ordog) within-subjects analysis of variance (ANOVA).

We used this analysis to examine planned contrasts

evaluating differences in suffering for humans versus

animals.

Overall, this ANOVA revealed significant interac-

tions in a network of regions involved with empathy,

including the bilateral parietal cortex, precuneus, and

lateral prefrontal cortex, as well as the left AI, the

bilateral premotor cortex, and dorsal and ventral pre-

frontal cortex (see Table 2). In order to examine

differences in empathy due to race or perceived age of



6 FRANKLIN ET AL.

TABLE 1

Regions of common activation for human and animal

suffering. Peaks and t -values reflect significant peaks for the

conjunction between the three analyses to baseline

Region x y z t-Value

L. striate cortex −12 −102 8 20.69

R. striate cortex 22 −86 −14 12.41

L. cerebellum −10 −76 −46 5.6

R. cerebellum 26 −76 −42 5.11

R. extrastriate cortex 44 −74 −14 19.33

L. extrastriate cortex −40 −74 −12 15.65

R. precuneus 28 −66 38 4.79

R. occipito-temporal sulcus −34 −64 24 5.2

R. occipito-temporal sulcus 46 −60 18 6.72

L. precuneus −20 −60 44 4.13

Posterior cingulate 0 −54 12 5.35

R. fusiform gyrus 38 −50 −18 11.85

L. fusiform gyrus −40 −44 −24 10.12

L. thalamus −22 −30 −4 7.32

R. parahippocampal gyrus 28 −

26 −

6 7.08R. insula 32 −18 14 2.74

R. precentral gyrus 52 −16 56 4.36

L. precentral gyrus −56 −14 48 4.23

R. superior temporal sulcus 48 −10 −18 2.59

L. amygdala −30 −6 −20 7.96

R. amygdala 28 −6 −16 7.41

L. putamen −24 4 −6 4.2

L. inferior frontal gyrus −36 6 24 4.6

R. inferior frontal cortex 38 8 26 4.56

R. anterior cingulate −4 16 60 3.82

R. temporal pole 44 18 −36 5.07

L. anterior insula −26 18 −22 4.94

L. temporal pole −46 20 −34 6.73

L. ventrolateral prefrontal cortex −54 30 16 4.36

R. orbitofrontal cortex 32 32 −20 4.53

R. vent rolateral prefront al cort ex 58 32 12 3.14

R. ventromedial prefrontal cortex 6 48 −20 5.02

L. ventromedial prefrontal cortex −14 62 −8 3.15

L. dorsomedial prefrontal cortex −10 64 24 5.1

R. dorsomedial pre frontal cortex 10 64 26 4.92

individuals, we conducted exploratory post-hoc com-

parisons examining differences in perceiving suffering

in Black versus White individuals, finding no signifi-

cant differences. In addition, we examined differences

between perceiving human and animal suffering.

First, we compared differences between responses

to humans versus animals (see Table 3 and Figure 2),

using a planned contrast examining differencesbetween humans and animals. We did this using

weighted second-level contrasts in order to account

for having twice as many human stimuli as animal

stimuli.3 Responses to human minus dog suffering

revealed activation in dorsal and ventral regions of

the medial PFC and cerebellum. This likely reflects

the activation of mentalizing processes involved with

3 See note 1.

3 t -value 8

Figure 1. Regions significantly active for suffering in Black and

White individuals as well as for animal suffering compared to

baseline. t -Maps reported reflect the conjunction between contrasts

comparing suffering in each of these groups to baseline with an

inclusive mask for only regions significantly active for all three

conditions to baseline. t -Statistic maps are overlaid on the mean

anatomical image of the participants.

decoding human mental states. Also active wereregions of the posterior cingulate and inferior parietal

lobe, which are involved in self-relevant processing

and thinking in a third-person perspective. Responses

to animal versus human suffering revealed activation

in areas related to affective simulation including the

AI, the premotor cortex, and the IFG. This suggests

that perceiving dog suffering, compared to humans

may capture attention to a greater degree than human

suffering as well as engage more emotional versus

cognitive empathy. Also active were bilateral areas of

the extrastriate cortex and precuneus. These were not

a priori regions of interest, but merit note as they

support evidence asserting that thinking about ani-mals requires more semantic knowledge (Caramazza

& Shelton, 1998) and implies that understanding ani-

mal suffering may involve our semantic knowledge of

animals.

In addition, we examined whether there were any

differences between suffering in immature versus

mature humans and dogs by examining the above-

mentioned ANOVA but three (type of sufferer: Black

individual, White individual, or dog) X 2 (age of suf-

ferer: immature versus mature). This analysis revealed




TABLE 2

Regions significant for the ANOVA comparing suffering for White and Black humans, and dogs. Beta

values reflect the beta value for the each contrast at the indicated peak voxel

MNI coordinates Peak beta value

Region x y z F-Value White Black Dog

L. cuneus −8 −92 16 9.92 0.73 1.11 0.81

R. cuneus 16 −90 0 10.63 2.48 3.03 3.25

L. striate cortex −36 −82 18 28.04 0.89 0.97 1.55

R. extrastriate cortex 36 −78 6 30.05 1.53 1.61 2.13

L. extrastriate cortex −34 −76 8 28.66 0.41 0.47 0.81

L. precuneus −18 −70 52 29.79 0.37 0.49 1.42

R. inferior parietal lobule 44 −70 42 11.14 −0.31 −0.24 −0.57

L. inferior temporal cortex −52 −68 −6 33.93 0.75 0.89 1.74

R. precuneus 18 −66 60 28.3 0.06 0.35 1.45

L. angular gyrus −42 −66 48 13.8 −0.26 −0.23 −0.80

R. inferior temporal gyrus 52 −60 −10 34.57 1.26 1.22 2.14

Precuneus 0 −58 30 11.57 0.75 0.90 0.29

R. fusiform gyrus 28 −34 −24 9.28 0.92 0.80 1.10

R. cerebellum 22 −30 −26 8.41 0.46 0.34 0.60

L. postcentral gyrus −60 −26 42 30.8 −0.07 0.16 0.54

R. inferior temporal gyrus 48 −8 −26 10.38 0.19 0.15 0.02

L. insula −46 0 6 13.75 −0.30 −0.03 −0.02

L. premotor cortex −44 2 24 15.8 0.35 0.29 0.68

R. premotor Cortex 48 10 26 16.59 0.73 0.55 1.10

R. dorsomedial PFC 16 40 22 9.35 −0.04 −0.02 −0.14

R. ventromedial PFC 4 48 −18 9.94 1.23 1.20 0.77

R. medial PFC 2 62 4 11.88 1.44 1.45 0.78

no activation at our threshold for the main effects of

age of sufferer the interaction between type of sufferer

and age of sufferer.

DISCUSSION

Anecdotal evidence suggests that we anthropomor-

phize animals and empathize with the suffering with

animals. However, psychological research indicates

that we may think of humans as special. Here, we

found that many of the same brain regions known to be

involved in human empathy are active when perceiving

both human and animal suffering. This suggests that

empathy is not simply a response we keep for humans

alone, but can also extend to nonhuman entities with

which we are familiar. In this study, we found that per-

ceiving suffering in animals, like humans, resulted inthe activation in the primary neural regions known to

be involved in empathy for the perception of suffering

of others, including the ACC and AI.

Empathy for humans versus animals

Despite the similarities in neural responses to human

and animal suffering, when we directly compared

images of suffering humans and animals, we did

find evidence for some distinct patterns of activa-

tion in response to depictions of humans versus ani-

mals, suggesting that different neural mechanisms may

underlie how we derive our empathic responses tohumans and animals. Empathy for humans appears

to elicit more activation in brain regions known to

be involved in decoding others’ mental states, specifi-

cally the mPFC. We found activation in both the dorsal

and ventral mPFC for human versus animal suffer-

ing. Previous work has shown different regions in the

mPFC serve different purposes when decoding others’

mental states. The dorsal mPFC is thought to involve

the use of stereotypical knowledge to understand what

others are thinking while the ventral regions of the

mPFC are involved in understanding similar others

(Mitchell, Macrae, & Banaji, 2006) as well as emo-

tional perspective taking (Hynes et al., 2006). Sucha dissociation indicates the ventral mPFC is involved

in decoding the emotions of others while more dor-

sal regions are involved in understanding meaning

through the actions of others (Amodio & Frith, 2006).

In addition, differences in activation in the ventral

mPFC may reflect differences in concern regarding

perceiving suffering in humans and animals. Lesions to

the ventral mPFC lead to deficits in empathy responses

(Rankin et al., 2006; Sturm et al., 2006). Further,

the development of the mPFC through childhood into



8 FRANKLIN ET AL.

TABLE 3

Peaks of regions active for the direct contrast between

human and animal and animal versus human empathy

Region x y z t-Value

Human Minus DogL. Inferior Parietal Lobul −44 −74 40 5.91

R. Inferi or Pari etal Lobul e 56 −66 28 5.36

R. Ventromedial Prefront al Cortex 2 62 4 4.85

Posterior Cingulate 0 −58 30 4.58

R. Inferi or Temporal Gyrus 48 −8 −26 4.53

R. Cerebellum 44 −72 −50 4.3

R. Dorsomedial Prefront al Cortex 16 42 22 4.27

L. Inferior Temporal Gyrus −58 −30 −16 4.25

Dog Minus Human

R. Inferi or Temporal Gyrus 52 −60 −10 8.25

L. Inferior Temporal Gyrus −52 −68 −6 8.23

R. Precuneus 18 −60 52 8.2

R. Extrastriate Cortex 36 −78 6 7.75

L. Precuneus −18 −70 52 7.72

L. Extrastriate Cortex −

34 −

76 8 7.76L. Postcentral Gyrus −60 −26 42 7.55

L. Parahippocampal Gyrus −28 −52 −10 7.11

R. Parahippoca mpal Gyrus 28 −50 −14 6.69

R. Postcentral Gyrus 32 −48 68 6.3

R. Inferior Frontal Gyrus 48 8 26 5.37

R. Premotor Cortex 28 −2 52 3.87

R. Cerebellum 40 −44 −42 3.68

L. Striate Cortex −10 −76 10 3.07

R. Lateral Prefrontal Cortex 50 44 10 3.07

R. Thalamus 18 −22 4 2.96

R. Insula 38 −6 −8 2.94

L. Insula −38 −10 −4 2.76

L. Thalamus −14 −24 −2 2.58

L. Inferior Frontal Cortex −44 2 24 5.5

adulthood indicates the importance of this region

in evaluating and regulating responses involved with

empathy (Decety & Michalska, 2010). This hypoth-

esis is also supported as empathy for humans also

evoked more activation in inferior parietal regions and

the posterior cingulate. These regions are implicated in

taking a third-person perspective of others’ situations

(Ruby & Decety, 2001) and distinguishing between

self-produced emotions and emotions as produced by

others (Decety & Grèzes, 2006). Thus, activation in the

ventral mPFC, inferior parietal lobe, and posterior cin-

gulate may represent taking a third-person perspectiveof those who are suffering and distinguishing between

one’s own emotions and the emotions of those who are

suffering.

Observing dog versus human suffering, on the

other hand, led to more activation in a different set

of brain regions, including the AI and IFG. The AI

is important in the affective nature of empathy, or

the feelings elicited by empathy-producing situations,

which suggests that perceiving animal suffering elic-

its greater emotional responses than human suffering,

Human–dog

Dog–human

3 8t -value

Figure 2. Regions active to human minus dog and dog minus

human suffering.

which may form the basis for empathy for animal suf-

fering. Also active for dog versus human suffering

were the IFG and precuneus, replicating findings by

Fillipi et al. (2010). The IFG is active in mentalizingand empathy-related tasks using picture-based stim-

uli (Adams et al., 2010; Lamm et al., 2011). This

may reflect the role of the IFG in action understand-

ing, as perceiving dog suffering may require a greater

degree of understanding the actions of those involved

than perceiving human suffering, which can use more

perspective-taking. Another possibility is that dog suf-

fering captures attention to a greater degree than

human suffering. The IFG is involved in attention allo-

cation as part of the ventral attention system and is

important in allocating attention upon detecting salient

stimuli and unexpected changes in the environment

(Corbetta, Kincade, Ollinger, McAvoy, & Shulman,2000). Participants may have allocated more attention

to animal suffering because they likely do not have

as much experience with animal suffering or because

our participants were not given specific commands in

regard to the stimuli. This is especially notable as a

right-lateralized ventral attention system is thought to

be involved even without specific attentional demands

(Fox, Corbetta, Snyder, Vincent, & Raichle, 2006).

Interestingly, we did not find differences in neu-

ral responses when perceiving suffering children and




puppies as compared to adult dogs and humans. This

suggests that the differences we found between human

and animal suffering were not due to relative differ-

ences in how helpless humans and dogs were perceived

due to their suffering. However, the lack of differ-

ences between perceiving suffering children and adultsis interesting in the light that children should evoke

greater empathy than adults because they are seen as

more helpless. One limitation of our study is that we

showed a series of still images of suffering, whereas it

is more ecologically valid to see suffering as a single

presentation. It is possible that more ecologically valid

presentations, such as high-definition video, would

lead to greater differences in perceiving suffering in

animals and humans.

CONCLUSIONS

The present study indicates that there are many over-

lapping regions in humans’ empathic responses to

viewing animal and human suffering, particularly in

areas classically associated with empathic response.

Direct comparisons also revealed different neural sub-

strates activated for empathy for humans than empathy

for animals. This finding is important as it suggests

that the way we arrive at our empathic responses

to the suffering of nonhuman entities, in this case

dogs, may be fundamentally different than how we

arrive at similar responses to suffering in humans.

Nonetheless, many of the regions that were differen-

tially active when comparing human versus animalsuffering were nonetheless significantly active for both

conditions in perceptions of suffering to baseline, indi-

cating that although they represent potentially different

sources for generating similar empathic responses,

they are not mutually exclusive, but rather differen-

tially predominant.

One notable limitation of our research is that we

only examined a homogenous college-aged popula-

tion. This population is relatively protected when it

comes to perceiving suffering animals, especially in

the context of worldwide and historical interactions

between humans and animals. It is possible these find-

ings may not extend to other individuals who are more

experienced with perceiving animal suffering or to cul-

tures that use animals more directly as beasts of burden

or for survival.

Future research is necessary to examine the degree

to which these findings generalize to perceptions of

suffering in other animals aside from dogs. The current

research examined empathy-related neural processes

in the perception of suffering in dogs for the purpose

of choosing an animal that would evoke the great-

est degree of human-like empathy processes, due to

human experience with dogs. However, this may indi-

cate that perceiving suffering in other species that

humans see as less like humans or have less expe-

rience with would evoke less empathy-related neuralactivation. As discussed in the introduction, Plous’s

(1993) similarity hypothesis indicates that humans

show greater empathy for judging suffering in ani-

mals perceived as more similar to humans. In addi-

tion, many of the same perceptual processes used for

judging traits in humans extend to how we judge ani-

mals (e.g., Franklin, Zebrowitz, Fellous, & Lee, 2013;

Kwan et al., 2008). For example, Zebrowitz et al.

(2011) found that perceptual stereotypes associated

with babyfaceness extend to perceptions of animals,

with more babyish-looking animals evoking greater

stereotypic associations with being more likeable and

warm. Based on this, we would predict that animalswho we perceive to be more likeable and warm may

elicit greater empathy, but this is a question for future

examination.

Empathy is a critical motivation for prosocial

behavior and as such, understanding the processes that

elicit empathy is essential to understand why and how

we engage in prosocial behavior. Responses to animal

suffering motivate a powerful animal rights movement

(Singer, 2002). This is evident in the rise of vegetari-

anism and veganism practices in dietary habits (Kim,

Schroeder, Houser, & Dwyer, 1999) and increases

in the number of people opposing animal experi-

mentation (National Science Board, 2010). Stories

arousing empathy for animal suffering may increase a

moral focus on the value of nature (Berenguer, 2010).

Additionally, animal suffering may be used to promote

awareness for more broad-based environmental top-

ics such as deforestation and anthropogenic climate

change (Cole et al., 2009). The research presented here

suggests the neural responses underlying empathy for

perceiving animal suffering are highly similar as for

perceiving human suffering, but with some potentially

critical differences in the mechanisms driving how we

arrive at these responses. Many studies detail how

empathy plays a critical role in prosocial behavior tohumans, but it is unclear how empathy for animals may

form a basis for pro-animal behavior. This is a critical

question for future research, especially in the context

of social and political issues that may affect the welfare

of humans and animals differently.

Original manuscript received 23 October 2012

Revised manuscript accepted 2 January 2013

First published online 12 February 2013



10 FRANKLIN ET AL.

REFERENCES

Adams, R. B. Jr, Rule, N. O., Franklin, R. G., Jr, Wang,E., Stevenson, M. T., Yoshikawa, S., . . . Ambady, N.(2010). Cross-cultural reading the mind in the eyes: AnfMRI investigation. Journal of Cognitive Neuroscience,22, 97–108.

Amodio, D. M., & Frith, C. D. (2006). Meeting of minds:The medial frontal cortex and social cognition. Nature

Reviews Neuroscience, 7 , 268–277.Batson, C. D., Polycarpou, M. P., Harmon-Jones, E., Imhoff,

H. J., Mitchener, E. C., Bednar, L. L., . . . Highberger, L.(1997). Empathy and attitudes: Can feeling for a mem-ber of a stigmatized group improve feelings toward thegroup? Journal of Personality and Social Psychology, 72,105–118.

Beeney, J. E., Franklin, R. G. Jr, Levy, K. N., & Adams,R. B. (2011). I feel your pain: Emotional closenessmodulates neural responses to empathically experiencedrejection. Social Neuroscience, 6 , 369–376.

Berenguer, J. (2010). The effect of empathy in environ-

mental moral reasoning. Environment and Behavior , 42,110–134.

Buck, R., & Ginsburg, B. (1997). Communicative genesand the evolution of empathy. Annals of the New York

Academy of Sciences, 807 (1), 481–483.Caramazza, A., & Shelton, J. R. (1998). Domain-specific

knowledge systems in the brain: The animate–inanimatedistinction. Journal of Cognitive Neuroscience, 10(1),1–34.

Cheng, Y., Chen, C., Lin, C. P., Chou, K. H., & Decety, J.(2010). Love hurts: An fMRI study. NeuroImage, 51(2),923–929.

Cole, M., Miele, M., Hines, P., Zokaei, K., Evans, B.,& Beale, J. (2009). Animal foods and climate change:Shadowing eating practices. International Journal of

Consumer Studies, 33(2), 162–167.Corbetta, M., Kincade, J. M., Ollinger, J. M., McAvoy, M.

P., & Shulman, G. L. (2000). Voluntary orienting is dis-sociated from target detection in human posterior parietalcortex. Nature Neuroscience, 3, 292–297.

Craig, A. D. (2002). How do you feel? Interception: Thesense of the physiological condition of the body. Nature

Reviews Neuroscience, 3, 655–666.Davidson, R. J., Putnam, K. M., & Larson, C. L.

(2000). Dysfunction in the neural circuitry of emotionregulation—a possible prelude to violence. Science, 289,591.

Decety, J. (2007). A social cognitive neuroscience model of human empathy. In E. Harmon-Jones & P. Winkielman(Eds.), Social neuroscience: Integrating biological and

psychological explanations of social behavior (pp.246–270). New York, NY: Guilford Press.Decety, J., & Grèzes, J. (2006). The power of simula-

tion: Imagining one’s own and other’s behavior. Brain Research, 1079(1), 4–14.

Decety, J., & Michalska, K. J. (2010). Neurodevelopmentalchanges in the circuits underlying empathy and sympathyfrom childhood to adulthood. Developmental Science, 13,886–899.

Eisenberger, N. I., & Lieberman, M. D. (2004). Why rejec-tion hurts: A common neural alarm system for physi-cal and social pain. Trends in Cognitive Sciences, 8(7),294–300.

Eslinger, P. J. (1998). Neurological and neuropsychologicalbases of empathy. European Neurology, 39(4), 193–199.

Filippi, M., Riccitelli, G., Falini, A., Di Salle, F.,Vuilleumier, P., Comi, G., & Rocca, M. A. (2010). Thebrain functional networks associated to human and ani-mal suffering differ among omnivores, vegetarians and

vegans. PLoS One, 5(5), e10847.Fox, M. D., Corbetta, M., Snyder, A. Z., Vincent, J. L., &

Raichle, M. E. (2006). Spontaneous neuronal activity dis-tinguishes human dorsal and ventral attention systems.Proceedings of the National Academy of Sciences, 103,10046–10051.

Franklin, R. G. Jr, Zebrowitz, L. A., Fellous, J. -M., & Lee,A. (2013). Human ability and cultural variation in sex-differentiating macaque faces. Journal of ExperimentalSocial Psychology, 49, 344–348.

Friston, K. J., Holmes, A. P., Price, C. J., Büchel, C., &Worsley, K. J. (1999). Multisubject fMRI studies andconjunction analyses. NeuroImage, 10, 385–396.

Gosling, S. D., Kwan, V. S., & John, O. P. (2003). A dog’sgot personality: A cross-species comparative approach to

personality judgments in dogs and humans. Journal of Personality and Social Psychology, 85, 1161–1169.

Hampshire, A., Chamberlain, S. R., Monti, M. M., Duncan,J., & Owen, A. M. (2010). The role of the right infe-rior frontal gyrus: Inhibition and attentional control.

NeuroImage, 50, 1313–1319.Hare, B., Brown, M., Williamson, C., & Tomasello, M.

(2002). The domestication of social cognition in dogs.Science, 298(5598), 1634.

Holroyd, C. B., Nieuwenhuis, S., Yeung, N., Nystrom, L.,Mars, R. B., Coles, M. G. H., . . . Cohen, J. D. (2004).Dorsal anterior cingulate cortex shows fMRI response tointernal and external error signals. Nature Neuroscience,7 , 497–498.

Hynes, C. A., Baird, A. A., & Grafton, S. T. (2006).Differential role of the orbital frontal lobe in emotionalversus cognitive perspective-taking. Neuropsychologia,44(3), 374–383.

Kennedy, J. S. (1992). The new anthropomorphism. NewYork, NY: Cambridge University Press.

Kim, E. H. J., Schroeder, K. M., Houser, R.F., & Dwyer, J. T.(1999). Two small surveys, 25 years apart, investigatingmotivations of dietary choice in 2 groups of vegetari-ans in the Boston area. Journal of the American Dietetic

Association, 99(5), 598–601.Kohn, A. (1990). The brighter side of human nature:

Altruism and empathy in everyday life. New York, NY:Basic Books.

Kwan, V. S. Y., Gosling, S. D., & John, O. P. (2008).Anthropomorphism as a special case of social perception:A cross-species social relations model analysis of humans

and dogs. Social Cognition, 26 , 129–142.Lamm, C., Decety, J., & Singer, T. (2011). Meta-analytic

evidence for common and distinct neural networks asso-ciated with directly experienced pain and empathy forpain. NeuroImage, 54, 2492–2502.

Leyens, J. P., Paladino, P. M., Rodriguez-Torres, R., Vaes, J.,Demoulin, S., Rodriguez-Perez, A., & Gaunt, R. (2000).The emotional side of prejudice: The attribution of sec-ondary emotions to ingroups and outgroups. Personalityand Social Psychology Review, 4(2), 186.

Mason, M. F., Banfield, J. F., & Macrae, C. N. (2004).Thinking about actions: The neural substrates of personknowledge. Cerebral Cortex , 14(2), 209–214.




Mitchell, J. P., Macrae C. N., & Banaji, M. R. (2006).Dissociable medial prefrontal contributions to judgmentsof similar and dissimilar others. Neuron, 50(4), 655–663.

National Science Board. (2010). Science and engineer-ing indicators: 2010. Arlington, VA: National ScienceFoundation.

Ostrowsky, K., Magnin, M., Ryvlin, P., Isnard, J., Guenot,M., & Mauguière, F. (2002). Representation of painand somatic sensation in the human insula: A studyof responses to direct electrical cortical stimulation.Cerebral Cortex , 12(4), 376.

Plous, S. (1993). Psychological mechanisms in the humanuse of animals. Journal of Social Issues, 49, 11–52.

Plous, S. (2003). Is there such a thing as prejudice towardanimals? In S. Plous (Ed.), Understanding prejudiceand discrimination (pp. 509–528). New York, NY:McGraw-Hill.

Preston, S. D., & de Waal, F. B. M. (2002). Empathy:Its ultimate and proximate bases. Behavioral and BrainSciences, 25, 1–20.

Rankin, K. P., Gorno-Tempini, M. L., Allison, S. C., Stanley,

C. M., Glenn, S., Weiner, M. W., & Miller, B. L. (2006).Structural anatomy of empathy in neurodegenerative dis-ease. Brain, 129, 2945–2946.

Ruby, P., & Decety, J. (2001). Effect of subjective per-spective taking during simulation of action: A PETinvestigation of agency. Nature Neuroscience, 4(5), 546.

Serpell, J. (1986). In the company of animals. Oxford: BasilBlackwell.

Shamay-Tsoory, S. G., Aharon-Peretz, J., & Perry, D.(2009). Two systems for empathy: A double dissocia-tion between emotional and cognitive empathy in inferiorfrontal gyrus versus ventromedial prefrontal lesions.

Brain, 132, 617–627.Singer, P. (1974). All animals are equal. Philosophical

Exchange, 1(Summer), 103–116.Singer, P. (1975). Animal liberation: A new ethics for our

treatment of animals. New York, NY: Random House.Singer, T., Critchley, H. D., & Preuschoff, K. (2009).

A common role of insula in feelings, empathy,and uncertainty. Trends in Cognitive Sciences, 13(8),334–340.

Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan,R. J., & Frith, C. D. (2004). Empathy for pain involvesthe affective but not sensory components of pain. Science,303, 1157.

Sturm, V. E., Rosen, H. J., Allison, S., Miller, B. L.,& Levenson, R. W. (2006). Self-conscious emotiondeficits in frontotemporal lobar degeneration. Brain, 129,2508–2516.

Weiner, B. (1980). A cognitive (attribution)-emotion-actionmodel of motivated behavior: An analysis of judg-ments of help-giving. Journal of Personality and SocialPsychology, 39, 186–200.

Zebrowitz, L. A., Wadlinger, H. A., Luevano, V. X., White,B. M., Xing, C., & Zhang, Y. (2011). Animal analo-gies in first impressions of faces. Social Cognition, 29,486–496.

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