Emotion perception in semantic dementia

EMOTION PERCEPTION IN SEMANTIC DEMENTIA

Emotion perception, but not affect perception, is impaired with semantic memory
loss
Kristen A. Lindquist,
!
Maria "endron,
#!
Lisa $e%dman &arrett,
#,',( )
* &rad+ord C.
Dic,erson
',(,-)

Department o+ Ps.c/o%o0., 1ni2ersit. o+ Nort/ Caro%ina, C/ape% 3i%%, NC #4-55
#
A++ecti2e Science Institute and Department o+ Ps.c/o%o0., Nort/eastern 1ni2ersit.,
&oston, MA 6#-
'
Department o+ Ps.c/iatr., Massac/usetts "enera% 3ospita% and 3ar2ard Medica% Sc/oo%,
&oston, MA 6#((
(
Martinos Center +or &iomedica% Ima0in0, Massac/usetts "enera% 3ospita%, C/ar%esto7n,
MA 6##5
-
$rontotempora% Disorders 1nit, Department o+ Neuro%o0., Massac/usetts "enera%
3ospita%, &oston, MA 6#((
* authors contributed equally

authors contributed equally

Corresponding author:
Kristen A. Lindquist
Department o+ Ps.c/o%o0.
1ni2ersit. o+ Nort/ Caro%ina, C/ape% 3i%%
Da2ie '#
,risten.%indquist8unc.edu
Emotion perception in semantic dementia
Abstract
$or decades, ps.c/o%o0ists and neuroscientists /a2e /.pot/esi9ed t/at t/e a:i%it.
to percei2e emotions on ot/ers; +aces is in:orn, pre<%in0uistic, and uni2ersa%. Concept
,no7%ed0e a:out emotion /as :een assumed to :e epip/enomena% to emotion perception.
In t/is paper, 7e report +indin0s +rom t/ree patients 7it/ semantic dementia t/at cannot
:e e=p%ained :. t/is >:asic emotion? 2ie7. T/ese patients, 7/o /a2e su:stantia% de+icits
in semantic processin0 a:i%ities, spontaneous%. percei2ed p%easant and unp%easant
e=pressions on +aces, :ut not discrete emotions suc/ as an0er, dis0ust, +ear, or sadness,
e2en in a tas, t/at did not require t/e use o+ emotion 7ords. Our +indin0s support t/e
/.pot/esis t/at discrete emotion concept ,no7%ed0e /e%ps trans+orm perceptions o+ a++ect
@positi2e%. or ne0ati2e%. 2a%enced +acia% e=pressionsA into perceptions o+ discrete
emotions suc/ as an0er, dis0ust, +ear and sadness. T/ese +indin0s /a2e important
consequences +or understandin0 t/e processes supportin0 emotion perception.
#
Emotion perception in semantic dementia
T/e a:i%it. to percei2e discrete emotions suc/ as an0er, dis0ust, +ear, sadness, etc.
in ot/er peop%e is a +undamenta% part o+ socia% %i+e. Bit/out t/is a:i%it., peop%e %ac,
empat/. +or %o2ed ones, ma,e poor socia% Cud0ments in t/e :oardroom and c%assroom,
and /a2e di++icu%t. a2oidin0 t/ose 7/o mean t/em /arm. T/e dominant paradi0m in
emotion researc/ +or t/e past (6 .ears, ca%%ed t/e >:asic emotion? approac/, assumes t/at
/umans e=press and detect in ot/ers discrete emotions suc/ as an0er @i.e., a sco7%A,
sadness @i.e., a poutA, +ear @i.e., 7ide e.esA, dis0ust @i.e., a 7rin,%ed noseA, or /appiness
@i.e., a smi%eA . Scientists %ar0e%. assume t/at t/is detection a:i%it. is in:orn, uni2ersa%
across a%% cu%tures, and ps.c/o%o0ica%%. primiti2e @i.e., it cannot :e :ro,en do7n into
more :asic ps.c/o%o0ica% processesA. Concept ,no7%ed0e a:out discrete emotion t/at is
represented in %an0ua0e is assumed to :e irre%e2ant to t/e a:i%it. to percei2e discrete
emotion in +aces . T/is >:asic emotion? 2ie7 is a standard part o+ t/e ps.c/o%o0.
curricu%um tau0/t at uni2ersities in t/e Bestern 7or%d, and dri2es researc/ in a ran0e o+
discip%ines inc%udin0 co0niti2e neuroscience , interpersona% communication and con+%ict
ne0otiation and ps.c/opat/o%o0. . T/e 1S 0o2ernment a%so re%ies on t/is +rame7or, to
train securit. personne% to identi+. t/e co2ert intentions o+ peop%e 7/o pose a t/reat to its
citi9ens .
Emotion concepts shape discrete emotion perception
Despite t/e pre2a%ence o+ t/e :asic emotion 2ie7, 0ro7in0 e2idence su00ests t/at
discrete emotion perception is not ps.c/o%o0ica%%. :asic, and in +act depends on more
>e%ementa%? ps.c/o%o0ica% processes suc/ as A perceptions o+ :asic a++ecti2e 2a%ence in
+aces @i.e., detectin0 +acia% :e/a2iors t/at correspond to positi2e 2. ne0ati2e 2. neutra%
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Emotion perception in semantic dementia
+ee%in0sA, and #A t/e a:i%it. to ma,e meanin0 o+ t/ose a++ecti2e +acia% :e/a2iors usin0
concept ,no7%ed0e a:out discrete emotion .

A 0ro7in0 %iterature demonstrates t/at accessi:%e emotion concept ,no7%ed0e
s/apes /o7 indi2idua%s ma,e meanin0 o+ a++ecti2e +acia% e=pressions as instances o+
discrete emotions suc/ as >an0er,? >dis0ust,? >+ear,? etc. $or instance, t7o<.ear o%d
c/i%dren, 7/o possess on%. t/e rudimentar. concepts o+ >sad? and >/app.,? can
correspondin0%. on%. percei2e +aces in terms o+ a++ecti2e 2a%ence @e.0., t/e. cate0ori9e a%%
unp%easant +aces, inc%udin0 sco7%in0, poutin0, 7ide e.ed and 7rin,%e nosed +aces as
>sad? and a%% smi%in0 +aces as >/app.?A. Det as c/i%dren 0radua%%. acquire additiona%
discrete emotion concepts o2er t/e course o+ de2e%opment @e.0., >an0er,? >dis0ust,?
>+ear?A, t/e. are su:sequent%. a:%e to percei2e unp%easant +aces @pouts, sco7%s, 7ide
e.es, 7rin,%ed nosesA as instances o+ distinct discrete emotion cate0ories. $or instance,
:. a0e se2en, 7/en c/i%dren /a2e %earned t/e meanin0s o+ >sad,? >an0er,? >+ear? and
>dis0ust? t/e. re%ia:%. percei2e poutin0 +aces as >sad,? sco7%in0 +aces as >an0er,? 7ide
e.ed +aces as >+ear,? and 7rin,%e nosed +aces as >dis0ust? .
T/e ro%e o+ concept ,no7%ed0e in emotion perception is not %imited to ear%.
de2e%opment, /o7e2er. E2idence su00ests t/at e2en /ea%t/. adu%ts re%. on concept
,no7%ed0e durin0 emotion perception tas,s, re0ard%ess o+ 7/et/er t/at tas, e=p%icit%.
in2o%2es %a:e%in0 o+ +aces or not. $or instance, /ea%t/. adu%ts +rom most cu%tures can
easi%. se%ect t/e 7ord t/at :est matc/es t/e e=pression 7it/ a re%ati2e%. /i0/ de0ree o+
a0reement 7/en emotion 7ord %a:e%s are e=p%icit%. 0i2en in an e=perimenta% tas, @e.0., a
posed +acia% e=pression is presented 7it/ a set o+ emotion adCecti2esA. Det it is possi:%e to

In t/is paper, as in our prior 7or,, 7e use t/e terms >a++ect? or >a++ecti2e 2a%ence? to re+er to /edonic
tone @i.e., positi2it., ne0ati2it., and neutra%it.A. Be use t/e term >discrete emotion? to re+er to instances o+
speci+ic emotion cate0ories suc/ as an0er, dis0ust, +ear, etc.
(
Emotion perception in semantic dementia
dramatica%%. impair discrete emotion perceptionEand t/us reduce accurac. on a tas,
suc/ as t/isE:. mere%. manipu%atin0 t/ose adu%ts; a:i%it. to access t/e meanin0 o+
discrete emotion 7ords. T/is e2en occurs in tas,s t/at do not e=p%icit%. require %a:e%in0
o+ +aces. $or instance, disruptin0 access to t/e meanin0 o+ discrete emotion concepts suc/
as >an0er,? >dis0ust,? or >+ear,? :. /a2in0 participants repeat ot/er 7ords durin0 t/e
discrete emotion perception tas, @ca%%ed >2er:a% o2ers/ado7in0?A, impairs participants;
a:i%it. to distin0uis/ :et7een +acia% portra.a%s o+ an0er and +ear as cate0orica%%. di++erent
emotiona% e=pressions . T/e simp%e remo2a% o+ discrete emotion 7ords +rom t/e
e=perimenta% tas, produces a simi%ar e++ect . An e=perimenta% manipu%ation t/at
temporari%. renders t/e meanin0 o+ an emotion 7ord inaccessi:%eEca%%ed semantic
satiationEa%so reduces t/e speed and accurac. o+ discrete emotion perception . $or
instance, a+ter repeatin0 a re%e2ant discrete emotion 7ord @e.0., >an0er?A out %oud '6
times unti% t/e meanin0 o+ t/e 7ord :ecomes temporari%. inaccessi:%e, participants are
s%o7er and %ess accurate to Cud0e t/at t7o sco7%in0 +aces matc/ one anot/er in emotiona%
content @Lindquist et a%. #66FA. Since t/e emotion Cud0ment tas, used in Lindquist et a%.
@#66FA mi0/t imp%icit%. require use o+ discrete emotion 7ords, 7e rep%icated and
e=tended t/ese +indin0s more recent%. usin0 a perceptua% primin0 tas, t/at does not
require t/e use o+ emotion 7ords. Be +ound t/at +o%%o7in0 semantic satiation o+ a
re%e2ant discrete emotion 7ord @e.0., >an0er?A, a +ace posin0 discrete emotion @e.0., a
sco7%in0 +aceA is %itera%%. seen di++erent%. :. participants. $or instance, t/e emotiona%
+ace percei2ed 7/en t/e meanin0 o+ an emotion 7ord is inaccessi:%e @e.0., a sco7%in0
+ace percei2ed a+ter semantic satiation o+ t/e 7ord >an0er?A does not perceptua%%. prime
itse%+ on a %ater presentation . A%t/ou0/ t/ese care+u% e=perimenta% manipu%ations
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Emotion perception in semantic dementia
produced data consistent 7it/ t/e /.pot/esis t/at concept ,no7%ed0e a:out emotion
s/apes instances o+ positi2e and ne0ati2e +acia% musc%e mo2ements into perceptions o+
discrete emotions, a po7er+u% test o+ t/is /.pot/esis is to e=amine discrete emotion
perception in peop%e 7/o /a2e natura%%. occurrin0 and permanent%. impaired concept
,no7%ed0e.
A case study of discrete emotion perception in semantic dementia
In t/e present report, 7e assessed discrete emotion perception in indi2idua%s 7it/
a neurode0enerati2e disease t/at impairs access to and use o+ concept ,no7%ed0e.
Semantic dementia is a pro0ressi2e neurode0enerati2e diseaseEone +orm o+ primar.
pro0ressi2e ap/asia Et/at resu%ts in nota:%e impairments in concept ,no7%ed0e
a2ai%a:i%it. and use . Researc/ on semantic dementia /as traditiona%%. documented
impairments to conceptua% ,no7%ed0e +or o:Cects, p%ants, and anima%s . Suc/ impairments
are associated 7it/ re%ati2e%. +oca% @t.pica%%. %e+t<%atera%i9edA neurode0eneration in t/e
anterior tempora% %o:es, 7/ic/ are /.pot/esi9ed to :e /u:s in a distri:uted net7or,
su:ser2in0 semantic memor. and conceptua% ,no7%ed0e . Ear%. in t/e course o+ t/e
disease, semantic dementia is associated 7it/ t/e 2er. speci+ic ina:i%it. to understand t/e
meanin0 o+ 7ords, amidst norma% 2isua% processin0, e=ecuti2e contro%, comportment and
:e/a2ior.
Sometimes termed t/e >tempora% %o:e? 2ariant o+ +rontotempora% dementia @$TDA,
semantic dementia is a su:<c%ass o+ t/e :roader dia0nosis o+ +rontotempora% dementia. As
suc/, some patients can de2e%op a :roader set o+ %esions in +ronta% or ot/er tempora% %o:e
re0ions a++ectin0 :rain areas in2o%2ed in ot/er ps.c/o%o0ica% processes suc/ as e=ecuti2e
contro% @e.0., dorso%atera% pre+ronta% corte=A or 2isuo<spatia% processin0 @e.0.,
F
Emotion perception in semantic dementia
/ippocampus, perir/ina% corte=A. Due t/e /etero0eneit. in/erent in +rontotempora%
dementia, 7e care+u%%. se%ected t/ree patients 7/o /ad speci+ic anatomica% and
:e/a2iora% pro+i%es o+ semantic dementiaG t/is a%%o7ed us to per+orm a 2er. precise test o+
our /.pot/esis a:out emotion perception. $irst, 7e se%ected patients 7it/ a speci+ic
neurode0eneration patternH 7e se%ected on%. t/ose patients 7it/ re%ati2e%. +oca% %esions to
t/e anterior tempora% %o:es. Second, 7e se%ected patients disp%a.in0 speci+ic :e/a2iora%
patternsH 7e per+ormed a /ost o+ neurops.c/o%o0ica% tests and contro% e=perimenta% tas,s
to ensure t/at t/e patients in our samp%e /ad semantic de+icits :ut re%ati2e%. preser2ed
e=ecuti2e +unction and 2isuospatia% processin0. To ru%e out t/at patients /ad more 0enera%
a++ecti2e a:norma%ities t/at mi0/t resu%t in impaired discrete emotion perception, 7e a%so
re%ied on c%inica% assessments to ensure t/at patients /ad norma% comportment and
:e/a2iora% approac/ and a2oidance. To0et/er, t/ese ri0orous inc%usion criteria a%%o7ed us
to per+orm a stron0 test o+ t/e /.pot/esis t/at impaired conceptua% ,no7%ed0e resu%ts in
impaired discrete emotion perception.
"ro7in0 e2idence documents de+icits in emotion perception in semantic dementia
, :ut no researc/ to date /as speci+ica%%. addressed t/e /.pot/esis t/at impairments in
concept ,no7%ed0e contri:ute to impairments in discrete emotion perception. Patients
7it/ semantic dementia /a2e di++icu%ties %a:e%in0 +acia% e=pressions o+ emotion , :ut suc/
+indin0s are t.pica%%. interpreted as e2idence t/at patients can understand t/e meanin0 o+
emotiona% +aces :ut per+orm poor%. on e=perimenta% tas,s due to an ina:i%it. to
manipu%ate %a:e%s . I+ t/is 7ere t/e case, %an0ua0e 7ou%d /a2e an impact on t/e
communication o+ discrete emotion perception, :ut not t/e understandin0 o+ emotiona%
+acia% :e/a2iors. Det t/e possi:i%it. remains t/at concept ,no7%ed0e p%a.s a muc/ more
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Emotion perception in semantic dementia
inte0ra% ro%e in discrete emotion perception :. /e%pin0 to trans+orm perceptions o+
a++ecti2e +acia% e=pressions into perceptions o+ discrete emotions. In t/is 2ie7, conceptua%
,no7%ed0e +or emotion is necessar. +or discrete emotion perception to proceed. To test
t/is /.pot/esis, 7e use a case stud. approac/ to test emotion perception a:i%ities in t/ree
patients 7it/ semantic dementia. &ecause t/ese t/ree patients /a2e re%ati2e%. iso%ated
impairments in semantic memor. 7it/out impairments in e=ecuti2e +unction, 2isuospatia%
a:i%ities, comportment, or :e/a2iora% approac/ or a2oidance, t/e. pro2ide an opportunit.
to per+orm a tar0eted test o+ t/e /.pot/esis t/at concept ,no7%ed0e is necessar. +or
discrete emotion perception.
The Present Study
To assess 7/et/er concept ,no7%ed0e is important to norma% discrete emotion
perception, 7e desi0ned a tas, in 7/ic/ patients 7it/ semantic dementia @7/o /a2e
di++icu%t. usin0 semantic %a:e%sA cou%d demonstrate t/eir discrete emotion perception
a:i%ities 7it/out re%.in0 on %in0uistic emotion concepts. Be t/us desi0ned a sortin0 tas,
t/at 7ou%d assess spontaneous emotion perception and not emotion %a:e%in0 per se.
Patients 7ere presented 7it/ pictures o+ sco7%in0, poutin0, 7ide e.ed, 7rin,%e nosed,
and smi%in0 +aces, as 7e%% as posed neutra% +aces and 7ere as,ed to +ree%. sort t/e pictures
into pi%es representin0 as man. cate0ories as 7ere meanin0+u%. Be used posed depictions
o+ discrete emotions @t/e standard in most scienti+ic studies o+ emotion perceptionA
:ecause t/e. are :e%ie2ed to :e t/e c%earest and most uni2ersa%%. reco0ni9a:%e si0na%s o+
discrete emotions :. :asic emotion accounts .
To ru%e out t/at patients /ad ot/er de+icits t/at 7ou%d impair t/eir per+ormance on
t/e discrete emotion sort tas,, 7e a%so as,ed t/em to a%so per+orm a num:er o+ contro%
I
Emotion perception in semantic dementia
sort tas,s. In t/ese contro% sort tas,s, patients 7ere as,ed to sort t/e +aces into si= pi%es
anc/ored 7it/ si= num:ers @a num:er anc/ored sortA, to sort t/e +aces into si= pi%es
anc/ored 7it/ si= posed discrete emotiona% +acia% e=pressions @a +ace anc/ored sortA, to
sort t/e +aces into si= pi%es anc/ored 7it/ si= emotion cate0or. 7ords @a 7ord anc/ored
sortA, or to +ree sort t/e +aces :. identit. @an identit. sortA. B/ereas t/e num:er and 7ord
anc/ored sorts ru%ed out t/e a%ternate /.pot/esis t/at patients cou%d per+orm a discrete
sort 7/en cued to t/e correct num:er or names o+ cate0ories, t/e +ace anc/ored and
identit. sorts ru%ed out t/e more 0enera% a%ternati2e interpretations t/at A patients did not
understand /o7 to sort pictures, #A t/at t/e. /ad 2isua% impairments t/at pre2ented t/em
+rom percei2in0 di++erences :et7een +aces @i.e., prosopa0nosia or more 0enera%
2isuospatia% de+icitsA, 'A or t/at t/e. /ad co0niti2e impairments in e=ecuti2e +unction t/at
7ou%d cause t/em to per+orm poor%. on an. sortin0 tas,. Patients; per+ormance on t/ese
sorts,a%on0 7it/ our neurops.c/o%o0ica% +indin0s @see supp%ementar. materia%sA, ru%es out
a%ternate e=p%anations o+ patients; per+ormance on t/e discrete emotion sort tas,s.
In %ine 7it/ our /.pot/esis t/at norma% discrete emotion perception re%ies on
concept ,no7%ed0e o+ emotion, 7e predicted t/at patients; semantic de+icits 7ou%d :e
associated 7it/ di++icu%t. percei2in0 same<2a%ence discrete emotiona% +acia% e=pressions
@e.0., an0er 2s. +ear 2s. dis0ust 2s. sadnessA. Det mirrorin0 t/e de2e%opmenta% +indin0s
t/at in+ants and .oun0 c/i%dren, 7/o /a2e %imited conceptua% ,no7%ed0e o+ emotion, can
detect positi2e and ne0ati2e a++ect on +aces , 7e predicted t/at patients 7it/ semantic
dementia 7ou%d /a2e re%ati2e%. preser2ed perception o+ positi2e 2s. ne0ati2e 2s. neutra%
e=pressions @i.e., a++ecti2e 2a%enceA. T/is /.pot/esis 7ou%d :e supported in our stud. i+
/ea%t/. contro% adu%ts, 7/o /a2e access to conceptua% ,no7%ed0e o+ emotion,
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Emotion perception in semantic dementia
spontaneous%. produced si= pi%es +or an0er, dis0ust, +ear, sadness, /appiness and neutra%
e=pressions and rare%. con+used mu%tip%e ne0ati2e +aces +or one anot/er @e.0., 7ou%d not
treat poutin0, sco7%in0, 7ide<e.ed and 7rin,%ed nose +aces as mem:ers o+ t/e same
cate0or. :. p%acin0 t/em in t/e same pi%eA. Patients, on t/e ot/er /and, 7ou%d
spontaneous%. sort +aces into pi%es correspondin0 to positi2e, ne0ati2e, and neutra% a++ect
and 7ou%d additiona%%. ma,e errors in 7/ic/ t/e. con+used mu%tip%e ne0ati2e +aces +or
one anot/er @e.0., 7ou%d treat poutin0, sco7%in0, 7ide<e.ed and 7rin,%ed nose +aces as
mem:ers o+ t/e same cate0or. :. p%acin0 t/em in t/e same pi%eA
#
. In contrast, a :asic
emotion /.pot/esis 7ou%d predict t/at emotion perception is a ps.c/o%o0ica%%. primiti2e
process e2o%2ed +rom ancestra% primate communicati2e disp%a.s t/at does not re%. on
concept ,no7%ed0e . I+ t/is /.pot/esis 7ere supported, 7e 7ou%d not o:ser2e a
di++erence :et7een contro% participants; and patients; sorts. At t/e 2er. %east, i+ patients
7ere impaired in discrete emotion perception as compared to contro%s, a :asic emotion
2ie7 7ou%d not predict t/at patients 7ou%d s/o7 maintained perception o+ a++ect
@positi2e, ne0ati2e and neutra% 2a%enceA. Accordin0 to t/e :asic emotion 2ie7, t/e
perception o+ discrete emotion is more ps.c/o%o0ica%%. +undamenta% t/an t/e perception
o+ a++ect, meanin0 t/at discrete emotion perception s/ou%d precede a++ect perception .
Methods
Participants
Be studied t/ree patients @E", a 46<.ear o%d ri0/t</anded ma%eG $J, a F(<.ear o%d
ri0/t</anded ma%eG and CP, a -'<.ear o%d ri0/t</anded +ema%eA 7it/ a re%ati2e%. rare +orm
o+ neurode0enerati2e disorder ,no7n as semantic dementia. Eac/ patient 7as dia0nosed
#
1n+ortunate%., since t/ere 7ere not mu%tip%e :asic<%e2e% cate0ories 7it/in t/e superordinate cate0or. o+
>positi2e,? 7e cou%d not conduct a compara:%e ana%.sis +or positi2e +aces. T/is is :ecause most :asic
emotion accounts consider /appiness to :e t/e on%. positi2e :asic emotion.
6
Emotion perception in semantic dementia
7it/ semantic dementia :. a team o+ neuro%o0ists :ased on t/eir :e/a2iora% s.mptoms,
neuroanatom., and per+ormance on neurops.c/o%o0ica% assessments. Eac/ patient
presented to t/e c%inic 7it/ 0radua%%. pro0ressi2e pro:%ems reca%%in0 t/e meanin0 o+
7ords @i.e., anomiaA and 7as +ound to /a2e a semantic memor. de+icit on
neurops.c/o%o0ica% testin0. Neurops.c/o%o0ica% tests 7ere co%%ected in a /ospita% c%inicG
7e re%. on t/e neurops.c/o%o0ica% data co%%ected in t/at settin0. Neurops.c/o%o0ica% tests
re2ea%ed t/at patients /ad re%ati2e%. speci+ic semantic de+icits amidst norma% inte%%ectua%
a:i%ities, e=ecuti2e +unction, and 2isuospatia% per+ormance. No patient e=/i:ited e2idence
o+ impaired reco0nition o+ 2isua% o:Cects @i.e., 2isua% a0nosiaA or +aces @i.e.,
prosopa0nosiaA. See supp%ementar. on%ine materia%s @SOMA +or case /istories and
neurops.c/o%o0ica% test resu%ts con+irmin0 t/e speci+icit. o+ eac/ patient;s semantic
impairments. Consistent 7it/ t/e dia0nosis o+ semantic dementia, structura% Ma0netic
Resonance Ima0in0 re2ea%ed re%ati2e%. +oca% %e+t tempora% po%e atrop/. in eac/ patient;s
:rain @see $i0ure , a<cA.
Patients; per+ormance 7as compared to t/e per+ormance o+ (( a0e<matc/ed
contro% participants @M
a0e
K 4(.(, SD
a0e
K-.I5A, 7/o a%so per+ormed t/e discrete
emotiona% +ree sort. Contro% participants 7ere recruited +rom t/e communit. and
participated at a %oca% uni2ersit.. Be did not inc%ude a patient contro% samp%e :ecause it
7as di++icu%t to +ind a samp%e o+ patients 7it/ anot/er +orm o+ dementia 7/ose
per+ormance 7ou%d demonstrate a c%ear dou:%e dissociation on t/e sort tas,s 7e
emp%o.ed. $or instance, patients 7it/ ot/er t.pes o+ neurode0enerati2e diseases @e.0.,
&e/a2iora% Lariant $rontomtepora% DementiaG A%9/eimer;s DiseaseA can per+orm poor%.
on t/e t.pe o+ sort tas, 7e used +or numerous reasons inc%udin0 attentiona% de+icits,

Emotion perception in semantic dementia

:e/a2iora% impu%si2it., or impairments in a++ecti2e 2a%uation. As a resu%t, 7e compared
t/e per+ormance o+ our semantic dementia samp%e direct%. to /ea%t/. contro%s, 7/i%e a%so
institutin0 mu%tip%e contro% tas,s 7it/in t/e semantic dementia samp%e to ru%e out
a%ternate e=p%anations +or our +indin0s. T/is approac/ 7as 7arranted +or se2era% reasons.
$irst, t/e aim o+ our stud. 7as not to un2ei% ne7 de+inin0 c/aracteristics o+ semantic
dementia, :ut rat/er to iso%ate t/ose c/aracteristics a%read. ,no7n to e=ist in order to test
a speci+ic /.pot/esis a:out emotion perception. Second, 7e instituted a num:er o+
7it/in<su:Cects contro% tas,s 7it/ our patient samp%e to ru%e out ot/er e=p%anations o+ our
+indin0s. Nota:%., :ot/ o+ t/ese approac/es are ta,en in ot/er pu:%is/ed case studies o+
patients 7it/ semantic dementia @Lam:on<Ra%p/ et a%. #66A.
Materials
Face sort stimuli. T/e set contained posed, caricatured, pictures o+ +acia%
e=pressions correspondin0 to F di++erent emotion cate0ories @an0erKsco7%, sadnessKpout,
dis0ustK7rin,%ed nose, +earK7ide e.es, /appinessKsmi%e, neutra%Kre%a=ed +acia%
musc%esA. Ima0es 7ere se%ected +rom t/e IASLa: $ace Set @777.a++ecti2e<science.or0A
and t/e Researc/ Net7or, on Ear%. E=perience and &rain De2e%opment $ace Set @#66F,
NimStim $ace Stimu%us SetG /ttpHMM777.mac:rain.or0Mresources./tmA. A %on0 2ersion o+
t/e tas, contained #6 identities and a s/ort 2ersion contained F. A%% identities 7ere
European American and an equa% num:er o+ ma%e and +ema%e identities 7ere used.
Patients did not sort +aces s.stematica%%. :. 0ender on t/e emotion sort tas,s, so 7e do
not discuss t/e 0ender o+ +aces +urt/er.
Number anchors. Si= pieces o+ I.- = paper containin0 t/e num:ers <F ser2ed
as pi%e anc/ors.
#
Emotion perception in semantic dementia
Face anchors. Si= pictures o+ a sin0%e 7oman +rom t/e NimStim $ace Stimu%us
set posin0 a sco7%, 7rin,%ed nose, 7ide e.es, pout, smi%e and a posed neutra% +ace ser2ed
as pi%e anc/ors.
Word anchors. Si= pieces o+ I.- = paper containin0 t/e 7ords >an0er,?
>dis0ust,? >+ear,? >/appiness,? >sadness? and >neutra%? ser2ed as pi%e anc/ors.
Procedure
T/e discrete emotion perception tas,s 7ere desi0ned to pro:e c/an0es in a++ecti2e
processin0 andMor discrete emotion perception. T/e +ree sort procedure 7as desi0ned to
identi+. t/e cate0ories t/at patients spontaneous%. percei2ed in posed +acia% e=pressions
7it/ minima% constraints and 7it/out as,in0 patients to e=p%icit%. use emotion 7ords. As
suc/, 7e as,ed participants to sort into t/e cate0ories t/e. +ound >meanin0+u%.? T/is
open<ended instruction necessari%. ensured t/at t/e emotion cate0ories /.pot/esi9ed to
0uide perception 7ere not e=p%icit%. in2o,ed :. t/e e=perimenta% procedure at t/e outset
o+ t/e tas,. $ortunate%., t/e per+ormance o+ contro% participants ensured t/at a%ternate
e=p%anations o+ t/e +ree sort +indin0s 7ere not possi:%e. A%% contro% participants
immediate%. understood t/at discrete emotion cate0ories 7ere t/e most meanin0+u% 7a.
to sort t/e +aces @despite t/e +act t/at ot/er cate0ories suc/ as identit. and 0ender 7ere
a%so possi:%eA. $urt/ermore, testin0 patients on su:sequent contro% tas,s ensured t/at
patients did not /a2e di++icu%t. +o%%o7in0 instructions, as t/e. 7ere a:%e to sort :.
perceptua% +eatures o+ t/e e=pressions 7/en cued. Important%., additiona% contro% tas,s
@constrainin0 t/e num:er o+ pi%es patients 7ere to%d to ma,e, and cuein0 patients 7it/ t/e
names o+ emotion cate0oriesA did not /e%p t/eir per+ormance, 7/ic/ 7ou%d :e predicted i+
'
Emotion perception in semantic dementia
impaired per+ormance 7as simp%. due to t/e interpretation o+ open<ended instructions.
T/ese additiona% tas,s t/us /e%ped to c%ari+. t/e interpretation t/at patients; semantic
de+icits %ed to impairments in discrete emotion perception. $ina%%., t/e identit. sort ru%ed
out t/at patients did not understand /o7 to sort +aces, /ad a 2isua% impairment t/at
pre2ented t/em +rom percei2in0 di++erences :et7een +aces @i.e., prosopa0nosia or ot/er
2isuospatia% de+icitsA, or /ad co0niti2e impairments in e=ecuti2e +unction t/at 7ou%d
cause t/em to per+orm poor%. on an. sortin0 tas,.
Emotional free sort. Participants 7ere /anded t/e +ace sort stimu%i and 7ere
as,ed to +ree%. ma,e pi%es to represent t/e num:er o+ meanin0+u% cate0ories t/e.
percei2ed in t/e set. Patients 7ere to%d, >I am going to give you a pile of pictures. What I
want you to do is organize them into groups that are meaningful to you. ou can create
as many piles as you need to. !t the end" each pile should be sorted so that only one type
of picture is included. It is sometimes helpful to loo# through the set of pictures first
before you begin sorting. $his is not timed" so feel free to ta#e as long as you need. ou
can also change the piles while you are sorting or at the end%it is up to you. &o you
have any questions'? Patients 7ere t/en as,ed to sort t/e pictures into pi%es on t/e ta:%e.
$o%%o7in0 comp%etion o+ t/e sort, t/e researc/er as,ed t/e patient se2era% questions
inc%udin0 A >Can you tell me about how you sorted the pictures'( Since a%% patients
indicated t/at t/e. /ad sorted :. +ee%in0, t/e researc/er ne=t as,ed )* >+ow confident are
you that all of the people in each pile feel e,actly the same way' -ot confident"
somewhat confident or very confident'( Ne=t, t/e researc/er 7ent t/rou0/ eac/ pi%e 7it/
t/e participant and as,ed, >What is in this pile'( I+ t/e patient responded 7it/ emotion
or a++ect 7ords @e.0., >/app.,? >dis0ust,? >+ear? or >0ood,? >:ad?A, t/e researc/er as,ed
(
Emotion perception in semantic dementia
t/e patient to %a:e% t/e +acia% action on t/e ne=t round :. as,in0, .What e,pression is on
these people/s faces'( I+ t/e patient ne2er used an emotion 7ord to descri:e t/e pi%e, t/e
researc/er prompted, .What emotion are the people in this pile feeling'( In t/e present
report, a%% patients understood t/e instructions 7e%% and eac/ immediate%. sorted t/e +aces
into pi%es representin0 t/e a++ecti2e meanin0 o+ t/e +ace @positi2e, ne0ati2e or neutra%A.
Once t/e content o+ eac/ pi%e 7as recorded, t/e researc/er s/u++%ed t/e +aces and mo2ed
on to t/e ne=t tas,.
Number anchored sort. T/e researc/er indicated t/at t/e patient s/ou%d ma,e si=
pi%es :. %a.in0 do7n t/e si= num:er anc/ors. T/is contro% tas, cued t/e patient to t/e +act
t/at t/ere 7ere si= perceptua% cate0ories in t/e +ace set and ru%ed out t/e a%ternate
interpretation t/at participants mere%. did not understand t/at 7e 7anted t/em to sort into
si= pi%es. Patients 7ere to%d, >-ow I want you to again sort these pictures based on
feeling" but this time I am going to as# you to ma#e 0 piles. I have 0 different numbers
that I will lay out for you so that you can #eep trac# of how many piles you create.
!gain" I want you to sort based on feeling. In each pile" there should be only people who
feel the same way. !t the end" each pile you/ve made should have pictures of only people
who feel the same way. !re these instructions clear'(
Face anchored sort. T/e researc/er indicated t/at t/e patient s/ou%d ma,e si=
pi%es :. %a.in0 do7n t/e si= +ace anc/ors. T/is contro% tas, cued t/e patient to t/e +act
t/at 7e 7ere as,in0 t/em to sort into si= cate0ories :ased on t/e perceptua% +eatures o+
t/e +aces in t/e set. It ru%ed out t/e a%ternate interpretations t/at participants mere%. did
not understand t/at 7e 7anted t/em to sort :ased on t/e +acia% e=pressions or t/at
patients /ad di++icu%t. 2isua%%. detectin0 di++erences in t/e e=pressions. Patients 7ere
-
Emotion perception in semantic dementia
to%d, >-ow I want you to again sort these pictures based on feeling" but this time I am
going to start the piles for you. +ere are si, different pictures of the same woman. $he
woman feels differently in each of the pictures. !gain" I want you to sort the pictures
into these piles I have already started based on feeling. In each pile" there should be only
people who feel the same way. !t the end of your sorting" each pile you/ve made should
have pictures of only people who feel the same. !re these instructions clear'( A+ter
patients made pi%es, t/e tas, proceeded as in t/e emotion +ree sort.
Word anchored sort. T/e researc/er indicated t/at t/e patient s/ou%d ma,e si=
pi%es :. %a.in0 do7n t/e si= 7ord anc/ors. T/is cued t/e patient to t/e names o+ t/e si=
emotion cate0ories in t/e +ace set. Addin0 7ords to t/e e=perimenta% tas, t.pica%%. /e%ps
/ea%t/. adu%ts :ecome more accurate at discrete emotion perception . T/e 7ord<anc/ored
sort tas, t/ere+ore ru%ed out se2era% important a%ternati2e e=p%anations o+ our data. $irst,
it ru%ed out t/e possi:i%it. t/at patients 7ere a:%e to percei2e and sort :. discrete emotion
:ut /ad not done so in t/e +ree sort tas, :ecause t/e instructions 7ere too 2a0ue or
:ecause t/e. +ound ot/er cate0ories to :e more re%e2ant. Second, t/is contro% tas, ru%ed
out t/e possi:i%it. t/at participants /ad intact concept ,no7%ed0e :ut per+ormed poor%.
on t/e +ree sort :ecause t/e. didn;t /a2e t/e a:i%it. or t/e moti2ation to spontaneous%.
access t/ose emotion concepts.
To start t/e sort tas,, t/e researc/er stated, >-ow I want you to again sort these
pictures based on feeling" but this time I am going tell you what should be in each of the
0 piles. I have 0 different words that I will lay out for you so that you can #eep trac# of
the piles. In each pile" there should be only people who feel the same way. In this pile" I
want you to sort people who feel happy. In this pile" I want you to sort people who feel
F
Emotion perception in semantic dementia
neutral. In this pile" I want you to sort people who feel angry. In this pile" I want you to
sort people who feel fearful. In this pile" I want you to sort people who feel sad. In this
pile" I want you to sort people who feel disgusted. !t the end of your sorting" each pile
you/ve made should have pictures of only people who feel the same way. !re these
instructions clear'( A+ter patients made pi%es, t/e tas, proceeded %i,e t/e emotion +ree
sort.
dentity free sort. T/e researc/er instructed t/e patient to sort into pi%es :ased on
identit.. I+ patients 7ere una:%e to do t/is accurate%., t/en t/is 7ou%d :e e2idence t/at
t/e. /ad ot/er co0niti2e or 2isua% de+icits t/at 7ou%d ma,e t/em unsuita:%e participants
+or t/e emotion perception tas,. T/e researc/er stated, >In this pile there are pictures of a
bunch of people. $here are several pictures of each person in the pile. What I would li#e
you to do is to sort the pictures into piles based on their identity. ou can create as many
new piles as you need to. !t the end" each pile you/ve made should have pictures of only
1 person in it. !re these instructions clear'( B/en t/e patient +inis/es, t/e researc/er
as,s, >+ow confident are you that all of the people in each pile are the same e,act
person' -ot confident" somewhat confident or very confident'(
!ata Analysis
To assess patients; per+ormance, 7e computed t/e num:er o+ pi%es t/e. created
on t/e emotiona% +ree sort and t/e percenta0e o+ errors @7/ere patients con+used one t.pe
o+ +ace +or anot/erA. Errors 7ere t/e percenta0e o+ +aces portra.in0 a di++erent e=pression
+rom t/e predominant e=pression in t/e same pi%e @e.0., t/e num:er o+ sco7%in0 and 7ide
e.ed +aces in a pi%e consistin0 predominant%. o+ poutin0 +acesA. Error t.pes 7ere
computed :. determinin0 t/e o2era%% num:er o+ 7it/in<2a%ence @e.0., one ne0ati2e +ace
4
Emotion perception in semantic dementia
con+used 7it/ anot/erA or cross<2a%ence @e.0., one ne0ati2e +ace con+used 7it/ a neutra%
+aceA errors. See Ta:%e +or a %ist o+ error t.pes.
Be used a modi+ied t<test to statistica%%. compare patients; error percenta0es to
t/ose o+ t/e (( contro% participants. T/is met/od is +requent%. used in case studies to
compare patient samp%es to contro% samp%es.
"esults and !iscussion
Consistent 7it/ our /.pot/esis t/at concept ,no7%ed0e is necessar. +or norma%
emotion perception, contro% participants 7/o /ad intact concept ,no7%ed0e +or discrete
emotion spontaneous%. percei2ed sco7%in0, poutin0, 7ide<e.ed, 7rin,%e<nosed, smi%in0
+aces, and neutra% +aces, as instances o+ an0er, sadness, +ear, dis0ust, /appiness and
neutra% emotion. T/is occurred despite t/e open<ended nature o+ our instructions to sort
t/e cate0ories into t/ose t/e. +ound most >meanin0+u%.? Contro% participants on a2era0e
produced si= @or moreA pi%es to represent t/e discrete emotion cate0ories in t/e set and
tended not to con+use ne0ati2e +aces 7it/ one anot/er in t/eir pi%es @i.e., /ad %o7 ne0<ne0
error ratesG see Ta:%e A. T/e maCorit. o+ contro% participants @FNA spontaneous%.
produced eit/er si= or se2en pi%es and 5FN o+ contro% participants produced si= or more.
On%. t7o contro% participants @(NA produced +e7er t/an si= pi%es on t/e sort tas,G one
participant produced +our pi%es and one produced +i2e. Nota:%., no contro% participants
produced t/ree pi%es. T/at on%. one indi2idua% +rom t/e contro% samp%e @#.#NA
spontaneous%. produced +our pi%es on t/e sort tas,, and none produced t/ree, stands in
star, contrast to t/e +act t/at 66N o+ our patient samp%e produced +our or +e7er pi%es on
t/e sort tas,. See Ta:%e +or contro%s; and patients; mean error rates and $i0ure ' +or an
e=amp%e o+ a contro% participant;s per+ormance.
I
Emotion perception in semantic dementia
Contrar. to contro% participants, and as predicted, patients 7it/ semantic
dementia, 7/o /a2e impaired concept ,no7%ed0e, did not spontaneous%. percei2e
discrete emotion on +aces. T/e patients in our case stud. demonstrated preser2ed a++ect
perception, /o7e2er, consistent 7it/ our /.pot/esis t/at a++ecti2e processin0 7ou%d :e
intact e2en in t/e presence o+ impaired conceptua% ,no7%ed0e. One interpretation o+ t/ese
+indin0s is t/at patients 7ere a:%e to percei2e discrete emotion on +aces, :ut mere%.
t/ou0/t t/at a++ect 7as t/e more >meanin0+u%? cate0or.. Det patients; per+ormance on t/e
2arious contro% tas,s e++ecti2e%. ru%es out t/is a%ternate interpretation. $or instance, no
patient 7as a:%e to sort :. discrete emotion 7/en as,ed to sort t/e +aces into si=
cate0ories, or 7/en e=p%icit%. as,ed to sort into pi%es +or >an0er,? >dis0ust,? >+ear,?
>sadness,? >/appiness? or >neutra%.? Anot/er interpretation o+ our +indin0s is t/at a++ect
perception 7as mere%. easier +or patients t/an discrete emotion perception. A0ain, t/e
per+ormance o+ t/e contro% participants, a%on0 7it/ t/e per+ormance o+ t/e patients on t/e
2arious contro% tas,s, ru%es out t/is a%ternate interpretation. I+ a++ect perception 7as easier
t/an discrete emotion perception, t/en contro% participants cou%d a%so /a2e ta,en t/e
>eas.? route and sorted +aces :. a++ect as 7e%%, :ut t/e. did not. More to t/e point,
patients continued to sort :. a++ect on t/e contro% tas,s, e2en 7/en t/ese tas,s pro2ided
e=tra structure and remo2ed co0niti2e %oad :. cuin0 patients to t/e num:er, appearance,
and e2en names o+ t/e discrete emotion cate0ories. T/e most parsimonious e=p%anation
o+ our +indin0s is t/us t/at participants /ad a preser2ed a:i%it. to percei2e a++ect :ut 7ere
una:%e to percei2e discrete emotion on +aces.
Be :e0in :. discussin0 t/e +indin0s +rom patient E", 7/o 7as our +irst case, and
as a resu%t, per+ormed +e7er contro% tas,s t/an su:sequent cases. Be ne=t discuss t/e
5
Emotion perception in semantic dementia
+indin0s +rom patients $J and CP, 7/o per+ormed a%% t/e contro% tas,s in our :atter..
Patient E#
Emotional free sort
Consistent 7it/ our /.pot/esis t/at concept ,no7%ed0e is necessar. +or discrete
emotion perception, :ut not a++ect perception, E" +ree sorted emotiona% +acia%
e=pressions into t/ree pi%es @see $i0ure (A t/at /e %ater %a:e%ed >/app.,? >not/in0? and
>rou0/.? Compared to contro%s, E" made more errors in 7/ic/ /e con+used ne0ati2e
@sco7%in0, poutin0, 7ide<e.ed and 7rin,%e<nosed +acesA +aces 7it/ eac/ ot/er
Ot@('AK#.4I, pP.6G see Ta:%e Q, indicatin0 t/at /e cou%d not percei2e t/e di++erences
:et7een e=pressions +or an0er, dis0ust, +ear, and sadness.
Face$anchored sort
E";s ina:i%it. to distin0uis/ ne0ati2e discrete emotiona% e=pressions +rom one
anot/er 7as not due to an ina:i%it. to detect t/e +acia% actions o+ poutin0, sco7%in0, 7ide<
e.es, etc. or a 0enera% ina:i%it. to per+orm an. sort tas,. E" per+ormed t/e contro% +ace<
anc/ored sort tas, per+ect%.G /e cou%d detect perceptua% di++erences in t/e e=pressions and
matc/ a sco7% to a sco7%, a pout to a pout, and so +ort/. In %i0/t o+ t/ese +indin0s, /is
per+ormance on t/e +ree sort indicated t/at 7it/out access to emotion concept ,no7%ed0e,
/e did not understand t/e ps.c/o%o0ica% meanin0 o+ +acia% e=pressions at a %e2e% more
nuanced t/an simp%e a++ecti2e 2a%ence.
Patients F% and &P
Emotional free sort
&ot/ $J and CP per+ormed simi%ar%. to E" on t/e emotiona% +ree sort. $J
produced ( pi%es @see $i0ure (A, 7/ic/ /e %a:e%ed >/app.,? >sad,? >norma%,? and a +ourt/
#6
Emotion perception in semantic dementia
pi%e t/at /e 2arious%. ca%%ed >sad,? >mad,? and >questionin0? at di++erent points
t/rou0/out t/e stud. @indicatin0 t/at 7/at t/ese +aces s/ared in common 7as ne0ati2e
2a%enceA. Li,e E", $J made more errors in 7/ic/ /e con+used ne0ati2e +aces 7it/ one
anot/er @sco7%in0, poutin0, 7ide<e.ed and 7rin,%e<nosed +acesA t/an did contro%s
Ot@('AK#.-', pP.6#G see Ta:%e Q, :ut /e ne2er con+used ne0ati2e +aces +or positi2e
@smi%in0A +aces.
CP made +our pi%es @see $i0ure (A, 7/ic/ s/e %a:e%ed >+unn.M/app.,? >re0u%ar,?
>not up,? and >rea%%. not up at a%%.? Li,e E" and $J, CP made more errors in 7/ic/ s/e
con+used ne0ati2e +aces 7it/ one anot/er @sco7%in0, poutin0, 7ide<e.ed and 7rin,%e<
nosed +acesA t/an did contro%s Ot@('AK.F6, pP.6-IG one<tai%edG see Ta:%e Q, :ut s/e rare%.
con+used ne0ati2e +aces +or positi2e @smi%in0A +aces. A%t/ou0/ CP produced one pi%e t/at
contained predominant%. sco7%in0 +aces on t/e emotion +ree sort, 7e do not t/in, t/is is
e2idence t/at s/e understood t/e cate0or. o+ an0er. $irst, CP did not produce t/is pi%e
spontaneous%.. S/e :e0an t/e tas, :. sortin0 +aces into t/ree pi%es representin0 positi2e,
neutra% and ne0ati2e a++ect @pi%e ' and ( 7ere a sin0%e pi%eA, :ut s/e random%. sp%it t/is
ne0ati2e pi%e into t7o ne0ati2e pi%es +o%%o7in0 a cue +rom researc/ers t/at s/e cou%d
c/ec, /er pi%es :e+ore mo2in0 on. T/e +act t/at s/e sp%it /er pi%e into additiona% pi%es
+o%%o7in0 a cue +rom t/e researc/ers su00ests t/at s/e mi0/t /a2e rea%i9ed t/at t/ere
s/ou%d :e more cate0ories in t/e set @e2en i+ s/e cou%d not percei2e t/emA. Second, t/e
name t/at CP spontaneous%. used to %a:e% t/ese t7o pi%es imp%ies t/at s/e did not see t/e
+aces in pi%e ' as cate0orica%%. di++erent +rom t/e +aces in pi%e (. Rat/er, t/e %a:e%s >not
up? and >rea%%. not up? su00est t/at s/e e=perienced t/e +aces in /er t7o ne0ati2e pi%es as
di++erin0 in intensit. o+ unp%easantness @a%t/ou0/ t/e +aces s/e p%aced in t/is pi%e 7ere
#
Emotion perception in semantic dementia
not rated as more intense :. a separate 0roup o+ /ea%t/. indi2idua%sA. $ina%%., as 7e
discuss :e%o7, CP did not s/o7 a consistent pattern o+ distin0uis/in0 sco7%in0 +aces
+rom ot/er ne0ati2e +aces in t/e su:sequent sort tas,s t/at s/e and $J per+ormed.
At +irst :%us/, it mi0/t a%so appear t/at :ot/ $J and CP 7ere a:%e to speci+ica%%.
percei2e dis0ust :ecause t/e. p%aced a%% 7rin,%ed<nose +aces in a sin0%e pi%e in t/e +ree
sort tas,, :ut it is un%i,e%. t/at t/e. 7ere disp%a.in0 discrete emotion perception. B/en
as,ed to per+orm %ater sorts @e.0., t/e num:er and 7ord anc/ored sortsA, neit/er $J nor
CP continued to p%ace 7rin,%ed nose +aces into a sin0%e pi%e @e.0., see $i0ure F +or a
depiction o+ CP;s num:er<anc/ored sort, 7/ere s/e p%aces 7rin,%ed nose +aces in ' o+ t/e
( ne0ati2e pi%es s/e createsA, indicatin0 insta:i%it. in t/eir perception o+ t/ese +aces.
Face$anchored sort
Li,e E", $J and CP comp%eted t/e +ace<anc/ored sort to ensure t/at t/e. cou%d in
+act distin0uis/ t/e perceptua% di++erences on t/e ne0ati2e +aces.
'
&ot/ $J and CP
per+ormed :etter on t/is tas, t/an t/e. /ad on t/e emotion +ree sort tas, @see Ta:%e #A,
indicatin0 t/at t/eir per+ormance on t/e emotion +ree sort 7as un%i,e%. to stem +rom t/e
ina:i%it. to detect perceptua% di++erences on t/e +aces. Li,e E", t/eir per+ormance
su00ested t/at t/e. cou%d detect di++erences :et7een +acia% e=pressions :ut did not
understand t/e ps.c/o%o0ica% meanin0 :e.ond :asic a++ecti2e 2a%ence.
Number$anchored sort
$J and CP per+ormed t/e num:er<anc/ored sort to pro2ide additiona% support +or
t/e interpretation t/at t/e. did not percei2e si= meanin0+u% cate0ories in t/e test stimu%i
'
$J and CP per+ormed t/e +ace<anc/ored sort a+ter t/e num:er<anc/ored sort, a%t/ou0/
7e discuss t/eir per+ormance on t/e +ace<anc/ored sort +irst +or ease o+ comparison 7it/
E" @7/o did not per+orm a num:er<anc/or sortA. Ot/er7ise, t/e contro% sorts are
discussed in t/e order in 7/ic/ t/e. 7ere imp%emented durin0 t/e testin0 session.
##
Emotion perception in semantic dementia
@e2en 7/en t/e. 7ere cued to t/e correct num:erA. $J made +i2e pi%es correspondin0 to
a++ect @one pi%e +or smi%in0 +aces, one +or neutra% +aces, and +our pi%es containin0 2arious
mi=es o+ ne0ati2e +aces in 7/ic/ /e con+used sco7%in0, poutin0, 7ide<e.ed and 7rin,%e<
nosed +acesG see Ta:%e # +or errorsA. CP made si= pi%es correspondin0 to a++ect @one pi%e
+or smi%in0 +aces, one +or neutra% +aces, and +our pi%es containin0 2arious mi=es o+
ne0ati2e +aces in 7/ic/ s/e con+used sco7%in0, poutin0, 7ide<e.ed and 7rin,%e<nosed
+acesG see Ta:%e # +or errorsA. Nota:%., neit/er patient seemed to t/in, t/at si= cate0ories
7ere appropriate +or descri:in0 t/e perceptua% cate0ories present in t/e +ace set. $J c/ose
not to use t/e si=t/ anc/or durin0 /is sort and CP spontaneous%. as,ed 7/. 7e /ad as,ed
/er to sort t/e stimu%i into so man. pi%es. T/is num:er<anc/or sort a%so a%%o7ed us to
o:ser2e t/e insta:i%it. in :ot/ patients; ne0ati2e pi%es across sort tas,s. $or instance,
a%t/ou0/ CP produced one pi%e in t/e +ree sort t/at contained more sco7%in0 +aces t/an
t/e ot/er pi%e, t/ese sco7%in0 +aces 7ere distri:uted across t/ree ne0ati2e pi%es in t/e
num:er<anc/ored sort, indicatin0 t/at s/e did not in +act percei2e t/em as mem:ers o+ a
sin0%e co/erent emotion cate0or. @see $i0ure -A.
T/e insta:i%it. in sortin0 t/at $J and CP demonstrated +rom one tas, to t/e ne=t is
simi%ar to t/e insta:i%it. in sortin0 t/at 7as o:ser2ed in t/e patient LEB, 7/o :ecame
ap/asic a+ter a stro,e . LEB produced di++erent pi%es 7/en as,ed to sort +aces across
t/ree di++erent instances. T/ese +indin0s su00est t/at 7it/out access to t/e meanin0 o+
7ords, patients cannot ma,e re%ia:%e ps.c/o%o0ica% interpretations o+ discrete emotiona%
+acia% e=pressions across instances. In comparison to t/e ear%ier 7or, 7it/ LEB, our
+indin0s are no2e% in t/at our patients demonstrated sta:%e a++ect perception across sort
tas,s, e2en as t/e. cou%d not re%ia:%. distin0uis/ sadness, +ear, dis0ust, and an0er +rom
#'
Emotion perception in semantic dementia
one anot/er across tas,s. Moreo2er, un%i,e LEB, 7/o /ad de+icits in %e=ica% retrie2a% :ut
not semantic memor., our patients; %ac, o+ discrete emotion concept ,no7%ed0e
a2ai%a:i%it. pro2ides t/e :est test o+ t/e /.pot/esis t/at discrete emotion concept
,no7%ed0e is necessar. +or discrete emotion perception @:ut not a++ect perceptionA.
Word$anchored sort
$J and CP ne=t per+ormed t/e 7ord<anc/ored sort to address t/e possi:i%ities t/at
A t/e. did not +ind discrete emotion cate0ories to :e t/e most >meanin0+u%? cate0ories in
t/e set, :ut cou%d sort :. t/ese cate0ories 7/en prompted, #A t/at t/e. 7ere mere%.
una:%e to spontaneous%. retrie2e t/e 7ords to support discrete emotion perception, :ut
t/at t/e. cou%d per+orm t/e tas, i+ 7e pro2ided t/e correct 7ords +or t/em. Addin0
emotion 7ords to a discrete emotion perception tas, a%most a%7a.s impro2es /ea%t/.
adu%ts; per+ormanceH t/e. are muc/ more >accurate? at detectin0 t/e discrete emotiona%
meanin0 o+ a +acia% action @e.0., a sco7%A 7/en as,ed to se%ect t/e meanin0 +rom a %ist o+
7ords @e.0., >an0er,? >dis0ust,? >+ear,? >/appiness,? >sadness?A t/an 7/en t/e. are as,ed
to spontaneous%. 0enerate t/e %a:e% t/emse%2es . Adu%ts remem:er +acia% e=pressions as
:ein0 more intense e=emp%ars o+ a particu%ar discrete emotion @e.0., /appinessA 7/en t/e.
/a2e pre2ious%. paired t/at +acia% e=pression 7it/ a 7ord @e.0., >/app.?A t/an a non<7ord
@e.0., a nonsense 7ordA . Pro2idin0 %a:e%s +or +acia% e=pressions can a%so impose t/e
perception o+ cate0ories 7/ere it did not e=ist :e+ore in /ea%t/. adu%ts. E2en .oun0
c/i%dren are more accurate 7/en as,ed to matc/ a +ace @e.0., sco7%A to a 7ord @e.0.,
>an0er?A t/an 7/en as,ed to matc/ a +ace to anot/er +ace depictin0 t/e same e=pression
@e.0., anot/er sco7%A . Det anc/orin0 t/e pi%es 7it/ emotion 7ords did not impro2e $J;s
and CP;s per+ormance @see Ta:%e #AG t/eir error rate increased a:o2e t/e %e2e% o:ser2ed in
#(
Emotion perception in semantic dementia
t/e +ace<anc/ored sort. Bords did not /e%p $J and CP :ecause t/e. did not understand
t/eir meanin0 @e.0., CP spontaneous%. as,ed >7/at is an0erR? as i+ s/e /ad ne2er
encountered t/e 7ord :e+oreA. E2en our attempts to descri:e a 7ord;s meanin0 to patients
@e.0., >an0er is a +ee%in0 .ou /a2e 7/en someone does somet/in0 :ad to .ou?A did not
/e%p, and patients cou%d not use t/is in+ormation to ma,e meanin0 o+ t/e +acia%
e=pressions posed in t/e p/oto0rap/s. T/ese +indin0s con+irm t/at our patients did in +act
/a2e impaired concepts +or emotion.
dentity sort
$ina%%., $J and CP per+ormed t/e identit. sort to ru%e out a%ternate interpretations
t/at t/e. did not understand t/e instructions o+ a sort tas,, /ad 2isua% de+icits t/at
impaired per+ormance on t/e emotiona% sort tas,s, or /ad 0enera% e=ecuti2e impairments
t/at 7ou%d inter+ere 7it/ an. sortin0 tas,. &ot/ $J and CP sorted t/e +aces per+ect%. :.
identit. @producin0 6 errorsA, ru%in0 out t/at t/eir per+ormance on t/e pre2ious tas,s 7ere
caused :. ot/er co0niti2e or perceptua% de+icits unre%ated to emotion concept ,no7%ed0e.
&onclusion
Our +indin0s are consistent 7it/ rapid%. 0ro7in0 e2idence t/at emotion concept
,no7%ed0e supports t/e norma% perception o+ discrete emotion cate0ories suc/ as an0er,
dis0ust, +ear, sadness, etc. . Pre2ious +indin0s +rom our %a:s indicate t/at temporari%.
impairin0 access to and use o+ emotion concept ,no7%ed0e in /ea%t/. .oun0 indi2idua%s
impairs discrete emotion cate0ori9ation , in+%uencin0 e2en t/e +ormation o+ emotion
percepts +rom t/e structura% +eatures o+ posed +aces . &. contrast, addin0 7ords to a tas,
/e%ps /ea%t/. participants percei2e cate0orica% :oundaries :et7een posed a++ecti2e +acia%
e=pressions 7/ere t/e. ot/er7ise cou%d not @$u0ate et a%. #66A. C/i%dren @Biden *
#-
Emotion perception in semantic dementia
Russe%%, #66'A and adu%ts are more accurate at pairin0 a sco7% 7it/ t/e 7ord >an0er?
t/an 7it/ anot/er sco7%in0 +ace, su00estin0 t/at 7ords si0ni+.in0 concept ,no7%ed0e
mi0/t actua%%. add somet/in0 to t/e perception o+ a discrete emotion, trans+ormin0 a
percept o+ a ne0ati2e +ace into a discrete percept o+ an0er. E2en neuroima0in0 e2idence is
consistent 7it/ t/e idea t/at concept ,no7%ed0e p%a.s a ro%e in constructin0 instances o+
discrete emotionH :rain areas in2o%2ed in t/e representation o+ semantic ,no7%ed0e suc/
as t/e media% pre+ronta% corte=, anterior tempora% %o:e, media% tempora% %o:e, and
2entro%atera% pre+ronta% corte= are routine%. in2o%2ed in :ot/ emotiona% perceptions and
e=periences across t/e neuroima0in0 %iterature . Our data t/us add a crucia% dimension to
t/is %iterature :. demonstratin0 t/at adu%ts 7it/ semantic impairment due to anterior
tempora% %o:e neurode0eneration cannot percei2e an0er, sadness, +ear, or dis0ust as
discrete emotions in peop%e;s +aces.
Pre2ious researc/ /as documented 0enera% decreases in discrete emotion
perception accurac. in patients 7it/ semantic dementia 7/en t/e. are as,ed to pair +aces
7it/ 7ords . To date, t/ese data /a2e :een interpreted 7it/ t/e understandin0 t/at
%an0ua0e is epip/enomena% to emotionH de+icits o:ser2ed on discrete emotion perception
tas,s are t/ou0/t to stem +rom di++icu%ties %a:e%in0 stimu%i, not +rom di++icu%ties in
discrete emotion perception per se . Our +indin0s s/o7 t/at patients; ina:i%it. to percei2e
discrete emotion is direct%. %in,ed to t/eir semantic impairments in a tas, t/at did not
require t/e use o+ emotion 7ords, and t/at cannot :e attri:uta:%e to ot/er de+icits suc/ as
%oss o+ e=ecuti2e contro%, prosopa0nosia, 2isuospatia% impairments, or a++ecti2e de+icits.
Our +indin0s mi0/t, at +irst :%us/, seem inconsistent 7it/ ot/er recent e2idence
+rom +rontotempora% dementia @$TDA patients @inc%udin0, :ut not %imited to, semantic
#F
Emotion perception in semantic dementia
dementia patientsA t/at speci+ic patterns o+ neurode0eneration spannin0 +ronta%, tempora%,
and %im:ic re0ions are associated 7it/ impairments in %a:e%in0 speci+ic emotions . $or
instance, Kum+or et a%. +ound t/at across patients 7it/ semantic dementia and ot/er
2ariants o+ $TD, de+icits in %a:e%in0 7ide<e.ed +aces as >+ear? 7ere re%ati2e%. more
associated 7it/ neurode0eneration in t/e am.0da%a 7/ereas de+icits in %a:e%in0 7rin,%ed<
nose +aces as >dis0ust? 7ere re%ati2e%. more associated 7it/ neurode0eneration in t/e
insu%a. A%t/ou0/ t/e aut/ors too, t/is as e2idence +or t/e :io%o0ica% :asicness o+ certain
discrete emotion cate0ories, t/ese +indin0s mi0/t not u%timate%. :e at odds 7it/ our o7n
+indin0s. &ecause t/e aut/ors %oo,ed +or areas o+ neurode0eneration t/at corre%ated 7it/
impairments in t/e perception o+ speci+ic discrete emotions @7/i%e contro%%in0 +or
re%ations/ips :et7een :rain areas and impairments in percei2in0 ot/er discrete emotionsA
t/e. 7ere not %i,e%. to re2ea% :rain areas, suc/ as t/e anterior tempora% %o:e, t/at are
0enera% to impairments in percei2in0 a%% ne0ati2e discrete emotions. "ro7in0 e2idence
demonstrates t/at concept ,no7%ed0e is represented in a >/u: and spo,es? manner , in
7/ic/ t/e anterior tempora% %o:e ser2es as a >/u:? to a set o+ >spo,es? consistin0 o+
patterns o+ :rain acti2it. spannin0 ot/er re0ions in2o%2ed in sensation, motor :e/a2ior,
a++ect and %an0ua0e, suc/ as t/ose in2esti0ated :. Kum+or and co%%ea0ues. A%t/ou0/
specu%ation at t/is point, Kum+or et a%.;s @#6'A +indin0s and our o7n mi0/t t/us :e
e2idence +or :ot/ >spo,es? and >/u:s? in t/e representation o+ emotion concept
,no7%ed0eEconcept ,no7%ed0e a:out certain discrete emotions mi0/t :e supported :.
distri:uted and some7/at distincti2e patterns o+ :rain acti2it., :ut t/ese patterns mi0/t
con2er0e +unctiona%%. in t/e anterior tempora% %o:e. A%t/ou0/ researc/ to date /as not
e=p%icit%. assessed t/e distri:uted patterns o+ :rain acti2it. in2o%2ed in representin0
#4
Emotion perception in semantic dementia
perceptions o+ di++erent discrete emotions, meta<ana%.tic e2idence +rom our o7n %a:
su00ests t/at it is quite distri:uted @Lindquist et a%., #6#A. Ot/er e2idence +rom
co0niti2e neuroscience is su00esti2e t/at a /u: and spo,es +ormation mi0/t represent
emotion ,no7%ed0e. +MRI studies demonstrate distri:uted patterns o+ :rain acti2it.
associated 7it/ perceptions o+ ot/er semantic cate0ories suc/ as :ic.c%es, :ott%es,
at/%etes, etc. , :ut +oca% %esions to t/e anterior tempora% %o:es @as occurs in semantic
dementiaA impair perception o+ t/ese cate0ories . $uture researc/ s/ou%d t/us in2esti0ate
t/e e=tent to 7/ic/ concept ,no7%ed0e o+ emotion is represented :. distri:uted, mu%ti<
moda%, :rain areas united :. an amoda% /u: in t/e anterior tempora% %o:e.
Important%., our +indin0s demonstrate somet/in0 important t/at pre2ious +indin0s
assessin0 emotion perception in semantic dementia patients /a2e notH Despite t/eir
semantic impairments, patients in our case stud. 7ere sti%% a:%e to percei2e a++ecti2e
2a%ence in +aces. T/ese +indin0s su00est t/at perceptions o+ a++ecti2e 2a%ence are more
ps.c/o%o0ica%%. :asic t/an @i.e., superordinate toA perceptions o+ discrete emotion and
counter :asic emotion 2ie7s c%aimin0 t/at 2a%ence is a descripti2e >um:re%%a? term t/at is
app%ied to a +ace a+ter it is percei2ed as an instance o+ discrete emotion . It;s possi:%e to
ar0ue t/at a++ect perceptions are Cust easier t/an discrete emotion perceptions. T/en
a0ain, it is equa%%. possi:%e to c%aim t/at 2a%ence perception it is more di++icu%t t/an
discrete emotion perception @:ecause it in2o%2es seein0 simi%arit. across perceptua%%.
distinct +acia% e=pressionsA. Re0ard%ess, patients persisted in ma,in0 2a%ence distinctions,
e2en 7/en su:sequent contro% tas,s pro2ided e=tra structure and remo2ed co0niti2e %oad
:. cuin0 patients to t/e num:er, appearance, and e2en names o+ t/e discrete emotion
cate0ories, su00estin0 t/at a++ect perceptions 7ere a%% patients 7ere capa:%e o+.
#I
Emotion perception in semantic dementia
T/e +indin0 t/at a++ect is superordinate to Cud0ments o+ discrete emotion is
consistent 7it/ se2era% sources o+ data. $irst, t/is +indin0 is consistent 7it/ :e/a2iora%
researc/ in /ea%t/. adu%ts demonstratin0 t/at t/e dimension o+ 2a%ence descri:es
simi%arities in discrete emotion cate0ories . Second, t/is +indin0 is consistent 7it/
e2idence s/o7in0 t/at in+ants, todd%ers, and non</uman primates, 7/o %ac, sop/isticated
%an0ua0e capacit., can percei2e a++ecti2e 2a%ence in +aces, 2oices, and :odies e2en 7/en
t/e. do not re%ia:%. distin0uis/ discrete emotiona% e=pressions +rom one anot/er . On%. as
c/i%dren acquire t/e meanin0 o+ emotion 7ords suc/ as >an0er,? >+ear,? >sadness? and
>dis0ust? 7it/ norma% de2e%opment do t/e. acquire t/e a:i%it. to re%ia:%. distin0uis/
:et7een sco7%in0, 7ide e.ed, poutin0 and 7rin,%ed nosed +aces as e=pressions o+ t/ese
cate0ories . T/ird, t/is +indin0 is consistent 7it/ cross<cu%tura% e2idence t/at a%% cu%tures
percei2e 2a%ence on +aces, e2en amidst di++erences in t/e speci+ic discrete emotions t/e.
percei2e on +aces or e2en di++erences in 7/et/er discrete emotions are percei2ed at a%% .
$ina%%., simi%ar to ot/er >%ast in, +irst out? t/eories o+ de2e%opment 2s. neurode0eneration,
our +indin0s are consistent 7it/ ot/er researc/ on semantic dementia documentin0 t/e
pro0ressi2e >prunin0? o+ concepts o2er t/e course o+ disease pro0ression +rom t/e
semantica%%. su:ordinate %e2e% @e.0., %ion 2s. ti0erA to t/e :asic %e2e% @e.0., cat 2s. do0A to
t/e superordinate %e2e% @e.0., anima% 2s. p%antA . To our ,no7%ed0e, our +indin0s are t/e
+irst to demonstrate a simi%ar pattern o+ >prunin0? +or emotion concepts. A%t/ou0/ it is
not addressa:%e in t/e present stud., +uture researc/ mi0/t use %on0itudina% met/ods to
speci+ica%%. in2esti0ate t/e >prunin0? /.pot/esis as it pertains to discrete emotion 2.
2a%ence perception. I+ 2a%ence Cud0ments re%. on concept ,no7%ed0e, and 2a%ence
concepts are superordinate to discrete emotion concepts, t/en 7e mi0/t e=pect 2a%ence
#5
Emotion perception in semantic dementia
perception to diminis/ o2er t/e course o+ neurode0eneration, +o%%o7in0 discrete emotion
perception. Det i+ intact 2a%ence perception re%ies on ot/er ps.c/o%o0ica% mec/anisms
:esides concept ,no7%ed0e per se t/en it is possi:%e t/at 2a%ence perception 7i%% :e
maintained o2er t/e course o+ t/e disease.
mplications
T/e o:ser2ation t/at peop%e 7it/ semantic dementia /a2e preser2ed a++ect
perception :ut impaired discrete emotion perception /as important imp%ications +or :ot/
:asic and app%ied science. T/ese +indin0s cannot :e accommodated :. >:asic emotion?
accounts 7/ic/ assume t/at emotiona% e=pressions are >ps.c/o%o0ica% uni2ersa%s and
constitute a set o+ :asic, e2o%2ed +unctions, t/at are s/ared :. a%% /umans? and 7/ic/
/a2e e2o%2ed +rom ear%. primate communication . A%t/ou0/ our +indin0s run contrar. to
:asic emotion mode%s, our stud. 7as not desi0ned to speci+ica%%. test ot/er mode%s o+
emotion, suc/ as appraisa% mode%s, t/at t/emse%2es ma,e no predictions a:out t/e ro%e o+
%an0ua0e and conceptua% ,no7%ed0e in emotion perception. Appraisa% mode%s ma,e
speci+ic predictions a:out t/e ro%e o+ appraisa% >c/ec,s? or >action tendencies? +or t/e
production o+ +acia% e=pressions. Aside +rom e2idence su00estin0 t/at /ea%t/. adu%ts
ma,e appraisa%<consistent persona%it. in+erences a:out sco7%in0, poutin0 and smi%in0
+aces , t/ere is %itt%e e2idence speci+ica%%. assessin0 t/e ro%e o+ appraisa% c/ec,s in
emotion perception. Re%ati2e%. more studies /a2e addressed t/e ro%e o+ action tendencies
durin0 emotion perception, 7it/ most studies +ocusin0 on t/e percei2er;s 0enera%
approac/ 2. a2oidance :e/a2iors +o%%o7in0 t/e perception o+ discrete emotion in a posed
+ace . It t/us remains a possi:i%it. t/at patients cou%d sort :. appraisa% c/ec,s or action
tendencies i+ prompted to do so, :ut suc/ a question is :e.ond t/e scope o+ our stud..
'6
Emotion perception in semantic dementia
Our data demonstrate t/at participants did not spontaneous%. sort +aces :ased on
appraisa%s @e.0., 7/et/er t/e person e=pressin0 emotion /as contro% o2er t/e situation,
7/et/er t/e person e=pressin0 emotion +inds t/e situation certainA or action tendencies
@e.0., 7/et/er t/e person e=pressin0 emotion is %i,e%. to +%ee t/e situation or 7ou%d ma,e
t/e percei2er 7ant to +%ee t/e situationA. Nor did an. o+ t/e patients in our samp%e ma,e
comments re%ated to appraisa%s or action tendencies 7/en sortin0 +aces @e.0., none said
>/e %oo,s uncertain? or >/e is 0oin0 to run a7a.?A. One possi:i%it. is t/at t/e content o+
appraisa%s concernin0 t/e situation @e.0., ,no7in0 7/et/er t/e situation in 7/ic/ emotion
occurs is certain, contro%%a:%e, etc.A and ,no7%ed0e a:out 7/ic/ action tendencies
accompan. certain emotions are part o+ t/e discrete emotion concept ,no7%ed0e t/at
:ecomes impaired in semantic dementia. T/is /.pot/esis 7ou%d :e important to test in
+uture researc/.
In conc%usion, our data su00est t/at t/e A perception o+ a++ect and #A
cate0ori9ation t/at is supported :. emotion concept ,no7%ed0e are :ot/ important
>in0redients? in norma% emotion perception. T/ese +indin0s au0ment t/e 0ro7in0
ar0ument t/at discrete emotions are psychologically constructed e2ents t/at are +%e=i:%.
produced in t/e mind o+ a percei2er and dependent on conte=t, cu%ture and %an0ua0e,
rat/er t/an innate modu%es +or speci+ic in2ariant cate0ories . Accordin0%., it seems 7ort/
in2esti0atin0 in +uture researc/ 7/et/er t/e discrete emotion perception de+icits t/at /a2e
:een documented in a0in0 and in patients 7it/ neurops.c/iatric disorders ori0inate +rom
c/an0es in more +undamenta% ps.c/o%o0ica% processes @e.0., conceptua% processin0 andMor
a++ecti2e processin0A. $ina%%., t/e resu%ts presented /ere su00est t/at t/e t/eories o+
discrete emotion :ein0 disseminated in te=t:oo,s and scienti+ic papers t/rou0/out t/e
'
Emotion perception in semantic dementia
Bestern 7or%dEand :ein0 used to train securit. a0ents and ot/er 0o2ernment o++icia%sE
s/ou%d :e re+ined :. considerin0 t/e ro%e o+ discrete emotion concept ,no7%ed0e in
discrete emotion perception.
'#
Emotion perception in semantic dementia
Ac'nowled(ements
K.A.L. and M.". contri:uted equa%%. to manuscript preparation and s/ou%d :e considered
Coint +irst aut/ors. L.$.&. and &.C.D. contri:uted equa%%. and s/ou%d :e considered Coint
senior aut/ors. Be t/an, Dere, Issaco7it9 and Senn. Stan%e. +or t/eir assistance in
co%%ectin0 contro% data. T/is researc/ 7as supported :. a Nationa% Institutes o+ 3ea%t/
Director;s Pioneer a7ard @DPOD66''#A to Lisa $e%dman &arrett, a Nationa% Institute
on A0in0 0rant @R6<A"6#5I(6A, an A%9/eimer;s Association 0rant to &rad+ord
Dic,erson, and a 3ar2ard 1ni2ersit. MindM&rainM&e/a2ior Initiati2e Postdoctora%
$e%%o7s/ip to Kristen Lindquist. Be appreciate t/e commitment o+ our participants and
t/eir +ami%ies to t/is researc/.
''
Emotion perception in semantic dementia

'(
Emotion perception in semantic dementia
Fi(ure ). M" scans of patients E#, F% and &P. T<7ei0/ted MRI scans o+ @aA patient
E" @:A patient $J @cA and patient CP s/o7in0 %e+t<%atera%i9ed anterior tempora% %o:e
atrop/.G ima0es are s/o7n in radio%o0ica% orientation @t/e %e+t /emisp/ere appears on t/e
ri0/t /and side o+ t/e ima0eA.
'-
Emotion perception in semantic dementia
Fi(ure *. E+ample of face stimuli. E=amp%es o+ +ace stimu%i +rom t/e IASLa: set used
in t/e +ace sort tas,s.
'F
Emotion perception in semantic dementia
Fi(ure ,. E+amples of a control participants- performance on the free sort tas'. A
F5<.ear o%d man made si= pi%es to represent t/e si= cate0ories.
'4
Emotion perception in semantic dementia
Fi(ure .. Patient-s performance on the emotion free sort tas'. In E";s +ree sort, t/e
+irst pi%e contained predominant%. /app. +aces, t/e second pi%e contained predominant%.
'I
Emotion perception in semantic dementia
neutra% +aces and t/e t/ird pi%e contained predominant%. ne0ati2e +aces @sco7%in0,
poutin0, 7ide<e.ed and 7rin,%e<nosed +acesA. In $J;s +ree sort, t/e +irst pi%e contained a%%
/app. +aces, t/e second pi%e contained a%% neutra% +aces, and t/e t/ird and +ourt/ pi%es
contained a%% ne0ati2e +aces. In CP;s +ree sort, t/e +irst pi%e contained predominant%.
/app. +aces, t/e second pi%e contained a%% neutra% +aces, and t/e t/ird and +ourt/ pi%es
contained a%% ne0ati2e +aces.
'5
Emotion perception in semantic dementia
Fi(ure /. B/en as,ed to sort +aces into si= pi%es anc/ored 7it/ t/e num:ers <F, CP
created one pi%e +or positi2e +aces, one +or neutra% +aces and +our +or ne0ati2e +aces. T/is
tas, indicated t/e insta:i%it. in /er sortin0 +rom one instance to t/e ne=t.
(6
Emotion perception in semantic dementia
Table 1. Emotion Free Sort Performance
#
piles
NEG-NEUT POS-NEUT NEG-NEG NEUT-NEG POS-NEG NEG-POS NEUT-POS
%
Total
Errors
EG
a
3 1.66% 0% 46.67%* 5.83% 0% 1.66% 5.83%* 61.66%*
FZ
b
4 0% 0% 44.44%* 0% 0% 0% 0% 44.44%
CP
b
4 0% 0% 36.11%* 0% 0% 2.77% 0% 38.89%
O!
a
7.82
(SD=
2.99)
2.88% 0.13% 21.72% 2.80% 0.27% 0.55% 1.69% 30.04%
a
long variant of free sort

s!ort variant of free sort
* in"i#ates statisti#all$ "ifferent fro% #ontrols (&'.05)
!bbre"iations#
S$# stan"ar" "eviation
O!# ol"er a"(lts
NEG-NEUT) errors in *!i#! negative fa#es *ere &(t in a &ile of &re"o%inantl$ ne(tral fa#es
POS-NEUT# refers to errors in *!i#! &ositive fa#es *ere &(t in a &ile of &re"o%inantl$ ne(tral fa#es
NEG-NEG# errors in *!i#! one t$&e of negative fa#e *as &(t in a &ile #onsisting &re"o%inantl$ of anot!er negative fa#e
NEUT-NEG# errors in *!i#! ne(tral fa#es *ere &(t in a &ile of &re"o%inantl$ negative fa#es
POS-NEG# errors in *!i#! &ositive fa#es *ere &(t in a &ile of &re"o%inantl$ negative fa#es
NEG-POS# errors in *!i#! negative fa#es *ere &(t in a &ile of &re"o%inantl$ &ositive fa#es
NEUT-POS# errors in *!i#! ne(tral fa#es *ere &(t in a &ile of &re"o%inantl$ &ositive fa#es
Emotion perception in semantic dementia (#
Emotion perception in semantic dementia
Emotion perception, but not affect perception, is impaired with semantic memory
loss
Supplementary 0nline Materials
Additional Patient Data
Patients 7ere tested in t/e neuro%o0. c%inic at a %oca% &oston /ospita%. Be report
t/e neurops.c/o%o0ica% tests t/at 7ere administered as part o+ a :atter. per+ormed :. a
trained neurops.c/o%o0ist.
&ase )
&ase history and presentation
E" is a 46<.ear<o%d ma%e /i0/ sc/oo% 0raduate 7/o 7or,ed +or most o+ /is adu%t
%i+e as an en0ineer at a construction compan.. 3e presented in #66F 7it/ 0radua%%.
pro0ressi2e s.mptoms o+ di++icu%t. 7it/ >memor.? and 7ord +indin0 in speec/. At t/e
Table %. Performance on !ll Emotion Sort Tas&s
# piles NEG-
NEUT
POS-
NEUT
NEG-NEG NEUT-NEG POS-NEG NEG-POS NEUT-POS %
Total
Errors
FZ
+ree sort 4 0% 0% 44.44% 0% 0% 0% 0% 44.44%
,(%er an#!or 5 0% 0% 33.33% 0% 0% 2.78% 2.78% 38.89%
+a#e an#!or 8 0% 0% 19.44% 0% 0% 0% 0% 19.44%
-or" an#!or 6 0% 0% 27.78% 0% 0% 2.78% 0% 30.56%
CP
+ree sort 4 0% 0% 36.11% 0% 0% 2.77% 0% 38.89%
,(%er an#!or 6 2.86% 0% 34.29% 0% 0% 0% 2.86% 39.00%
+a#e an#!or 6 5.71% 0% 17.14% 0% 0% 0% 0% 22.00%
-or" an#!or 6 5.71% 0% 31.43% 0% 0% 0% 0% 36.00%
Emotion perception in semantic dementia
time o+ presentation, /is +ami%. reported t/at /e 7as /a2in0 di++icu%t. remem:erin0
7ords and /ad stopped readin0 :oo,s. 3e 7as sti%% doin0 t/e +ami%. +inances 7it/out
di++icu%t.. 3is +ami%. did not report c/an0es in mood or persona%it.. On /is +irst
e2a%uation in #66F, /e demonstrated 7ord<+indin0 di++icu%ties and anomia :ut norma%
a++ect and comportment. Structura% MRI demonstrated +oca% atrop/. o+ t/e %e+t tempora%
po%e and /e 7as dia0nosed 7it/ Primar. Pro0ressi2e Ap/asia<Semantic 2ariant o+
semantic dementia. $indin0s +rom a +u%% neurops.c/o%o0ica% :atter. per+ormed in #66F
are as +o%%o7s.
ntellectual abilities. T/is patient /ad norma% inte%%ectua% a:i%ities. 3e /ad an
a2era0e estimated inte%%i0ence score on t/e Besc/%er Test o+ Adu%t Readin0 and
per+ormed superior%. on t/e Ra2en;s Pro0ressi2e Matrices.
Attention and E+ecuti1e function. T/is patient /ad norma% attention and
e=ecuti2e +unction. Per+ormance 7as in t/e a2era0e ran0e on an auditor. attention span
test and on t/e Menta% Contro% su:test o+ t/e Besc/%er Memor. Sca%e III. 3e 7as in t/e
superior ran0e +or Part A o+ t/e Trai% Ma,in0 Test @5 secA. 3e /ad one sequencin0 error
and one set<s/i+tin0 error on Part & o+ t/e Trai% Ma,in0 Test, :ut time to comp%etion 7as
4' sec.
Memory. T/is patient /ad norma% reco0nition memor., :ut consistent 7it/ t/e
semantic dementia dia0nosis, /ad poor per+ormance on t/e 7ord reca%% portion o+ t/e
Consortium to Esta:%is/ a Re0istr. +or A%9/eimer;s Disease memor. tas,.
2isuospatial performance. T/is patient /ad norma% 2isuospatia% s,i%%s. 3e
per+ormed 7e%% 7it/ no omissions on t/e %etter cance%%ation tas,, /ad intact per+ormance
on t/e Lisua% Or0ani9ation Test, and per+ormed +%a7%ess%. on t/e &enton Lisua% $orm
((
Emotion perception in semantic dementia
Discrimination Tas,.
3an(ua(e. Consistent 7it/ t/e dia0nosis o+ semantic dementia, t/is patient /ad
impaired per+ormance on %an0ua0e tests. Le=ica% 2er:a% +%uenc. 7as impaired @tota% $AS
K #A, as 7as semantic 2er:a% +%uenc. @anima%s K A. Per+ormance on t/e &oston
Namin0 Tas, 7as a%so impaired @'#MF6 spontaneous%. p%us ( additiona% items 7it/
p/onemic cuesA.
Profile at time of emotion testin(
&. #66I, 7/en E" comp%eted t/e present e=perimenta% tas,s, /e /ad under0one
pro0ressi2e impairment in t/e domain o+ %an0ua0e and semantic memor.. 3e 7as
e=/i:itin0 anomia and semantic memor. impairment 7it/ +%uent and articu%ate speec/.
Per+ormance on con+rontationa% namin0 @IM- on a::re2iated &oston Namin0 TestA and
2er:a% +%uenc. tas,s 7as se2ere%. impaired @' $ 7ords and 4 anima%s in one minute eac/A
a%t/ou0/ /e 7as sti%% a:%e to repeat %en0t/. sentences. 3e /ad se2ere impairments in :ot/
immediate and de%a.ed 2er:a% memor. and 7as no %on0er a:%e to use cues to increase /is
memor. per+ormance @no 7ords reca%%ed a+ter a :rie+ de%a.A. 3is Mini Menta% State E=am
score o+ 5M'6 7as impaired on%. as a resu%t o+ /is 7ord retrie2a% impairment.
Amidst t/ese %an0ua0e de+icits, E" demonstrated norma% memor. +or 2isua%
materia% and norma% 2isua% construction @e.0., /e 7as a:%e to dra7 a c%oc, and p%ace t/e
/ands correct%. to 6 minutes a+ter A. 3is ca%cu%ationa% a:i%ities remained norma%H /e
7as a:%e to per+orm simp%e addition and su:traction. 3is mood 7as Cud0ed c%inica%%. to
:e norma% and /e demonstrated appropriate a++ect durin0 c%inica% and researc/ 2isits. 3is
son reported no si0ni+icant :e/a2iora% pro:%ems at /ome.
(-
Emotion perception in semantic dementia
&ase *
&ase history and presentation
$J is a F(<.ear o%d ma%e 7it/ a Masters o+ &usiness Administration and Certi+ied
Pu:%ic Accountant de0ree, 7/o 7or,ed as an accountant. 3e presented in #665 7it/
0radua%%. pro0ressi2e 7ord +indin0 di++icu%ties. In particu%ar, /e +or0ot names o+ peop%e
/e /ad ,no7n +or man. .ears. Once an a2id reader, /e :e0an /a2in0 di++icu%ties
+o%%o7in0 ne7spaper artic%es. 3e reported mi%d depression and an=iet. as a resu%t o+ /is
s.mptoms, :ut 7as not dia0nosa:%e 7it/ a +orma% mood disorder. 3e /ad no :e/a2iora%
s.mptoms or persona%it. c/an0e. On /is +irst e2a%uation, /e demonstrated si0ni+icant
7ord +indin0 di++icu%ties and semantic parap/asic errors durin0 casua% con2ersation.
Structura% MRI demonstrated :i%atera% tempora% po%e atrop/. 7it/ more prominent
atrop/. in t/e %e+t tempora% po%e. 3e 7as dia0nosed 7it/ PPA<S @semantic dementiaA.
$indin0s +rom a +u%% neurops.c/o%o0ica% :atter. per+ormed in #665 are as +o%%o7s.
ntellectual abilities. T/is patient /ad norma% inte%%ectua% a:i%ities. 3e /ad
a2era0e Perceptua% Reasonin0 and Bor,in0 Memor. on t/e Besc/%er Adu%t Inte%%i0ence
Sca%e<IL. 3e per+ormed in t/e /i0/ ran0e on Matri= Reasonin0 @5
st
percenti%eA.
Attention and E+ecuti1e function. T/is patient /ad norma% attention and
e=ecuti2e +unction. 3is di0it span 7as /i0/ a2era0e @4 +or7ard and - in re2erseA, as 7as
/is 2isua% attention @+or7ard spanK F, :ac,7ard span K (<-A. 3e /ad no di++icu%t. on a
0rap/omotor sequencin0 tas, @a%ternatin0 M and NA. Per+ormance on t/e DKE$S Trai%
Ma,in0 Test 7as :order%ine @Trai%s A, (' seconds, (t/ percenti%eG Trai%s &, 6 seconds,
#nd percenti%eA. 3e demonstrated no di++icu%t. on a 0oMno<0o tas,. 3is 7as a:%e to
quic,%. %earn a seria% /and mo2ement sequence 7it/ /is ri0/t /and and 7as a:%e to
(F
Emotion perception in semantic dementia
trans+er %earnin0 to /is %e+t /and. Concept +ormation and co0niti2e +%e=i:i%it. 7as
preser2ed @BCST, FMF cate0oriesA.
Memory. T/is patient /ad norma% reco0nition memor., :ut consistent 7it/ t/e
semantic dementia dia0nosis, /ad poor per+ormance on t/e 7ord retrie2a%. On t/e
CERAD 6<7ord %ist, /is immediate reca%% 7as norma% @-, I, and I 7ordsG Tota% Learnin0
K #, (4t/ percenti%eA. A+ter I minutes, /e on%. reca%%ed ' 7ords @st percenti%eA.
De%a.ed reco0nition 7as in<%ine 7it/ encodin0, @6M6 7ords, +a%se positi2eA. On t/e
$ree and Cued Se%ecti2e Remindin0 Test, /e /ad mi%d di++icu%t. retrie2in0 ne7 materia%
across t/e t/ree %earnin0 tria%s @$ree Reca%% K ##A, :ut :ene+ited +rom t/e pro2ision o+
cues paired 7it/ t/e items at t/e time o+ %earnin0 @$ree and Cued Tota% K ((A.
2isuospatial s'ills. T/is patient /ad norma% 2isuospatia% s,i%%s. 3is per+ormance
on t/e Re.<O +i0ure cop. 7as +u%%. intact a%t/ou0/ t/e desi0n 7as dra7n in a se0mented
+as/ion.
3an(ua(e. Consistent 7it/ t/e dia0nosis o+ semantic dementia, t/is patient /ad
impaired per+ormance on %an0ua0e tests. Lisua% con+rontation namin0 7as impaired on
t7o measures @&oston Namin0 Test, ''MF6, Mu%ti%in0ua% Ap/asia E=amH Lisua% Namin0,
#M'6A. P/onemic cuein0 7as on%. minima%%. /e%p+u%, 7it/ an additiona% ' items named.
3e /ad mi%d di++icu%t. on an auditor. 7ord picture matc/in0 tas,, se%ectin0 t/e correct
picture @out o+ # c/oicesA +or #5M'# concrete 7ords @-
t/
percenti%eA. 3e a%so /ad di++icu%t.
compre/endin0 a:stract 7ords, 7/ere accurac. in c/oosin0 7/ic/ o+ t7o 7ords matc/ed
a tar0et 7ordTs meanin0 @e.0., does naU2e mean innocent or stupidRA +e%% in t/e impaired
ran0e. In contrast, /is a:i%it. to access ot/er aspects spo,en %an0ua0e, inc%udin0
p/ono%o0ica%, morp/o%o0ica% and s.ntactic in+ormation 7as intact. 3e 7as a:%e to
(4
Emotion perception in semantic dementia
distin0uis/ 7ords +rom non<7ords, to distin0uis/ 7ord meanin0 :ased on morp/o%o0.
@e.0., emp%o.er 2s. emp%o.ee, :us 2s. :ussesA, and 7as a:%e to appreciate t/e s.ntactic
+orm o+ sentences as assessed on a sentence<picture matc/in0 tas,, /o7e2er, and a%%
scores +e%% in t/e a2era0e ran0e. &asic compre/ension usin0 t/e to,en test 7as preser2ed.

Profile at time of emotion testin(
&. #6#, 7/en $J comp%eted t/e present e=perimenta% tas,s, /e /ad under0one
pro0ressi2e impairment in t/e domain o+ %an0ua0e and semantic memor.. 3e 7as
e=/i:itin0 anomia and semantic memor. impairment 7it/ +%uent and articu%ate speec/.
Per+ormance 2er:a% +%uenc. tas,s 7as impaired @Ler:a% +%uenc. +or anima%s K IG
2e0eta:%es K #A. 3is Mini Menta% State E=am 7as #-M'6. Ler:a% memor. encodin0 7as
impaired :ut /e retained 7/at /e %earned a+ter a #6<minute de%a. @Bec/s%er Lo0ica%
Memor. Immediate K (G De%a.ed K (A.
Amidst t/ese %an0ua0e de+icits, $J disp%a.ed norma% 2isuospatia% +unction @/e
7as a:%e to cop. a picture o+ a penta0on on t/e Mini Menta% State E=am and accurate%.
dra7 a c%oc, 7it/ t/e instructed timeA. A%t/ou0/ some aspects o+ e=ecuti2e +unction
demonstrated pro0ressi2e impairment +rom #665 @Trai% Ma,in0 Test A -6sG Trai% Ma,in0
Test & #' sA, ot/ers remained re%ati2e%. intact @e.0., di0it span +or7ard 4, :ac,7ard, FA.
3is mood 7as Cud0ed c%inica%%. to :e norma% and /e demonstrated appropriate a++ect
durin0 c%inica% and researc/ 2isits. 3is 7i+e reported no :e/a2iora% pro:%ems at /ome.
&ase ,
&ase history and presentation
(I
Emotion perception in semantic dementia
CP is a -'<.ear<o%d +ema%e 7it/ a Master;s De0ree in Education 7/o 7or,ed as
an administrator at a :an, :e+ore retirin0. S/e presented in #66I 7it/ 0radua%%.
pro0ressi2e 7ord +indin0 di++icu%ties. At t/e time o+ presentation, /er +ami%. reported t/at
s/e /ad :een stru00%in0 to +ind 7ords @most%. nounsA and /ad e=perienced some minor
di++icu%ties 7it/ memor. retrie2a% +or con2ersations. T/e. denied an. c/an0es in mood or
persona%it.. On /er +irst e2a%uation, s/e demonstrated 7ord<+indin0 di++icu%t. 7it/
anomia and pauses durin0 spontaneous speec/ :ut norma% a++ect and comportment.
Structura% MRI demonstrated %e+t tempora% po%e atrop/.. S/e 7as dia0nosed 7it/ PPA<S
@semantic dementiaA. $indin0s +rom a +u%% neurops.c/o%o0ica% :atter. per+ormed in #66I
are as +o%%o7s.
ntellectual abilities. T/is patient /ad norma% inte%%ectua% a:i%ities. S/e /ad a /i0/
a2era0e estimated inte%%i0ence score on t/e Besc/%er Test o+ Adu%t Readin0.
Attention and E+ecuti1e function. T/is patient /ad norma% attention and
e=ecuti2e +unction. Per+ormance 7as in t/e superior ran0e on an auditor. attention span
test and a2era0e on t/e Menta% Contro% su:test o+ t/e Besc/%er Memor. Sca%e III. Di0it
span 7as 4 +or7ard and F in re2erse. Per+ormance on a num:er<%etter sequencin0 tas,
7as in t/e a2era0e ran0e. Bisconsin Card Sort 7as per+ormed at an a2era0e %e2e% 7it/ no
perse2erati2e errors and F cate0ories o:tained. Per+ormance on DKE$S Trai% Ma,in0
Test 7as in t/e /i0/ a2era0e to superior ran0e. Co%or 7ord inter+erence 7as in t/e
a2era0e to /i0/ a2era0e ran0e.
Memory. T/is patient /ad norma% memor.. Per+ormance on t/e Besc/%er
Memor. Sca%e III Lo0ica% Memor. 7as in t/e /i0/ a2era0e ran0e +or immediate reca%%
@4-
t/
percenti%eA, 7it/ '6 minute de%a.ed reca%% in t/e /i0/ a2era0e ran0e @I(
t/
percenti%eA.
(5
Emotion perception in semantic dementia
One /undred percent o+ encoded materia% 7as retained a+ter t/e de%a.. Lisua% memor.
7as in t/e /i0/ a2era0e ran0e @#6<minute de%a.ed reca%% o+ Re.<O +i0ure K IF
t/

percenti%eA.
2isuospatial s'ills. T/is patient /ad norma% 2isuospatia% s,i%%s. 3er 2isuospatia%
attention 7as /i0/ a2era0e on t/e Besc/%er Adu%t Inte%%i0ence Sca%e III. Re.<O +i0ure
cop. 7as 5-
t/
percenti%e.
3an(ua(e. Consistent 7it/ t/e semantic dementia dia0nosis, t/is patient /ad
impaired per+ormance on %an0ua0e tests. Per+ormance on t/e &oston Namin0 Tas, 7as
impaired @4M'# spontaneous%.G additiona% correct response 7as o:tained 7it/
p/onemic cuesG semantica%%. correct descriptions 7ere o+ten o:tained @e.0., >.ou t/ro7
it? +or dartA. Semantic access +rom pictures 7as re%ati2e%. maintained on t/e P.ramids
and Pa%m Trees test @(5M-#A. Le=ica% 2er:a% +%uenc. 7as a2era0e @tota% $AS K #5A :ut
semantic 2er:a% +%uenc. 7as :order%ine @DKE$S cate0or. tota% K #-A.
Profile at time of emotion testin(
&. #6, 7/en CP comp%eted t/e present e=perimenta% tas,s, s/e /ad under0one
pro0ressi2e impairment in t/e domain o+ %an0ua0e and semantic memor.. S/e 7as
e=/i:itin0 se2ere anomia and semantic memor. impairment 7it/ +%uent and articu%ate
speec/. 3er Mini Menta% State E=am 7as #4M'6, 7it/ errors due to %an0ua0e de+icits.
Amidst t/ese %an0ua0e de+icits, /er :asic ca%cu%ationa% s,i%%s @addition and su:tractionA,
2isuospatia% s,i%%s @e.0., s/e 7as a:%e to cop. a picture o+ a penta0on on t/e Mini Menta%
State E=am and accurate%. dra7 a c%oc, 7it/ t/e instructed timeA and attention remained
intact. 3er mood 7as Cud0ed c%inica%%. to :e norma% and s/e demonstrated appropriate
-6
Emotion perception in semantic dementia
a++ect and comportment durin0 c%inica% and researc/ 2isits. 3er /us:and reported no
:e/a2iora% pro:%ems at /ome.
-