doi 10.1098/rstb.2000.0690 Sensorysystemevolution at theorigin of craniates AnnB. Butler Krasnow Institute for Advanced Studyand Department of Psychology,MSN 2A1,George Mason University, Fairfax,VA22030,USA ([email protected] ) Themultiple events atthe transitionfrom non-craniate invertebrate ancestors tocraniates included the gainand/ orelaborationof migratory neural crest andneurogenic placodes. These tissues giverise tothe peripherallylocated, bipolar neurons of allnon-visual sensory systems. Thebrain was also elaborated at orabout this same time. Were the peripheraland central events simultaneousor sequential ?Aserial transformationhypothesis postulates that pairedeyes andan enlarged brain evolved before the elabora- tionof migratory neural crest ^placodalsensory systems. Circumstantialevidence for this scenariois derivedfrom the independentoccurrence ofthe combinationof large,paired eyes plusa large,elaborated brainin atleast three taxa(cephalochordates, arthropods and craniates) andpartly from the exclusivity ofthe diencephalonfor visual system-related distalsensory components versus the restricted distribution ofmigratory neural crest ^placodalsensory systems tothe remainingparts ofthe neuraxis.This scenario accountsfor the similarity ofall central sensorysystem pathwaysdue to the primaryestablishment of descendingvisual pathways via the diencephalonand midbrain tectum tobrainstem motorregions and the subsequent exploitationof the same central beachheadby the migratoryneural crest ^placodal systems asatemplate fortheir organization. Keywords: cephalochordates;cerebral vesicle ;visualsystem addresses the evolutionof craniate sensory system 1.INTRODUCTION componentsin the central andperipheral nervous Thetransition from an invertebrate chordate ancestral systems. conditionto that ofthe ¢rst true craniates(hag¢ shes and vertebrates) wasmarked by multiple seminalchanges 2.MIGRATORY NEURAL CREST AND PLACODES (Northcutt 1996).Thesechanges included the gainof a neurocraniumand alterations in the embryologicaldevel- Manyof the changesat the non-craniate ^craniate opmentof the paraxialmesoderm inthe headregion that transitioncan be attributed tothe gain(and/ orelabora- resulted inthe gainof a muscular pharynxin the bran- tion)of migratory neural crest andneurogenic placodes chiomeric region.They also encompassed numerous (Northcutt 1996).Inthe earlystages ofnervous system changesin the nervoussystem. Thebrain was markedly morphogenesisin craniates, a populationof ectodermal enlargedand elaborated in conjunction with the forma- cells atthe lateralaspect ofthe invaginatingneural tube tionof paired eyes. Migratory neural crest andneuro- forms the neuralcrest. Someof the neuralcrest cells genicplacodes were gained(and/ orelaborated); these remainnear the neuraltube andgive rise toor contribute tissues producethe bipolarsensory neurons of the periph- tothe sensorybipolar neurons of spinaland cranial nerve eralnervous system. ganglia,while other neuralcrest cells migrateventro- Majornew insights havebeen made recently intohow laterallyto give rise toor contribute to a host oftissues, this transitionoccurred as the result ofthe duplicationof includingthe motorganglia of the peripheralnervous regulatorygenes, and a crediblescenario describing the system, calcitoninand chroma¤ n cells ofthe gut,the elaborationof craniatecharacters from acephalochordate- barsof the visceralarches, the neurocraniumand sensory likeancestral condition has been postulated (Holland & capsulesof the pairedsense organs,dermal skeleton, Graham1 995).Questions remain,however ,including: melanocytesand teeth (Northcutt 1996).Neurogenic whetherthe elaborationof the craniatebrain occurred placodes(subsequently referred tosimply as placodes) simultaneouslywith the gainof migratory neural crest consist ofthickened patches ofepithelium lateralto the andcraniate placodal systems; whether allaquatic regionof the neuralcrest, whichgive rise tomost orall craniatesensory systems evolvedsimultaneously or not; ofthe bipolarsensory neurons of the olfactoryand howall of the central pathwaysfor these sensorysystems terminal nerves (andthe vomeronasalnerve in tetra- evolved;why the central pathwaysfor all the di¡erent pods),the taste-receptive cranialnerve components, and modalitieshave such similar organization;and how the the vestibulocochlearand lateral line nerves, aswell as branchiomericmotor column evolved in concert withthe tothe receptor cells forthe last twosystems (Northcutt branchiomericmuscles ofthe visceralarches. Thispaper 1996). Phil. Trans.R. Soc.Lond. B (2000) 355, 1309^1313 1309 © 2000The RoyalSociety 1310A.B.Butler Originof craniate brain 3.CRANIATE CENTRAL SENSORY PATHWAYS pallium Thechanges within the central nervoussystem atthe non-craniate ^craniatetransition cannot be accounted for bye¡ ects and/orproducts ofthe more lateralregion of the striatum developingnervous system öthe migratoryneural crest andplacodes. The forebrain, midbrain, and hindbrain were allmarkedly expanded, and a host ofmultisynaptic, large central pathwaysfor ascending sensory system projections paired diencephalon tothe telencephalonwere established. Any plausible eyes scenarioof craniate brain evolution must accountfor the gainof these multisynapticcentral pathways,which öas the generalcondition across craniates öallexhibit the same pattern oforganization.All sensory system pathways havebipolar a¡ erent neuronsthat either innervate receptor cells ortransduce sensoryinformation themselves tectum attheir distalprocesses (see Hodos& Butler 1997).Forthe retina,these bipolarneurons are neural tube derivatives. Forallnon-visual sensory systems, the bipolarneurons are partof the peripheralnervous system andare derived PMC from migratoryneural crest and/orplacodes. Inall sensory systems, the bipolarneurons project to multipolarneurons that lie withinthe central nervous mNC/P system. Sincethese bipolar-receptiveneurons are the sensory hindbrain initialmultipolar neurons in the sensorypathway ,they systems arereferred tohere as¢rst-ordermultipolar neurons. The pattern ofprojections for the latter sets ofneurons is similar forall sensory systems, asshownin ¢ gure1 .From spinal cord allsets of¢ rst-ordermultipolar neurons that arelocated Figure1. Diagram of theoverall, generalized plan of caudalto the telencephalon,projections arise that are ascendingsensory systems (thick arrows) and descending either tothe midbrainroof and thence tothe dience- motorpathways (thin arrows). The basicplan of sensory phalonand/ orto the diencephalondirectly .Theretinal systemsis a relayfrom bipolar neurons to ¢rst-order ganglioncells giverise toboth midbrain-relay and direct multipolarneurons, which thenproject, as shownwith the pathways,while the other,neuralcrest ^placodal,sensory thickarrows (from the retina and hindbrain in this¢ gure) systems eachgive rise toboth pathways or to one or the tothediencephalon directly or indirectlyand from the other.From the diencephalicsite foreach sensory diencephalonto thetelencephalon. For the sake of illustrating themain point, a numberof pathwaysare omitted from this pathway,projectionsto the telencephalonarise. Avaria- ¢gure,including ascending projections from the spinal cord tionon the theme is withthe olfactorysystem (not (suchas thespinothalamic pathway) and projections from includedin ¢ gure1 ); projectionsfrom olfactory bipolar thediencephalon to thestriatum in thetelencephalon. Also neuronsare to ¢ rst-ordermultipolar neurons that are omittedare telencephalic sensory systems, which area locatedwithin the olfactorybulb, and relay to the dience- variationon thesame theme; the olfactory system, for phalonoccurs viathe olfactorypallium rather thanvia example,projects to thediencephalon via its own area of the tectum. thepallium, and a subsequentrelay then occurs from the diencephalonto adi¡erent pallial region. mNC/ P,migratory neuralcrest/ placodes;PMC, primarymotor centre. 4.THE ANCESTRAL CHORDATE CONDITION Recent anatomicalwork and new ¢ ndingson brainregions of craniates. Gene expressionstudies homeoboxgenes and their expressionpatterns indicate supportthese interpretations (Holland& Graham1 995; that the extantcephalochordate Branchiostoma , the Holland et al. 1996). lancelet,may in fact be a reasonableapproximation of However,acredibleprecursor ofthe craniatebrain is the actualcommon ancestor of modern lancelets and notthe onlyrelevant neural tissue that lancelets andtheir their craniatecousins, at least inmost respects. Lacalli invertebratechordate relatives have to o¡ er. Holland et al. (1996)and his co-workershave demonstrated rostral (1996)have identi¢ ed gene expression patterns inthe specializationsin the neuraltube oflancelets that appear lanceletthat indicatethe presence ofneural crest- tobe homologous to some ofthe rostral neuraltube struc- precursor tissue inthe epidermis dorsalto the developing tures incraniates. In the lancelet,a cerebralvesicle is neuraltube. Likewise,W ada et al.(1998)have found present andhas a frontalorgan, or eye, consisting of similar evidencein ascidians, which are the chordate pigmentedand associated cells atits rostral endthat may outgroupto lancelets andcraniates, indicating the behomologousto the pairedeyes ofcraniates.This vesicle existence ofplacodal tissue that givesrise toa sensory alsocontains other structures that maybe homologous to organhomologous to the craniateear .These¢ ndingsare the epiphysisof vertebrates (whichhag¢ shes lack)and the excitingbut notentirely surprising, since the existence ofa infundibularregion