Albert Et Al (1999) Visual Thalamotelencephalic Pathways in the Sturgeon Acipenser, A Non-teleost...

8/11/2019 Albert Et Al (1999) Visual Thalamotelencephalic Pathways in the Sturgeon Acipenser, A Non-teleost Actinopterygian

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Original Paper

B rain, Beh aviorand Evolut ion Brain Behav Evol 1999;53:156-172

Visual Thalamotelencephalic Pathwaysin the Sturgeon Acipenser,a Non-Teleost Actinopterygian FishJames S. Albert 3 Naoyuki YamamotcrNobuhiko Sawai 8 Hironobu lto a 'b

Masami Yoshimoto 3

aDepartment of Anatomy and Laboratory for Comparative Neuromorphology, Nippon Medical School,Tokyo, Japan; b School of Fisheries and Ocean Sciences, University of Alaska, Fairbanks, Alaska, USA

Key WordsVisu al system Brain Thalamus TelencephalonFiber connections Evolution Ray-finned fish

AbstractTerrestrial vertebrates (amphibians, reptiles, birds, andmammals) possess two visual systems, the geniculateand extrageniculate pathways to the telencephalon. Incartilaginous fishes (e.g. sharks) both retinal and tectalneurons p roject to neurons in the thalamus, which them-selves project to a single area in the telencephalon. Thecondition in ray-finned fishes (Actinopterygii) is ambig-uous. In many teleosts there is a well developed extra-geniculate pathway but no obvious geniculate system.This study reports on the thalamotelencephalic projec-tions of a sturgeon, a non-teleost ray-finned fish. Sev-eral tract tracing methods (e.g., HRP, WGA-HRP, biocytin,BDA, Oil) were employed in conjunction with normal

techniques for identifying neural structures (e.g., Nissl,Golgi). After injections of tracer into retinal and tectalrecipient areas of the thalamus, labeled terminals wereobserved in the ventrolateral region of the caudal telen-cephalon, an area referred to as the thalamic projectionarea. After injections of tracer into the telencephalon,populations of retrogradely filled neurons were locatedin both the dorsal and ventral thalamus. These datademonstrate that thalamic neurons in both retinal and

tectal pathways project directly to the telencephalon.These results support the view that two visual pathwaysare a primitive feature of vertebrate brain organization.These results are also consistent with the hypothesis thatthe ancestor of Acipenser and Teleostei (Actinopteri)acquired a novel visual pathway to the telencephalonthrough the ventral portion of the thalamus.

Introduction

The visual system of vertebrates is composed of twoanatomically discrete systems, the geniculate and extra-geniculate pathways [Schneider, 1969; Hall and Ebner,1970; Karten and Hodos, 1970]. Both pathways have beenreported in all gnathostomes (jawed vertebrates) examinedin which the telencephalic hemispheres develop as evagina-tions from the lateral wall of the secondary prosencephalon

[Johnston, 1909; Northcutt, 1995]. In chondrichthyans (e.g.,sharks) retinal and tectal projection areas may overlap inthe dorsal thalamus [Ebbesson et al., 1972; Schroeder andEbbesson, 1974], or the two pathways may in fact be sepa-rate [Luiten, 1981]. In either case, neurons from both visualsystems project to a single area in the telencephalon. In ter-restrial vertebrates (i.e., tetrapods) the two pathways remainseparate through the thalamus and to their immediate targetsin the telencephalon [Schneider, 1969; Kicliter and North-

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James S. AlbertNippon Medical School, Department of Anatomy, Sendagi 1-1-5Bunkyo -ku, Tokyo 113-8602 (Japan)Tel. +81-3-3822-2131, ext. 5320, Fax +81-3-5685-6640E-Mail [email protected]


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Abb rev iat ions

A an te ri or n u c leu s of t he dor sa l th a la m us EA D T an te ri or port io n of d or sa l th ala m us H aBO bulb us olfactor ius HdCC corpus cerebel l i I fbCd preoptic cudg el LTCH opt ic chiasm OCDd telencephal ic area dorsal is pars dorsal is PA Dl te lenc epha l ic area dorsal is pars la teral is PDTDm telencep hal ic area dorsal is pars med ial is PTDp telenceph al ic area dorsal is pars poster ior is PThDT dorsal thalam us Ret

entopedunc ular nucleus TEhabenula TOdorsal hypo thala mu s tpalateral forebrain bun dle Vdlateral portion of the thala mu s VIopt ic chiasm Vppreoptic areaposterior portion of dorsal thalam us Vspituitary nucleus prethalamicus VTretina

te lencephalontectum opt icumthalam ic project ion area of te lencephalonte lencephal ic area ven tral is pars dorsal istelencephalic area ventralis pars lateralistelencephal ic area ventral is parspos tcommissura l i ste lencepha l ic area ventral is parssupuracommissura l i s ven tr al th ala m us

cutt, 1975; Neary and Northcutt, 1983; reviewed in Butler and Hodos, 1996].

The organization of thalamotelencephalic visual projections in actinopterygian (ray finned ) fishes, however, remainsambiguous. In these fishes, the telencephalon develops froman eversion of the alar pate [Gage, 1893; Johnston, 1911], and

identifying homologous elements with other vertebrates hasproven elusive [Nieuwenhuys, 1963; Nieuwenhuys and Meek,1990]. Projections from retinorecipient thalamic regions tothe telencephalon are known for several taxa [Northcutt,1981; Braford and Northcutt, 1983], yet a thorough knowledge of visual thalamic pathways is presently available only in several highly specialized teleost species [Ito et al., 1980;Ebbesson, 1980; Ito and Vanegas, 1983; Murakami et al.,1986; Ito et al., 1986; Striedter, 1990; Roony and Szabo,1991]. Among these species there has been no clear demonstration of a geniculate pathway. Indeed the data availablefrom several of these taxa indicate that most, if not all, visual

information to the telencephalon is mediated by the optic tectum before passing through the thalamus [Ito and Vanegas,1983; Murakami et al., 1986; Ito et al., 1986; Striedter, 1990].This pathway therefore resembles the extrageniculate systemof mammals. In these teleost species, little or no direct retinalinputs to the thalamus are transmitted to the telencephalon.

The position and connections of the visual thalamic nuclei are relatively conservative among non actinopterygianfishes and terrestrial vertebrates [Butler and Hodos, 1996].Although the ontogenetic eversion by which the telencephalon of actinopterygian fishes develops obscures the topog

raphy of these neural structures, the connections of theseneurons may be used as criteria to identify homologous elements. The visual system of teleost fishes possesses a number of high ly specialized nuclei and connections, so as torender comparison with other vertebrates ambiguous. As acontribution to understanding the organization and evolution of the forebrain in vertebrates, this study reports thethalamotelencephalic connections in the visual pathways of sturgeons, non teleost ray finned fishes.

Materials and Methods

For the study of the visual system a total of 34 sturgeon specimens were ex am in ed . These in clud e 16 ma ture spe cim ens (55 73 cm totallength) of Acipenser transmontanus [Richardson , 1836] acqu ired as

ju ve nil es fro m Fishpro Farms, Potochard, Wa sh ington , USA, andraised to maturity by Dr. Takeshi Furuta of the Central Research Institute of Electric Power Industry. An additional 18 juvenile specimens(14 19 cm total l ength ) of A. schrenkii [Brandt, 1869] were acquiredfrom commercial dealers. The original research reported herein wasperformed under the official Japanese regulations for research onanimals.

Cytoarchitecture and Nuclear OrganizationNuclear organization was determined from Nissl and Golgi Cox

preparations in conjunction with the results of tract tracing experiments. Sections sampled at each 50 ! along the neuraxis were tracedusing a Olympus microscope slide projection system. Nuclear boundaries and nomenclature were compiled from several sources, includingNorthcutt and Braford [1980], Reperant et al. [1982], Nieuwenhuysand Meek [1990], Rupp and Northcutt [1998], and Nieuwenhuys[1998]. Diencephalic organization follows Nie uwe nhu ys and Bodenheimer [1967], Rupp and Northcutt [1998], and Nieuwenhuys [1998] wi th the exc eption that the thalam us is divided on ly in to dorsa l, ventral, and lateral portions, based on the distributions of cells and labeledterminals.

Nissl Method. A specimen of A. transmontanus was anesthetized by immersi on in a tank contain ing MS222 at a rat io of 140 mg/li ter ,then perfused intracardially with 10% unbuffered formalin. The brain wa s removed fro m the cran ium, ev en ly tr im me d of cran ia l nerves,embedded in paraffin, sectioned frontally at 10 !, and stained with0.1%cresyl violet.

Golgi Cox Method. Two specimens of A. transmontanus wereanesthetized by immersion in MS222, and one of these specimens wasperfused intracardially as described above. Both brains were removedfrom the cranium, immersed in a Golgi Cox solution, and maintainedfor four weeks in darkness. After dehydration through a series if increasing concentrations of alcohol, brains were embedded in celloidin, sectioned frontally at 60 or 100 ! and reduced by immersionin 15% ammonium hydroxide. After washing in distilled water, sections were dehydrated, cleared in xylene, and mounted on slides. Insome cases, after reaction with ammonium hydroxide, sections werecounterstained with 0.025% cresyl violet. Tracings of individual cells were dra wn wi th the aid of an Ol ym pu s micro scope equipped wit h acamera lucida.

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Retrograde Tracer Labeling. After tracer injections into the thalamus or telencephalon, retrogradely labeled neurons of the source areaexhibited a 'Golgi like' staining, and were studied for cell morphology. Tracings of individual cells were drawn with the aid a cameralucida.

Fiber ConnectionsIn vivo Tracer Experiments. In different experiments, biocytin,

bio tinyl ated dextranamin e (BDA), horsera dish peroxidase (HRP). or wheat germ a gg lu ti ni n (WGA ) conjugated HRP was injected in to oneof several brain regions. Injections of biocytin or BDA confined to themedial portion of the ventral thalamus were made in three specimensof A. transmontanm and two specimens of A. schrenkii. Injectionsof biocytin or BDA confined to the posterior portion of the dorsalthalamus were made in one specimen of A. transmontanus and twospecimens of A. schrenkii. Injections of BDA, HRP, or WGA HRP were injected int o por tions of the tel encephal on in two specimens of A. transmontanus and six specimens of A. schrenkii.

Before surgery animals were anesthetized in MS222, and maintained in an ice water bath during surgery. The dorsal part of the cranium was removed with the aid of a dental drill and a glass micropipette containing a 30% solution of HRP (SIGMA, type VI) in

distilled water, a small (0.5 g) crystal of BDA, or 3 5% biocytin in0.05 M tris buffer (pH 7.4) driven by a micromanipulator was used todeliver a minute amount of tracer to a specific location of the brain[Graham and Karnovsky, 1966]. Tracers were inserted into the thalamus from the anterior dorsal aspect to avoid damaging the suprahabenular artery. A small cluster of HRP crystals was inserted with out current, and iontophoretic injections of biocytin were made with anegative current at 3 4 , 0.5 Hz for 20 min. Aspirated adipose tissuewas replaced after each injection with Terramycin (Pfizer) ophthalmicointment, and the cranial opening was sealed with a counterfeited capof dental cement affixed with an acrylic adhesive.

Animals were mainta ined pos toperatively in a tank at 20-22 C for7 days (A. schrenkii) or 10 days (A. transmontanus). after which ani-mals were deeply anesthetized with MS222, and then perfused intra-cardially with saline followed by a solution of 2% paraformaldehydeand 1% glutaraldehyde in 0.1 M phosphate buffer (pH 7.4). Brainswere removed from the skulls, embedded in egg yolk (A. trans-montanus). postfixed in the same fresh fixative at 4 C for 24 h, andthen stored in 0.1 M phosphate buffer (pH 7.4) containing 20% sucroseat 4 C for 24 h. Brains were then immersed in n-hexane at -50 C, andserial frontal sections were cut at 50 ! with a cryostat. Sections of

A. schrenkii were thaw mounted.In the case of HRP and WGA HRP injections, sections were

reacted with diam inobe nzidi ne (DAB) after protocol of Adams [1981].In the case of biocytin and BDA injections, sections were first treated with 0.3% H2O2 sol ution in 0.05 M phosphate buffered saline (pH 7.4)for 20 min for blocking of remaining blood and non specifi c reactions,incubated in a solution of avidin biotin HRP complex (Vector), andreacted with DAB after the protocol of King et al. [1989]. Sections wh ic h reac ted wi th DAB wer e mounted on slides with 1% gela tin in water, dried over nigh t at room temperature, and counterstained wi th0.025% cresyl violet.

Carbocyanine Dye (Dil) Experiments. Following deep anesthesia with MS222 two spe cim ens of A. transmontanus and one specimen of A. schrenkii were perfused through the heart with 4% paraformaldehyde in 0.1 M phosph ate buffe r (pH 7.4) follow ing 0.9% saline. The br ai ns were removed from the skul l and f ixed in the same f res h fixativefor 2 days. After postfixation, a small crystal of carbocyanine dye

[God ementeta l., 1987] was inserted into the ventral thalamu s near the ventricular margin at the level of the ros tral marg in of the pos terior commissure in one specimen of A. transmontanus, and into the posterior portion of the dorsal thalamus immediately ventral to the fasciculus retroflexus at the level of the rostral margin of the posterior commissure in a specimen of A. schrenkii.

The insertion sites were covered with several layers of 5% gelatin,and stored in fixative at 37 C in darkness for 9 weeks. The brains were

then sectioned frontally with a Microslicer (D.S.K., DTK 3000) at50 !. Sections were mounted on slides with 50% sucrose in 0.1 M phosphate buffer (pH 7.4). observed, and photographed using anOly mpu s Vanox microscope (AHBS) equipped with epi fluorescenceil lu mi na ti on system (AH2 REL) at a wavelength of 546 nm. Sections

were then Nis sl sta ined and reexamined to de term ine the exact locations of labeled terminals.

Results

There are four recognized genera and 25 species of

extant sturgeons [Acipenseridae; Grande and Bemis, 1996],several of which have been subjected to neuromorphological study. Figure 1 depicts a dorsal view of the brain of thesturgeon Acipenser transmontanus. The general organization of cell groups and fiber tracts in the forebrain of Aci

penser is reported in Johnston [1901], Rupp and Northcutt[1998], and Nieuwenhuys [1998]. The results reported hereare primarily derived from studies on adult specimens of

Acipenser transmontanus. Additional experiments wereundertaken using another sturgeon species, A. schrenkii, totest the generality of the results within the genus Acipenser.Due to limited specimen availability, only juveniles of

A. schrenkii were examined. Qualitative data on the connectivity and organization of the visual pathways obtainedfrom experiments on these two species are similar, and theresults are reported together. Several minor differences wereobserved in the distributions of labeled terminals and cells, which are inferred to be a consequence the size diffe rence between the two experimental groups.

Cell ConfigurationsSix types of thalamic neurons were identified based on

morphological criter ia (fig. 2). Throughout the th alamu s

most dendrites, especially those of the more distal ramules,are oriented perpendicular to the ventricular margin. Multipolar horizontal cells have a spherical or ovoid cell body of 7 15 ! diameter along the long axis, and 2 or sometimes3 primary dendrites possessing few to numerous spines(fig. 2A). These dendrites give the multipo lar horizontalcells a '


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Fig. 1. Dorsal v iew of the brain of thesturgeon Acipenser transmontanus, showingtransverse levels of sections in figures 4 (top)and 6 (bottom). Rostral to left. Abbreviationsin list. Scale bar = 2 mm.

(fig. 2B). Although these primary dendrites may extend inany direction, secondary and more distal dendrites tend tobe horizontal . Unipolar cells possess a spherical or teardropshaped cell body of 7 20 diameter and a single horizontal dendrite (fig. 2C, 2D). The single dendrite of unipolar cells may emerge from either the medial or lateral surfaceof the cell body. Bipolar vertical cells have a spherical or ovoid cell body of 10 20 ! diameter and 2 primary dendrites extending dorsally and ventrally respectively (fig. 2E).Bipolar hoizontal cells are the largest thalamic neurons,with an ovoid cell body of 10 40 ! diameter and 2 primary dendrites extending medially and laterally respec

tively (fig. 2F).Most of the dendrites observed in the telencephalic area

ventralis pars lateralis are oriented ven tro laterally, many extending in the underlying thalamic projection area (fig. 3A).The axon of these neurons was commonly emerges from thedorsomedial face of the soma. Additional dendrites in thisregion are oriented dorsolaterally, paralleling the ventricular margin. Most dendrites in the thalamic projection area arealso oriented ventrolaterally, and the position of the axon isvariable (fig. 3B). Some dendri tes were also observed oriented dorsomedially. Cells in telencephalic area dorsalispars posterioris are arranged in 47 layers, with more layersin the middle, thicker portion of the structure.

There is no ventricular recess rostral to the optic chiasm.The preoptic area is composed of cells in the walls of thethird ventricle, bounded rostrally by the anterior commissure, dorsally by the telencephalon and ventral thalamus,and ventrally by the optic chiasm. There is a population of small round cells in the ventral portion of the preoptic area,wh ich may be homologous with the parvocellular compo

nent of the preoptic area of other ray finned fishes. Cells inthe ventral portion of the preoptic area are small (42.9 11.33 m2, mean SD, n = 20), round or slightly ovoid, andare arranged in 5 6 layers aligned with the ventricular margin. Many cells in the dorsal portion of the preoptic area arelarger (71.2 10.1 m2, n = 20), ovoid, and not arranged inlayers; these cells may correspond with magnocellular component of the preoptic nucleus of other ray finned fishes.These two cell populations are not segregated into distinctnuclei.

Fiber Connections

Thalamotelencephalic Projections. Injection sites intothe thalamus were determined from the position of terminalfields from the retina and tectum [Ito et al., 1999; Yamamotoet al., 1999]. Retinal and tectal terminal fields are located inmost portions of the thalamus, and are most dense in the ven tromedia l, ven tro latera l, and dorsomedial portions of thethalamus.

Af te r injections of tracers (HRP, biocytin , or Dil) confined to the medial portions of either the dorsal or ventralthalamus, labeled fibers and terminals were observed in several telencephalic areas (fig. 4J A, 5A, 7F). The most dense bundle of labeled fibers emerging from thalamic injectionsites courses rostrodorsally within the medial forebrain bundle [ascending tractus striohypothalamicus of Johnston,1901; fasciculus telencephali of Nieuwenhuys, 1963].Numerous fibers were observed along the ventricular margin of the diencephalon, terminating ipsilaterally in the thalamic eminence and preoptic area at levels correspondingto the optic chiasm, and in the preoptic cudgel. Very fewlabeled terminals were observed in the contralateral preoptic

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Fig. 2. Camera lucida tracings of representative cells in the thalamus of Acipenser transmontanus. Drawn from Golgi-Cox preparations. A Multipolar horizontal cells. B Multipolar non-oriented cells. C Unipolar cells with single lateraldendrite. D Unipolar cells with single medial dendrite. E Bipolar vertical cells. F Bipolar horizontal cells. Dorsal to thetop, lateral to the left. Note most dendrites, especially distal ramules, are oriented horizontally. Scale = 0.1 mm.

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Fig. 3. Camera lucida tracings of representative cells in the ventral telencephalon ofAcipenser transmontanus. Drawnfrom Golgi-Cox preparations. Note that most dendrites from cells in VI are oriented perpendicularly to the ventricle, ter-minating in the thalamic projection area of the telencephalon. Dorsal to the top, lateral to the left. Note also the positionof axons (arrows) which traverse dorsomedially from the cell bodies. Scale bar = 0.1 mm.

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area and labeled terminals were not observed in the con-tralateral thalamic eminence.

The majority of fibers labeled from these injections con-tinue ipsilaterally within the medial forebrain bundle intothe caudoventral portion of the telencephalon (fig. 4, 7F).These fibers are not fasciculated and are interspersed withnumerous small, round and ovoid cells. This region isreferred to here as the thalamic projection area of the tel-encephalon (tpa). Some thalamotelencephalic terminals arelocated in the cell-rich areas close to the ventricular margin(i.e., VI, Vp, Vs, Vv), and in the caudal and ventral portionsof telencephalic area dorsalis pars posterioris (i.e., Dp).Thalamotelencephalic terminals are distributed from thelevel of the entopeduncular nucleus rostrally to the level of the telencephalic area ventralis (fig. 4A-D).

The thalamic projection area of the telencephalon may bedivided into three layers; a deep (ventrolateral) layer com-posed mainly of fibers lying immediately medial to the lat-

eral forebrain bundle, a central layer composed of fibers,terminals, and some retrogradely filled cells, and a superfi-cial (dorsomedial) layer composed primarily of cells andlabeled terminals, lying ventral and lateral to the periven-tricular telencephalic parts. The terminal-rich layer consti-tutes the medial four fifths of the thalamic projection area,and invades the lateral and posterior parts of the area ven-tralis.

Most thalamotelencephalic projections are bilateral, thedensity of ipsilateral terminals being much heavier thancontralateral terminals. Ipsilateral projections also extendfurther rostrally and dorsally. The rostral-most labeled ter-minals were observed ipsilaterally, rostral to the anteriorcommissure. At the level of the anterior commissure thala-motelencephalic terminals are concentrated in the thalamicprojection area immediately lateral to the supracommissuraland lateral parts of area ventralis, and also within the supra-commissural part itself (fig. 4B). At this level thalamotelen-cephalic terminals are more sparsely distributed than in therest of the thalamic projection area, being relatively moredense lateral to area ventralis and even more sparse lateralto area dorsalis. Thalamotelencephalic fibers are of variouscaliber and the terminals are fine and beaded (fig. 5A).

There are three populations of neurons in the thalamusthat were retrogradely labeled after injections of either HRP,WGA-HRP, or BDA into portions of the telencephalon. Onepopulation of labeled neurons was observed in a looselyorganized column located in the lateral portion of the thal-amus, immediately medial to the lateral forebrain bundle(fig. 5B; 7E). In the rostral portion of the thalamus thesecells are located mainly in the lateral portion the ventralthalamus, and in the posterior portion of the thalamus these

cells are located in the lateral portions of both the dorsal andventral thalamus. These cells vary in size and shape, rangingfrom fusiform to ovoid in appearance, and bear dendrites of many orientations. After injections of HRP into the caudal-most portion of Dp, at the level of the rostral margin of theoptic chiasm (fig. 6A), faintly labeled cells were observed inthe lateral portions of the thalamus, at levels extending fromthe rostral margin of the habenula to the posterior commis-sure (fig. 5B, 6D, E). After injections of WGA-HRP into therostral portion of Dp, at the level of the anterior commissure(fig. 7C), faintly labeled cells were also observed in the lat-eral portions of the thalamus, at levels from the subcommis-sural organ to the rostral margin of the pretectum (fig. 7E).After heavy injections of either HRP or BDA into the telen-cephalon, including the thalamic projection area, a fewfaintly labeled cells were observed in the lateral portion of the thalamus.

A second population of retrogradely labeled neurons is

located in the medial portion of the ventral thalamus. Thesecells were strongly labeled after injections into the caudalportion of Dp (fig. 6C) and after injections into several ros-trocaudal levels of the thalamic projection area. These cellswere faintly labeled after injections into the rostral portionof Dp (fig. 7D). Labeled cells in the rostral portion of ven-tral thalamus are fusiform in shape and possess dendritesoriented in parallel with the ventricular margin. Labeledcells in the caudal portion of the ventral thalamus are ovoidin shape, and possess dendrites of many orientations.

A third population of retrogradely labeled neurons wasobserved in two or three rows lying along the ventricular

margin of the dorsal thalamus (fig. 7B). These cells werestrongly labeled after injections into the thalamic projectionarea, and not labeled at all by injections restricted to eitherthe rostral or caudal portions of Dp. These cells are large,either spherical or ovoid in shape, and their dendrites areoriented perpendicular to the ventricular margin. Some of these dendrites extend to almost the lateral surface of thethalamus. Retrogradely labeled cells were not observed out-side the telencephalon after injections into telencephalicarea dorsalis rostral to the anterior commissure.

Fig. 4. Diagrams of frontal sections through the forebrain of Aci- penser transmontanus following injection of HRP into the ventralthalamus. Injection site indicated by black area in panel J. Antero-gradely labeled fibers (dashed lines) and terminals (dots), and retro-gradely labeled cell bodies (solid circles). Projections are bilateral (asshown) and nuclear boundaries are omitted for clarity. Levels A-Jarranged rostrocaudally (see fig. 1). Dorsal to the top. Abbreviations inlist. Scale bar = 1 mm.

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Fig. 5. Photomicrographs of frontal sections through the forebrain of Acipenser transmontanus. A Anterogradely labeledfibers and terminals (arrows) in the caudal region of the thalamic projection area of the telencephalon after injection of biocytin into the medial portion of the ventral thalamus. B Retrogradely filled neurons in the lateral portion of the thalamusafter injection of HRP into the caudal telencephalon. C Retrogradely filled neurons in the medial portion of the ventral thalamus after injection of HRP into the caudal telencephalon. D Labeled terminals in the lateral portion of the ventral thalamus after injection of HRP into the caudal telencephalon. Ifb = Lateral forebrain bundle. E Retrogradely filled neurons inthe thalamic projection area of the telencephalon after injection of biocytin into the thal amus. Dorsal to top, lateral to rightin all panels. Scale bar in panel A = 20 . applies also to panels B. C, and E: scale bar in panel D = 50 .

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Fig. 6. Diagrams of frontal sections through the forebrain of Acipenser transmontanus following HRP injection totelencephalic area dorsalis pars posterioris (Dp). Injection site indicated by black area in panel A. Anterogradely labeledfibers (dashed lines) and terminals (dots), and retrogradely labeled cell bodies (solid circles). Nuclear boundaries omit-ted for clarity. Levels A-E arranged rostrocaudally. Dorsal to the top. Abbreviations in list. Scale bar = 1 mm.

Telencephalothalamic Projections. After injections intovarious portions of the dorsal and ventral telencephalonlabeled fibers were observed along the entire extent of thethalamotelencephalic fiber tracts. After injections into thecaudal portion of Dp, labeled fibers were observed coursingalong the lateral surface of the caudal telencephalon anddiencephalon, and labeled terminals were observed in theeminentia thalami, the preoptic area, the dorsal and ventral

thalamus, and the hypothalamus. The density of these termi-nals decreases with distance from the injection site. Afterinjections into dorsal portion of the telencephalon at thelevel of the anterior commissure, labeled fibers were ob-served coursing in the medial forebrain bundle, and net-works of fine-beaded terminals were observed in the lateraland medial portions of both the dorsal and ventral thalamus,and in the lateral portions of the thalamus.


Pathways

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Fig. 7. Photomicrographs of frontal sections through the forebrain of Acipenser schrenkii. A Location of HRP injection (dense black area) into the telencephalon posterior to the anterior commissure. Note the injection site includes boththe area dorsalis posterioris and the thalamic projection area (separated by dotted line). B Retrogradely filled neurons(arrows) and dendrites (arrow heads) in the medial portion of the dorsal thalamus, after injection depicted in panel A. CLocation of HRP injection into the telencephalon, at the level of the anterior commissure. Note injection site is restrictedto the Dp (dotted line as in A). D Retrogradely fi lled neurons (arrows) in the medial portion of the ventral thalamus after the injection depicted in panel C. Scale as in B. E Retrogradely filled neurons (arrows) in the lateral portion of the dorsal thalamus after the injection depicted in panel C. Scale as in B. F Fluorescing (labeled) fibers and terminals in thalamicprojection area of the telencephalon after injection of Dil into the posterior portion of the dorsal thalamus. Scale bars =300 ! in panels A and C, 25 ! in panel B (applies also to panels D and E), and 10 ! in panel F. Dorsal to top in allpanels; lateral to left in panels B, D, E, and F.

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After injections of WGA-HRP into either the ventralthalamus or dorsal thalamus, retrogradely filled neuronswere observed in several regions of the telencephalon (e.g.,fig. 4). The majority of these cells are located in the tha-lamic projection area of the telencephalon. Cells were alsoobserved in several periventricular parts of telencephalicarea ventralis, extending from the posterior margin of thetelencephalon to the rostral margin of the anterior commis-sure. Based on their cytoarchitecture and position these cellsappear to represent two distinct populations (fig. 3). Labeledneurons in the medial, cell-rich portion of telencephalic areaventralis possess dendrites oriented parallel to the ventricu-lar margin. Labeled neurons in the lateral, cell-poor regionsof the ventral telencephalon (i.e., the telencephalic projec-tion area) possess dendrites oriented parallel to the ventricu-lar margin (e.g., fig. 5E).

After injections of biocytin into the ventral thalamus afewer number of retrogradely filled cells were labeled in the

medial portion of thalamic projections area rostral to theanterior commissure, and in the lateral parts of area ven-tralis, at the level of the anterior commissure. After Dilinjections into the dorsal thalamus a few labeled cells werelocated in a dorsolateral region of the telencephalic projec-tion area, adjacent to area dorsalis pars centralis, at the levelof the caudal margin of the anterior commissure. Labeledcells were not observed in other portions of area dorsalis, orin the 'dorsal-most' part of area ventralis.

Other Thalamic Connections. In addition to the thalamo-telencephalic projection, many other fibers were labeledafter injections into portions of the thalamus. These includefibers of the optic tract which retrogradely labeled the opticnerve, and fibers of the tractus bulbolobaris, which termi-nate bilaterally in the anterior pole of the hypothalamus.After injections of tracers confined to portions of the thala-mus retrogradely labeled cell bodies were observed in theipsilateral and contralateral preoptic areas, and in the preop-tic cudgel. A sparse field of retrogradely filled cells was alsoobserved in the torus lateralis and posterior tuberculum.

After injection of different tracers to the ventral thala-mus, approximately 20% of ascending fibers cross in thepostoptic decussation and then continue caudally to the

contralateral thalamus and pretectum. In this region numer-ous labeled terminals and small retrogradely filled neuronswere observed in the periventricular region dorsal to the fas-ciculus retroflexus at levels immediately caudal to the pos-terior commissure, within an area occupied by the large neu-rons of the nucleus of the medial longitudinal fasciculus. Acomplete description of thalamic interconnections with theoptic tectum are reported elsewhere [Yamamoto et al.,1999].

In these experiments, projections to the posterior hypo-thalamus and inferior lobes coursed through the rostral por-tion of the commissure ansulata, at the level of the nucleusof the medial longitudinal fasciculus. Several smaller tractswere also observed emanating from thalamic injection sites,including relatively sparse periventricular tracts to theposterior tuberculum and hypothalamus. Labeled fibers andterminals were observed in a layer traversing the medialportion of the ventral hypothalamus, immediately lateral tothe periventricular cell layer. After injection to the dorsalthalamus only the dorsal portion of the hypothalamus waslabeled, in addition to fibers in the tecto-lobar tract whichcourse along the lateral surface of the hypothalamus. Sev-eral retrogradely labeled cells were observed in the medialportion of the ventral thalamus ipsilateral to the injectionsite.

Discussion

Visual Pathways in Acipenser The connectional data in Acipenser indicate the presence

of both geniculate and extrageniculate visual pathways tothe telencephalon (fig. 8). The pathway from the retinathrough the thalamus directly to the telencephalon resem-bles the geniculate system of other vertebrates [Schneider,1969; Ebbesson et al., 1972; Ito, 1986]. The pathway fromthe retina to the optic tectum to the thalamus to the telen-cephalon, resembles the extrageniculate system of other ver-tebrates [Ito et al., 1980; Ebbesson, 1980; Ito and Vanegas,1983, 1984; Vanegas and Ito, 1983]. In both of these path-ways fibers from the retina and optic tectum terminate inthe area of dendritic fields of neurons in the lateral portionof the thalamus (fig. 2). Cells in these areas project directlyto areas of dendritic fields of neurons in the ventrolateralportion of the telencephalon, the thalamic projection area(fig. 3).

Retinal and tectal projection areas in the thalamus of Acipenser exhibit considerable overlap. Retinal projectionsare concentrated rostrally and tectal projections caudally,yet both project at least some fibers to most portions of the

thalamus [Ito et al., 1999; Yamamoto et al., 1999]. Retinalterminals are most dense in the rostral portion of the con-tralateral ventral thalamus, in transverse sections from themiddle of the habenula to the rostral margin of the posteriorcommissure. Tectal terminals are most dense ipsilaterally,in the caudal portion of the dorsal and ventral thalamus, atabout the level of the posterior margin of the posterior com-missure [Yamamoto et al., 1999]. From the available data itis not possible to determine if retinal and tectal terminals in

Sturgeon Thalamotelencephalic V isual

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Fig. 8. Schematic diagram of visual thala-motelencephalic pathways in the sturgeon

Acipenser. Heavy lines indicate retinal projections, dashed line indicates a sparse oruncertain projection. Note that there are threepopulations of thalamic neurons (DT, VT, LT)which receive direct retinal and tectal affer-ents, and which project to the telencephalon.Note also that DT projects only to the thala-mic projection area (tpa), whereas the twoother groups of thalamic cells also project totelencephalic area dorsalis posterioris (Dp).Other abbreviations in list.

the same region of the thalamus synapse on different pop-ulations of neurons. Examination of cell shapes and sizesfrom Golgi preparations and the Golgi-like staining of retro-gradely-filled cells in the tract tracing experiments does notsuggest neuronal specificity for retinal or tectal projections.

The position of the thalamic projection area in Acipenser differs from the main visual recipient area of the telen-cephalon in teleosts, the area dorsalis pars lateralis (Dl).Unlike teleosts, thalamotelencephalic terminals in Acipen-ser are located primarily in the ventral portions of the telen-cephalon, in the thalamic projection area and in area ven-tralis pars lateralis (VI). The configuration of cells in theseregions, however, indicates they receive terminals fromascending thalamotelencephalic projections (fig. 3). Thala-

motelencephalic projections in Polypterus are also reportedto be concentrated in the ventral part of the telencephalon[Northcutt, 1981].

The position of the thalamotelencephalic projection areain Acipenser is similar to the region of olfactory projections

in another sturgeon, Scaphyrinchus platorhynchus [North-cutt and Braford, 1980]. After severing the olfactory tract,degenerating terminals were observed in the area dorsalispars posterior, all divisions of area ventralis except the ven-tral division, and a region equivalent with the medial portionof the thalamic projection area of the present study. Manybipolar and multipolar neurons in the periventricular partsof area ventralis and the pars posterioris of area dorsalisextend ventrolateral dendrites into the thalamic projection

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area, and may therefore participate in multimodal sensoryprocessing.

Comparisons with Other VertebratesThe overlap of retinal and tectal terminal areas in the

thalamus of Acipenser resembles the condition observed insome chondrichthyans [Ebbesson et al., 1972] and amphib-ians [Kicliter and Northcutt, 1975], and may represent theprimitive gnathostome condition. The general pattern is arostrocaudal arrangement of retinal and tectal projectionswithin the diencephalon, in which retinal terminals areconcentrated rostrally and tectal terminals caudally [Butlerand Hodos, 1996]. Because the retinal and tectal pathwaysthrough the thalamus are not entirely discrete, the data areambiguous with respect to the precise homology of the tha-lamic subdivisions. After injections in the telencephalon thecaudal-most group of retrogradely labeled neurons werelocated in the lateral part of the dorsal thalamus. With regard

to position therefore, these cells resemble the dorsoposteriorthalamic nucleus of other vertebrates [LP/pulvinar of mam-mals; Northcutt, 1995]. Yet the lateral portion of the thala-mus also receives retinal and tectal projections, in whichregards it more closely resembles the anterior nucleus of thedorsal thalamus of other vertebrates.

Other aspects of retinal and tectal projections in Aci-penser are not observed in other plesiomorphic vertebratetaxa, and may be uniquely derived features. Retinal projec-tions to the dorsal thalamus in Acipenser are not restrictedto the rostral portion, the region presumably correspondingwith the anterior nucleus of Braford and Northcutt [1983].The rostral portion of the dorsal thalamus further differsfrom other vertebrates in receiving direct tectal inputs[Yamamoto et al., 1999]. In addition, the retina projects tocells in the posterior and lateral portions of the dorsal thala-mus. Neither of these cell groups are known to receive reti-nal inputs in other ray-finned fishes [Northcutt and Butler,1980; Northcutt and Braford, 1984; Striedter and Northcutt,1989; Northcutt, 1995; Ito and Yoshimoto, 1990; Ito et al.,1997].

Thalamotelencephalic connections in actinopterygianshave been reported in a cladistian [Northcutt, 1981], a stur-

geon (this report), and representatives of four teleost groups[reviewed in Braford, 1995]. Data available from these taxaindicate that most, if not all, visual information to the telen-cephalon is extrageniculate, first passing through the optictectum and then the thalamus. A complete description of visual thalamic pathways is, however, presently availablefor a handful of highly specialized species [Ito et al., 1980;Ebbesson, 1980; Ito and Vanegas, 1983, 1984; Murakami etal., 1986; Ito et al., 1986; Striedter, 1990; Roony and Szabo,

1991]. The identity of the geniculate-like thalamic structure,the anterior nucleus of the dorsal thalamus, is uncertain inthese species because it does not always receive direct reti-nal input [Murakami et al., 1986], and does not always pro-

ject to telencephalic areas [Striedter, 1990].The connections and organization of the visual pathways

in the sturgeon Acipenser differ from those of teleosteanfishes for which sufficient data on retinal, tectal and tha-lamotelencephalic projections are available. In euteleosteanfishes only fibers from tectorecipient thalamic neurons havebeen confirmed to project directly to the telencephalon. Inthe catfish Ictalurus, an ostariophysan teleost, the retina pro-

jects to the rostral portion of the ventral thalamus and tel-encephalic efferents arise only from the caudal portion of that nucleus [Striedter, 1990]. In this species the retinorecip-ient anterior nucleus does not project to the telencephalon.The extrageniculate pathway is also indirect in Ictalurus.Although the tectum projects primarily to the dorsal poste-

rior nucleus, it is the central posterior nucleus that projectsto the telencephalon.Evidence for a geniculate pathway is also ambiguous in

another ostariophysan, the common carp Cyprinus carpio.Ito and Kishida [ 1978] document the main visual pathwaysin this species, but despite large injections of tracer into thetelencephalon they were unable to label neurons in eitherthe dorsal or ventral portions of the thalamus. A single pop-ulation of diencephalotelencephalic cells was observed, inthe preglomerular nucleus, an area which does not receiveretinal or tectal projections. They concluded that visualinformation may not reach the telencephalon. Echteler andSaidel [1981] report projections to the dorsal telencephalonfrom the anterior portion of the dorsal thalamus (nucleus A)in the closely related species, Carassius auratus. Striedter[1990] demonstrated retinal input to an equivalent cellgroup in the catfish Ictalurus, but neither he nor otherreports in teleosts [e.g., Ito and Kishida, 1978; Echteler,1984; Wullimann and Meyer, 1993] report projections fromnucleus A to the telencephalon. The situation with nucleusA is therefore not entirely clear, but the bulk of the evidencesuggests it does not relay retinal input to the telencephalonin these species.

In the several species of spiny-ray (acanthopterygian)teleosts for which extensive connectional data are available,most if not all visual information is mediated by the optictectum and a rostroventrally positioned thalamic nucleus,the nucleus prethalamicus of Meader [1934] [Ito et al.,1980; Ebbesson, 1980; Ito et al., 1986; Ito and Vanegas,1983, 1984; Murakami et al., 1986]. Like the lateral poste-rior nucleus or pulvinar of mammals, the nucleus pretha-lamicus is reciprocally connected with different parts of the


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Fig. 9. Cladogram of actinopterygian taxawith data on visual pathways to the telen-cephalon. Data for terminal taxa compiledfrom one or more species (see text for refer-ences). The plesiomorphic condition assumesa geniculate pathway through the anteriordorsal thalamus (ADT), and an extragenicu-late pathway through the posterior dorsal thal-amus (PDT); other abbreviations in list. '+'indicates evolutionary gain, '-' evolutionaryloss (or substantial reduction), '>' efferentprojection, '


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netic generality of this transformation is ambiguous dueto the reported absence of projections from the ventralthalamus to the telencephalon in osteoglossomorph fishes[Braford, 1995]. The origin of the visual thalamotelen-cephalic pathway through the ventral part of the thalamus isoptimized as a shared character of Acipenser and othermembers of Actinopteri using the Accelerated Transforma-tion (ACCTRAN) model of character-state change. Theindependent gain of this pathway in Acipenser and euteleostfishes is an equally parsimonious alternative.

There are two simple ontogenetic mechanisms whichmay have resulted in the origin of a pathway through theventral part of the thalamus. One mechanism posits changesin the connections of neurons and conservation of theirposition to explain the observed distribution of characters.Under this view, the thalamotelencephalic neurons in theventral thalamus of Acipenser are homologous with cells inthe Ventral Thalamus (sensu stricto) of non-actinopterygian

gnathostomes. An alternative mechanism posits changes inposition and conservation of connections. This model sup-poses that the visual cells in the ventral portion of the thal-amus of sturgeons and teleosts are homologous with cells inthe dorsal thalamus of other gnathostomes. The secondhypothesis would also result from a change in the positionof the architectonic landmarks used to recognize the bound-aries between the dorsal and ventral thalamus. Under either

of these scenarios, the nucleus prethalamicus of acantho-pterygian teleosts is regarded as part of the 'ventral thala-mus' of other actinopterygian fishes.

A third logical possibility is that the several thalamo-telencephalic nuclei observed in ray-finned fishes are nothomologous with one another, or with structures in othervertebrates, beyond their more general commonality as tha-lamic neurons. Visual pathways through other parts of thebrain are known to differ substantially between percomorphand ostariophysan teleosts and this presumably reflects theirvastly different histories [Ito et al., 1986; Striedter andNorthcutt, 1989]. In this context it should be noted that thecommon ancestor of actinopterygian fishes lived in theDevonian Period, almost 400 mya, approximately the timeof the origin of terrestrial vertebrates. A greater sampling of visual pathways in actinopterygian taxa is required to testthese alternative hypotheses.

Acknowledgments

Dr. Takeshi Furuta of the Central Research Institute of ElectricPower Industry kindly made the adult specimens of A. transmontanusavailable for this study. Dr. Chikako Shingyoji, Graduate School of Sciences, Tokyo University, provided helpful information. We thankMiss Kyoko Fukushima for technical assistance.

References

Adams, J.C. (198 1) Heavy metal intensification of DAB-based reaction product. J. Histochem.Cytochem., 29 : 775.

Bergquist, H. (1932) Zur Morphologie des Zwi-schenhirns hei niederen Wirbeltieren. ActaZoologica, 13: 57-304.

Braford, M.R., Jr. (1995) Comparative aspects of forebrain organization in the ray-finned fishes:Touchstones or not? Brain Behav. Evol., 46:259-274.

Braford, M.R., Jr., and R.G. Northcutt (1983) Or-ganization of the diencephalon and pretectumof the ray-finned fishes. In Fish Neurobiology,Vol., 2 (ed. by R.E. Davis and R.G. Northcutt),University of Michigan Press, Ann Arbor,pp. 117-164.

Brandt, J.F. (1869) Acipenser schrenkii. MelangesBiol.v., 7: 115.Butler, A.B., and W. Hodos (1996) Comparative

Vertebrate Neuroanatomy, Wiley-Liss, NewYork.

Ebbesson, S.O.E. (1980) A visual thalamo-telen-cephalic pathway in a teleost fish (Holocentrusrufus). Cell Tissue Res., 213: 505-508.

Ebbesson, S.O.E., J.A. Jane, and D.M. Schroeder(1972) A general overview of major interspe-cific variations in thalamic organizat ion. BrainBehav. Evol., 6: 92-130.

Echteler, S.M., and W.M. Saidel (1981) Forebrainconnections in the goldfish support telence-phalic homologies with land vertebrates. Sci-ence, 272: 683-685.

Echteler, S.M. (1984) Connections of the auditorymidbrain in a teleost fish, Cyprinus carpio.J. Comp. Neurol., 230: 536-551.

Gage, S.P. (1893) The brain of Diemyctilus viri-descens from larval to adult life and compar-isons with the brain ofAmia and Petromyzon. InThe Wilder Quarter Century Book, Ithaca N. Y.,pp. 259-314.

Godement, P., J. Vanselow, S. Thanos, and F. Bon-hoeffer (1987) A study in developing visualsystems with a new method of sta ini ng neuronsand their processes in fixed tissue. Develop-

ment, 101: 171.Graham, R.C., and M.J. Karnovsky (1966) Theearly stages of absorption of injected horserad-ish peroxidase in the proximal tubules of mousekidney: Ultrastructural cytochemistry by a newtechnique. J. Histochem., 14: 291-295.

Grande, L., and W.E. Bemis (1996) Interrelation-ships of Acipenseriformes. In Interrelation-ships of Fishes (ed. by M. Stiassney, L.R.Parenti, and G. David Johnson), AcademicPress, New York, pp. 85-115.

Hall, W.C., and F.F. Ebner (1970) Thalamotelen-cephalic projections in the turtle (P.seudomysscripta) and the hedgehog (Paraechinushypomelas). J. Comp. Neurol, 140: 101-122.

Ito, H. (1986) Multiplicity of sensory pathwaysfrom a phylogenetic perspective, with a focuson the visual system (in Japanese). Brain andNerve, 38(9): 845-852.

Ito, H., and R. Kishida (1978) Afferent and efferentfiber connections of the carp torus longitudi-nalis. J. Comp. Neurol., 181: 46576.

Ito, H., and H. Vanegas (1983) Cytoarchitectureand ultrastructure of nucleus prethalamicus,with special reference to degeneratin g afferentsfrom optic tectum and telencephalon, in ateleost (Holocentrus ascensionis). J. Comp.

Neurol., 227: 401-415.Ito, H., and H. Vanegas (1984) Visual receptivethalamopetal neurons in the optic tectum inteleosts, Holocentridae. Brain Res., 290: 201-210.

Ito, H., and M. Yoshimoto (1990) Cytoarchitectureand fiber connections of the nucleus lateralisvalvulae in the carp (Cyprinus carpio). J.Comp. Neurol., 298: 1-15.


Pathways

Brain Behav Evol 1999:53:156-172 171


17/17

Ito, H., A.B. Butler, and S.O.E. Ebbesson (1980)An ultrastructural study of the normal synapticorganization of the optic tectum and the degen-erating tectal afferents from retina, telen-cephalon, and contralateral tectum in a teleost Holocentrus rufus. J. Comp. Neurol., 191:639-659.

Ito, H., Y. Morita, N. Sakamoto, and S. Ueda (1980)Possibility of telencephalic visual projectionsin teleosts, Holocentridae. Brain Res.. 197:219-222.

Ito, H., T. Murakami, T.K. Fukuoka, and R. Kishida(1986) Thalamic fiber connections in a teleost(Sebastiscus mannoratus): visual, somatosen-sory, octavolateral, and cerebellar relay regionto the telencephalon. J. Comp. Neurol., 250:215-227.

Ito, H., M. Yoshimoto, J.S. Albert. N. Yamamoto,and N. Sawai (1999) Retinal projections andretinal ganglion cell distribution patterns in asturgeon (Acipenser transmontanus), a non-teleost actinopterygian fish. Brain Behav.Evol., 53: 127-141.

Ito, H., M. Yoshimoto, J.S. Albert, Y. Yamane, N.Yamamoto, N. Sawai, and A. Kaur (1997) Ter-minal morphology of two branches arisingfrom a single stem-axon of pretectal (PSm)neurons, in the common carp Cyprinus carpio(Teleostei: Cypriniformes). J. Comp. Neurol.,378: 379-388.

Johnston, J.B. (1901) The brain of Acipenser. Acontribution to the morphology of the verte-brate brain. Zool. Jahr., 75: 59-260.

Johnston, J.B. (1909) The morphology of the fore-brain vesicle in vertebrates. J. Comp. Neurol.,19: 457-539.

Johnston, J.B. (19 11 ) The telencephalon of ganoidsand teleosts. J. Comp. Neurol., 21: 489-591.

Kallen, B. (1950) A contribut ion to the ontogeneticdevelopment of the nuclei in the forebrain of Lepisosteu s. Acta Anat, 9: 297-308.

Karten, H.J., and W. Hodos (1970) Telencephalicprojections of the nucleus rotundus in thePigeon (Columbia livia). J. Comp. Neurol.,140: 35-52.

Kicliter, E., and R.G. Northcutt (1975) Ascendingafferents to the telencephalon of ranid frogs: Ananterograde degeneration study. J. Comp. Neu-rol., 767: 239-254.

King, M.A., P.M. Louis, B.E. Hunter, and D.W.Walker (1989) Biocytin: a versatile antero-grade neuroanatomical tract-tracing alterna-tive. Brain Res., 497: 361-367.

Luiten, P.G.M. (1981) Two visual pathways to thetelencephalon in the nurse shark (Ginglimo-stoma cirratum). II. Ascending thalamotelen-cephalic connections. J. Comp. Neurol., 196:539-548.

Meader. R.G. (1934) The optic system of the tele-ost, Holocentrus. J. Comp. Neurol., 60: 361-407.

Murakami, T, T. Fukuoka, and H. Ito (1986) Telen-cephalic ascending acousticolateral system in ateleost (Sebastiscus marmoratus). with specialreference to the fiber of the nucleus proglome-rulosus. J. Comp. Neurol., 247: 383-397.

Neary, T.J., and R.G. Northcutt (1983) Nuclearorganization of the bullfrog diencephalon. J.Comp. Neurol., 275: 262-278.

Nieuwenhuys, R. (1963) The comparative anatomyof the actinopterygian forebrain. J. Hirnforsch.,6(3): 171-192.

Nieuwenhuys , R. (1998) C hondrostean fishes. InThe Central Nervous System of Vertebrates,Vol. 2 (ed. by R. Nieuwenhuys, HJ. TenDonkelaar, and C. Nicholson), Springer, Ber-lin, pp. 701-758.

Nieuwenhuys, R., and T.S. Bodenheimer (1967)The diencephalon of the primitive bony fishPolypterus in the light of the problem of homol-ogy. J. Morph., 778: 415-450.

Nieuwenhuys, R., and J. Meek (1990) The telen-cephalon of Actinopterygian fishes. In CerebralCortex, Vol. 8A (ed. by E.G. Jones and A.Peters), New York, Plenum Press, pp. 31-73.

Northcutt, R.G. (1981) Evolution of the telen-cephalon in nonmammals. Ann. Rev. Neuro-sci.,4:301-350.

Northcutt, R.G. (1995) The forebrain of gnathos-tomes: in search of a morphotype. Brain Behav.EvoL, 40:275-318.

Northcutt, R.G., and M.R. Braford, Jr. (1980) Newobservations on the organization and evolutionof the telencephalon of actinopterygian fishes. In Comparative Neurology of the Telenceph-alon (ed. by S.O.E. Ebbesson), New York,Plenum Press, pp. 41-98.

Northcutt, R.G., and M.R. Braford, Jr. (1984) Someefferent connections of the superficial pretec-tum in the goldfish. Brain Res., 296: 181-184.

Northcutt, R.G., and A. Butler (1980) Projectionsof the optic tectum in the longnose gar Lepisos-teus osseus. Brain Res., 790: 333-354.

Northcutt, R.G., and M. Wullimann (1988) Thevisual system in teleost fishes: morphologicalpatterns and trends. In Sensory Biology of Aquatic Animals (ed. by J. Atema, R. Fay,A. Popper, and W. Tavolga), Springer-Verlag,New York, pp. 515-552.

Reperant, J., N.P. Vesselkin, TV. Ermakova, E.K.Rustamov, J.-P. Rio, G.K. Palatnikov, J. Peyri-choux, and R.V. Kasimov (1982) The retino-fugal pathways in a primitive actinopterygian,the chondrostean Acipenser giildenstadti. Anexperimental study using degeneration, radio-autographic and HRP methods. Brain Res.,257: 1-23.

Richardson, J. (1836) The Fish (Part 3). In FaunaBoreali-American a, New York, pp. 1-327.

Roony, D.J., and T. Szabo (1991) Reciprocal con-nections between the 'nucleus rotundus' andthe dorsal lateral telencephalon in the weaklyelectric fish Gnathonemuspetersii. Brain Res.,543: 153-156.

Rupp, B., and R.G. Northcutt (1998) The dienceph-alon and pretectum of the White Sturgeon (Aci-

penser transm ontanus): a cytoarchitectonicstudy. Brain Behav. Evol., 57: 239-262.

Schneider, G.E. (1969) Two visual systems. Sci-ence, 763: 895-902.

Schnitzlein, H.N. (1962) The habenula and the dor-sal thalamus of some teleosts. J. Comp. Neurol.,118: 225-267.

Schroeder, D.M., and S.O.E. Ebbesson (1974)Nonolfactory telencephalic afferents in theNurse Shark (Ginglymostoma cirratum). BrainBehav. Evol., 9: 121-155.

Stnedter, G.F. (1990) The diencephalon of thechannel catfish Ictalurus punctatus. II. Retinal,tectal, cerebellar and telencephalic connec-tions. Brain Behav. Evol., 36: 355-377.

Striedter, G.F., and R.G. Northcutt (1989) Two dis-tinct visual pathways through the superficialpretectum in a percomorph teleost. J. Comp.Neurol., 283: 342-354.

Vanegas, H., and H. Ito (1983) Morphologicalaspects of the teleostean visual system: a re-view. Brain Res. Rev., 6: 117-137.

Wullimann, M.F., and D.L. Meyer (1993) Possiblemultiple evolution of indirect telencephalo-cerebellar pathways in teleosts: studies inCarassius auratus and Pantodon buchholzi.Cell Tissue Res., 274: 447-455.

Yamamoto, N., M. Yoshimoto, J.S. Albert, N.Sawai, and H. Ito (1999) Tectal fiber connec-tions in a non-teleost actinopterygian fish, thesturgeon Acipenser. Brain Behav. Evol., 53:142-155.

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