AnimalSentience2016.X:CommentaryonKeyonFishPain
FishBrainsandBehaviourIndicateCapacityforFeelingPain
CommentaryonKeyonFishPain
DonaldM.Broom
CentreforAnthrozoologyandAnimalWelfare
UniversityofCambridge
Abstract: Studies of behaviour are of major importance in understanding human
pain and pain in other animals such as fish. Almost all of the characteristics of the
mammalianpainsystemarealsodescribedforfish.Emotions,feelingsandlearning
from these are controlled in the fish brain in areas anatomically different but
functionallyverysimilartothoseinmammals.Theevidenceofpainandfearsystem
functioninfishissosimilartothatinhumansandothermammalsthatitislogicalto
concludethatfishfeelfearandpain.Fisharesentientbeings.
Donald M. Broom [email protected]
Emeritus Professor of Animal Welfare,
Cambridge University, has developed
concepts and methods of scientific
assessmentofanimalwelfare.
http://www.animal-welfareindicators.net/site/index.php/professor-donald-m-broom
Key(2016)isscornfulaboutevidencefromstudiesoffishbehaviourindicatingthat
fishareawareandfeelpainbutpresentsathoroughexplanationofthepainsystem
inthehumanbrainandconcludesthatfishcouldnotfeelpain,orhaveanyother
feelings,astheydonothavethebrainstructuresthatallowpainandotherfeelings
inhumans.Section2ofhispaperemphasises“thecorticaloriginsofhumanpain”
andstatesthat“structuredeterminesfunction,”explainingthefunctionsofthefive
layersofthehumancortex.Healsoarguesthatthereis“noevidenceforthe
emergenceofnovelpainregionsinthefishnervoussystem”because“thecircuitryis
inadequate”and“feedforwardpathways”aresimpleexplanationsforresponses
apparentlyparallelwithwhatoccursinthebrainwhensomethingisfeltinhumans.
Keyperpetuatesthedistinctionbetweennociceptionandpain,whichisarelicof
attemptstoemphasisedifferencesbetweenhumansandotheranimalsorbetween
"higher"and"lower"animals.Wherepainisanaversivesensationandfeeling
associatedwithactualorpotentialtissuedamage(Broom2001,modifiedafter
InternationalAssociationfortheStudyofPain,Iggo,1984),theuseoftheterm
nociception,whichseparatesonepartofthepainsystemfromotherparts,should
bediscontinued.Thesystemshouldbeconsideredasawhole(Wall1992,Broom
2001,2014).
Theselectiveadvantageofbeingabletofeelandlearnfrompain,fearandother
feelingshasbeenarguedforbyBroom(1998,2001,2014),Dawkins(2012),and
Sneddonetal.(2014).Activeanimalswithsophisticatedbehaviour,suchasall
1 AnimalSentience2016.X:CommentaryonKeyonFishPain
vertebratesandcertaininvertebrates,needacertainlevelofpainandotherfeelings
inordertorespondeffectivelytotheirenvironmentandsurvive.Hencepainandfear
systemsarephylogeneticallyoldandveryunlikelytohavesuddenlyappearedin
mammalsorinhumans.
Keyissuesinanydiscussionoffishwelfarearewhetherfishareawareofwhatis
happeningaroundthem,whethertheyarecapableofcognitiveprocessingand
whethertheycanhavefeelingssuchaspain(Chandrooetal.2004,Broom2007,
2014,2015,BroomandFraser2015).Ourbestevidenceforpainandotherfeelings
inhumansisderivedfromobservationsofbehaviour.Evidencefromhuman
reportingislessreliableandtheanatomicalevidenceisoflittleusewithout
observationsofbehaviourandphysiology.
Therehasbeenevidenceformanyyearsthatsomefishmusthavemental
representationsoftheirenvironmentinordertobeabletonavigate(Reese,1989;
Rodriguezetal.,1994),learnspatialrelationships(Odling-SmeeandBraithwaite,
2003),useinformationaboutsequencesofspatialinformation(BurtdePerera,
2004),recognizesocialcompanions(Swaneyetal.,2001),andavoidforsome
monthsoryearsplaceswheretheyhavepreviouslyencounteredapredator(Czanyi
andDoka,1993)orwerecaughtonahook(Beukema,1970).Recentlearningstudies
(Salwiczeketal.,2012,PepperbergandHartsfield,2014)showedthatinacomplex
learningtaskinwhichtheyhavetolearntodiscriminatereliablefromephemeral
foodsources,cleaner-wrassefish(aswellasparrots)performbetterthan
chimpanzees,orangutansorcapuchinmonkeys.Itislikelythatmanyofthesefish
abilitiesareassociatedwithsomedegreeoffeeling.Thetimingofeventscanbe
integratedtoallowfishtoproduceappropriateavoidanceresponses(Portavellaet
al.,2004;Yueetal.,2004).Itisdifficulttoexplaintheresultsoftheirstudieswithout
assumingthatthefishfeelfear.
EvidenceforpaininfishisreviewedbyBraithwaite(2010)andSneddonetal(2014).
Fishnociceptorsareverysimilartothoseofmammalsand,ofthe18criteriaforpain
perceptionlistedbySneddonetal(2014),17arecommontofishandmammals;only
relieflearninghasnotyetbeendemonstratedforfish.Forexample,intherainbow
trout,Onchorhynchusmykiss,anatomicalandelectrophysiologicalinvestigationof
thenociceptorsconnectedtothetrigeminalnervehasrevealedthatthesefishhave
twotypesofnociceptor,A-deltaandcfibres(Sneddon,2002;Sneddonetal.,2003a).
ThetransmittersubstanceP,andtheanalgesicopioidenkephalinsandβ-endorphin,
whichactasendogenousanalgesicsinmammals,arepresentinfish(RodriguezMoldesetal.,1993;Zacconeetal.,1994;BalmandPottinger,1995)andthe
behaviouralresponsesofgoldfishtoanalgesicsarethesameasinrats(Ehrensinget
al.,1982).WhenSneddonetal.(2003b)administeredweakaceticacidsolutionor
beevenomtothemouthofatrout,thefishrestedonthesubstratum,rockedfrom
sidetosideandrubbedtheirsnoutsonsolidsurfaces.Thesebehavioursstopped
whentheanalgesicmorphinewasgiven.
Infishthepartsofthebrainusedduringfearandpainresponsesarenot
anatomicallythesame(Broglioetal.,2003)asinmammals,butthefunctionisvery
2 AnimalSentience2016.X:CommentaryonKeyonFishPain
similar.Differentgroupsoffishmayusedifferentpartsoftheirbrainstoshowfear
andpainresponsesandlearnfromthem.Recentinformationaboutfearandpain
behaviour(Portavellaetal.2004)showsthatfishhaveintheirbrainsareaswith
functionsthatcloselyparallelthoseoftheamygdalaandhippocampusinmammals.
Thesearethebrainareasinmammalsthatprocessemotion,feelingandlearning
fromemotions.Insomefish,themedialandlateraltelencephalicpalliumprocess
emotionandlearning.Kawakamiandcolleagueshaveshownthatzebrafish,learning
fromafearsituation,havebrainactivityinthehabenulaandotherareasandthat
transgenicfishthatlacksuchareas,andnormalfishtreatedwithaneurotoxinthat
targetssuchareas,cannotrespondtoandlearnfromfearresponses.Asakawaetal.
(2008)describetheproductionofsucheffectsinthetransgeniczebrafish,Mutoet
al.(2013)demonstratevisualizationofneuronalactivityintheoptictectumoflarval
zebrafishduringactivebehaviour,andAgetsumaetal.(2010)giveevidenceforthe
habenulabeingcriticalforfear-dependentlearninginzebrafish.Furtherworklinks
theimagingandbrainareadeletionevidenceforthefunctions(Kawakami,personal
communication).
Fishdonothaveanamygdalaandhippocampusthatisanatomicallyhomologousto
thoseofhumans,buttheyhaveanalogousbrainareaswhosefunctionistocontrol
andlearnfromemotionalresponses.Keyarguesthat“neitherthemedialpalliumnor
thewholepalliumisrequiredforescapebehavioursfromelectricshockstimuliin
fish”andthatablationofthemidbrainoptictectumingoldfishdoesnotaffect
escaperesponses.However,suchescapemaybecontrollablebyadifferentbrain
area.Key’sargumentabouttheeffectsoflesionsonpallialsub-regionsinfishdoes
notshowthatfishdonotfeelpain.ThefindingsofPortavella,Kawakamiandothers
stronglysupportstheexistenceandfunctioningofsystemsforemotionalresponse
toandlearningfromfearandpaininfish.
IagreewithKeythat“paininvolvesconsciousneuralprocessing”butconcludethat
theevidenceofpainsystemfunctioninfishissosimilartothatinhumansandother
mammals,itisnotlogicaltodeducethatfishcannotfeelpain.Fisharesentient
beingsandpublicattitudestothemaregraduallychangingasscientificevidencefor
theircapabilitiesaccumulates(Broom2014).
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