Sensory System Evolution at the Origin of Craniates

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 elaborationof 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 chiomericregion. 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 froma cephalochordate- 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 of epithelium lateralto the andcraniate placodal systems; whetherall aquatic regionof the neuralcrest, whichgive rise tomost orall craniatesensory systems evolvedsimultaneously or not; ofthe bipolarsensory neurons of the olfactoryand howall of the centralpathways for these sensorysystems terminal nerves (andthe vomeronasalnerve in tetra- evolved;why the centralpathways for 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. This paper 1996).

3.CRANIATE CENTRAL SENSORY PATHWAYS pallium Thechanges within the central nervoussystem atthe non-craniate ^craniatetransition cannot be accounted for bye¡ ects and/orproductsof the more lateralregion of the striatum developingnervous system öthe migratoryneural crest andplacodes. The forebrain, midbrain, and hindbrain wereall markedly 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 frommigratory neural crest and/orplacodes. Inall sensory systems, the bipolarneurons project to multipolarneurons that liewithin the 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 not entirely surprising, since the existence ofa infundibularregion of craniates.Caudal to these structures widevariety of peripheral sensory neurons with is aregionthat mayencompass the midbrainand hind- projectionsinto the central nervoussystem ininvertebrates

Phil.Trans.R. Soc.Lond. B (2000) Originof craniate brain A.B.Butler 1311 is welldocumented and extensively studied, oneexample Graham1 995).Therostral neuralplate derivatives of beingthe proprioceptivehair cell sensorysystem insquid pairedeyes, diencephalon and mesencephalon, along (Preuss &Budelmann1995) .Thus,before the ¢rst true withhindbrain regions, could thus havebeen elaborated craniatesappeared, cephalopods and arthropods had beforethe gainof the neuralfolds with their derivatives, exploitedthe developmentalpath to large brains and includingthe telencephalichemispheres, migratory pairedeyes, and in the ancestralinvertebrate chordate neuralcrest andplacodes. line,neural crest, placodaland brain precursors werein Severallines ofcircumstantial evidencesupport the place.With the evolutionarystage thus fullyset, canwe plausibilityof a serial transformation.First, onecan note nowreconstruct the sequence ofthe play? that across allbilaterally symmetrical animals,the presence ofan enlarged, elaborated brain is oftenlinked withthe presence oflarge, paired, lateral eyes. F urther, 5.CONCURRENT GAIN AND SERIAL this combinationhas arisen multiple times independently TRANSFORMATION HYPOTHESES incephalopods, arthropods and craniates, and can arise Thatthe elaborationof migratory neural crest and withor without the elaborationof the migratoryneural craniateplacodes with their resultant productionof cell crest^placodalsensory systems that arepresent incrani- types, includingthe bipolarneurons of the peripheral ates. Incontrast, inthe normalphenotypes of bilaterally nervoussystem, occurredat the same time asthe elabora- symmetrical animals,the reverse combinationof elabo- tionof the brain(and the rest ofthe central nervous ratedmigratory neural crest ^placodalsensory systems system) hasbeen suggested ( Holland& Graham1 995; withan enlarged, elaborated brain but without large, Northcutt 1996)and is referred tohere asthe `concurrent paired,lateral eyes hasnever arisen. The implication of gainhypothesis’ .Northcutt (1996)has proposed that this pattern is that the genesis ofthe paired-eyevisual these events occurredfrom changes in neurulation that system plusbrain combination may result fromdi¡ erent involvedthe formationof transverse andlongitudinal regulatoryconstraints thanthe migratoryneural crest ^ neuralfolds rostral andlateral to the developingneural placodalsensory systems. plate.In the developingamphibian Xenopus,the rostral Anothernoteworthy observation is that noneuralcrest partof the neuralplate has been found to give rise to and/orplacodal-derived bipolar sensory neurons project majorportions of the diencephalon,including the neural toalar plate ¢ rst-ordermultipolar neurons that are retinas, andof the midbrainand hindbrain, while the predominantlylocated within the craniatediencephalon. transverse andlongitudinal neural folds give rise tothe Suchprojections to ¢ rst-ordermultipolar cell groupsexist telencephalichemispheres andalso contribute to some of atmost otherlevels of the neuraxis:telencephalon, hind- the alarparts ofmore caudalbrain regions ( Eagleson& brainand spinal cord. A possibleexplanation for this Harris 1990).AsN orthcutt (1996)discussed, the more situationis the priorestablishment ofvisual ¢ rst-order lateralparts ofthe neuralfolds and laterally adjoining multipolarneurons in the diencephalon(i.e. the retinal ectodermaltissue giverise toneural crest andplacodes. ganglioncells) asa populationthat is thus di¡erent from Thus,N orthcutt (1996)has postulated that the gainof allother sets of¢ rst-ordermultipolar neurons for the neuralfolds during the embryologicaldevelopment of the other,later-evolved sensory systems. Further,the central earliest craniateswould account for the gainof major projectionsof the visualmultipolar neurons could have parts ofthe craniatebrain in conjunction with the migra- established analar plate beachhead in the diencephalon toryneural crest andplacodal derivatives. andmesencephalon, which could be subsequently Alternatively,that the elaborationof migratory neural exploitedby the ascendingprojections from the neural crest andplacodes in craniates did not occur simulta- crest^placodalsensory systems. neouslywith the elaborationof the brainhas also been Theidea of such analar plate beachhead established suggested.Thomson ( 1988),forexample, speculated that bythe visualsystem hassome interesting implicationsfor pairedsensory organs and an enlarged forebrain evolved the evolutionof similarly organized, multisynaptic beforethe neuralcrest, dueto changes in signalling from sensorysystems incraniate brains. The visual system rostral mesodermal tissue. Aplausiblescenario that pathwaysthat wouldhave been established atthis junc- explainshow elaboration of the brainin the craniate ture wouldinvolve retinal projections to the diencephalon ancestralline occurred and that accountsfor the gainof andmesencephalon and relays from these sites tomore paired,lateral eyes andan expanded alar plate with caudal,motor-related andmotor neuronal groups of the multiple, ascending,sensory system pathways,has not, brainstem andspinal cord. As shown schematically in however,previously been o¡ ered. ¢gure2, such descendingpathways could form the A`serialtransformation hypothesis’ that expandson template forthe subsequentlyevolved ascending pathways Thomson’s(1988)idea and postulates that atleast partof ofthe other systems. Just asthe ¢rst-order multipolar the brainwas elaborated in the ancestralcraniate line neuronsof the visualsystem projectto the diencephalon beforemigratory neural crest andplacodes is proposed andmesencephalon, ascending projections from the here (andsee Butler 2000)to provide such ascenario. migratoryneural crest andplacodal systems coulddo Basedon the workof Eagleson & Harris (1990)and likewiseby using the same path¢nder system andthus Northcutt’s (1996)¢ ndingsand analysis, the rostral part participatein determining the descendingoutput to ofthe neuralplate of developing craniates would appear motorsystems. Thefact that the central pathwaysof re- togive rise tothe parts ofthe brainthat arehomologous evolvedand additionally evolved neural crest ^placodal tothe cerebralvesicle of lancelets. Asmentionedin ½ 4,a systemsösuch asthe occurrence ofthe electrosensory regionhomologous to the craniatehindbrain has been system insome teleost ¢shes andthe infraredsystem in identi¢ed caudal to the cerebralvesicle ( Holland& snakes,respectively öuse the same template lends credence

Phil. Trans.R. Soc.Lond. B (2000) 1312A.B.Butler Originof craniate brain

pallium

striatum

large large frontal paired diencephalon paired diencephalon eye eyes eyes

tectum tectum tectum

PMC PMC PMC ? ?

mNC/P sensory hindbrain sensory hindbrain sensory hindbrain cells cells systems

spinal cord spinal cord spinal cord

Figure2. Summary of theevolution of similarlyorganized central sensory pathways according to theserial transformatio n hypothesisproposed here. The conditionin extantlancelets (Lacalli 1996) is diagrammed on theleft, showing projections of the frontaleye to thetectal region and thence to motor-relatedregions of thebrainstem. The middlediagram shows the hypothesized intermediatecondition of transitionalcraniate ancestors with elaborationof thehindbrain, mesencephalon and diencephalon with pairedeyes. The alarplate beachhead in thediencephalon and mesencephalon allows the elaboration of thedescending visualpathways consistent with thecondition in lancelets.The diagramon theright shows the condition of the¢ rsttrue craniates with thesubsequent gain of thetelencephalic hemispheres and the elaboration of migratoryneural crest ^placodalsensory systems (Northcutt1996). The similarityof organization of these systems to thatof thevisual pathways is due to their exploitation of the samealar plate beachhead. mNC/ P,migratoryneural crest/ placodes;PMC, primarymotor centre. tothis idea.Theconcurrent gainof the telencephalichemi- resulted inthe infoldingof the neuralplate to produce a sphereswiththe originalneural crest ^placodalset ofsystems neuraltube butwithout the formationof neural folds. In wouldhave supplied an additionalrostral target forthese the actualancestral situation, embryological development sensorypathways that wasadded on to the existing withthis conditioncould have resulted inan elaborated diencephalic ^mesencephalic ^hindbraintemplate. hindbrain,midbrain and diencephalon with paired eyes. Thesignalling protein encoded by the genesonic Thelater gainof signi¢ cant horizontal ectodermal move- hedgehog, Shhöand/orits downstreame¡ ects östands ments wouldhave then allowedthe formationof the outas an excellent candidate for e¡ ecting the elaboration neuralfolds with their derivatives,de¢ ning the emergence ofthe pairedeyes andneural tube inthe ancestralline ofthe ¢rst true craniatetaxon. that ledto the ¢rst true craniates. Shh playsa rolein the dorsoventralspeci¢ cation of the neuraltube andin the The authorthanks Shaun Collin and Justin Marshall for their formationof paired lateral eyes asopposedto the default invitationto the First International Conference on Sensory Pro- cyclopeancondition (R ubenstein &Beachy1 998).The cessingof the Aquatic Environment and the valuable feedback fromthem and the other attendees of that meeting on themate- upregulatedexpression of an ancestral homologue of Shh rialin thispaper. The authorthanks Bill Hodosfor numerous inalancelet-likeancestral invertebrate could have caused collaborativediscussions on many aspects of craniate sensory the formationof lateral eyes andan elaborated dience- systemorganization and evolution, which contributedto some of phalonand mesencephalon. Shh expressione¡ ects include theideas expressed herein. She also thanks Bill Saidelfor his the activationof the proneuralgene achaete-scute , which veryhelpful comments on this manuscript and is grateful to participatesin signalling neurogenesis, as discussed by KellyCookson for producing ¢ gures1 and2. This workwas sup- portedby National Science F oundationgrant no. IBN 97281 55. Kerszberg &Changeux( 1998).Infact, a computer simu- lationof primary neurulation recently publishedby Kerszberg &Changeux( 1998)corresponds closely to the REFERENCES morphogeneticevents postulatedfor this ¢rst partof the Butler,A. B. 2000Chordate evolution and the origin of crani- serial transformation.This simulation had restricted ates:an old brain in anew head. Anat. Rec. (New Anat.) 261, epidermalcell movements inthe horizontalplane, which 111^125.

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