Anatomical identification of a telencephalic visual area in crocodiles: Ascending connections of nucleus rotundus inCaiman crocodilus

Anatomical Identification of a Telencephalic Visual Area in C roc0 d i I es : Ascend i n g Go n n ec t i on s of N uc I eu s Rotundus in Caiman crocodilus

MICHAEL B. PRITZ 1

Department of Anatomy, Ohio 441 06

Case Western Re serve University, Cleveland,

A B S T R A C T Nucleus rotundus receives a major input from the optic tectum in crocodiles, C a i m a n crocodilus. Telencephalic projections of nucleus rotundus were studied in C a i m a n by means of the Fink-Heimer procedure after anodal, stereotaxic lesions. Efferent axons of nucleus rotundus assemble on the ventromedial aspect of this nucleus and swing ventrolaterally to enter the dorsal peduncle of the lateral forebrain bundle. These ascending fibers continue rostrally in the dorsal peduncle of the lateral forebrain bundle to enter the telencephalon where they remain restricted to a lateral portion of the lateral forebrain bundle. At more anterior levels, these fascicles turn dorsally, pass through the ventrolateral area, and terminate massively in a lateral part of the rostral dorsolateral area.

The results of this experiment are compared with similar studies on thalamotelencephalic connections of diencephalic visual areas in other amniotes. Parallels in fiber connections of thalamic auditory and visual areas and the segregation of these modalities in the telencephalon of C a i m a n are discussed. These similarities in neural circuitry and synaptic elements of auditory and visual systems that synapse in the midbrain of C a i m a n form the basis for a different interpretation of sensory system organization in amniotes.

Physiological studies indicate that auditory and visual space are represented in a highly ordered fashion in anatomically separate areas in the midbrain of crocodiles. Audition is organized tonotopically in the torus semicircularis (Manley, '71) whereas vision is represented retinotopically in the optic tectum (Heric and Kruger, '65). Addi- tional similarities between midbrain auditory and visual areas can also be demonstrated. Among these are parallels in ascending fiber connections. Both of these midbrain sensory regions project bilaterally to a prominent nucleus in the posterior thalamus. In each case, contralateral connections are achieved by way of the supraoptic decussation. The central nucleus of the torus semicircularis sends axons to terminate in nucleus reuniens pars centralis (Pritz, '74a) whereas the optic tectum projects to nucleus rotundus (Braford, '72). Moreover, audition and vision, which are segregated in the midbrain, also remain separate in the thalamus.

J. COMP. NEUR., 164: 32S338.

These findings raise two questions: (1) do audition and vision remain separate in the telencephalon? and ( 2 ) are there further parallels in the efferent connections of nucleus reuniens pars centralis and nucleus rotundus? A partial answer to these questions was obtained in a subsequent experiment (Pritz, '74b). This study, which investigated the ascending connections of nucleus reuniens pars centralis, demonstrated that this neuronal aggregate pro- jected to an area in the medial caudal telencephalon. The next logical step was to investigate the efferent projections of nucleus rotundus. The purpose of the present report is to describe these results.

Stereotaxic lesions were placed in nucleus rotundus in Caiman and the degenerated fibers were traced by means of silver impregnation methods (Fink and Heimer, '67). Lesions of nucleus rotundus resulted in terminal degeneration restricted to a lateral

Present address: University Hospitals, University of Michigan Medical Center, Ann Arbor, Michigan 48104.

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part of the anterior dorsolateral area and did not overlap the auditory projection area. The results of the present study demonstrate two important aspects of the organization of these sensory systems. First, audition and vision, which are segregated in the midbrain and thalamus, remain s e p arate in the telencephalon. Second, nucleus reuniens pars centralis and nucleus rotundus, which share similar inputs from the midbrain, exhibit similar outputs to the telencephalon. Additional parallels between auditory and visual systems that synapse in the midbrain of crocodiles are presented. These similarities form the basis for a different interpretation of sensory system organization in amnio tes.

Some of these findings were presented previously (Pritz, '73).

METHODS AND MATERIALS

Since the procedures and techniques used in this experiment are identical to those described in detail in two previous re- ports (Pritz, '74a,b), only a brief account is presented here.

Anodal, stereotaxic lesions were attempted in 13 juvenile Caiman crocodilus which ranged in snout-vent length from 11.0 to 14.0 cm. After adequate anesthesia by cold narcosis, the calvarium over the telencephalon and optic tectum was removed. Then a stainless steel microelectrode was stereo- taxically inserted through the ipsilateral, caudal telencephalon. Since the results of a pilot study (Pritz, '73) indicated that the projections of nucleus rotundus are restricted to the ipsilateral telencephalon, bilateral lesions were made in five cases. Nine to 16 days postoperatively, animals were given a lethal overdose of sodium pentobarbital and were perfused through the heart with 10% formalin. After the brains had har- dened in 10% formalin, they were blocked in situ in order to achieve a standard and reproducible plane of section. The blocked brains were then removed from the skull and placed in 10% formalin for several days before they were embedded in albumin-gelatin (Fink and Kess, '70). The brains were sectioned transversely on a freezing micro- tome at 25 p . Sections were stored in 2% formalin. Selected sections were stained with the Fink-Heimer ('67) method and ad- jacent sections were stained with cresyl vio-

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let. In certain cases, a fiber stain (Fink and Schneider, '69) was used. In some cases, a Prussian blue reaction on sections counterstained with cresyl violet was em- ployed. Chartings of degeneration and the interpretation of degenerated axons and terminals were done in the same manner as described previously (Pritz, '74a,b). De- generated axons were easily distinguished from degenerated terminals. The former appeared as chains of black dots while the latter appeared as solid black spherules over and between neuronal perikarya.

When reconstructions were made, the ex- ternal boundary of these ablations was drawn around the zone of increased cellularity that surrounded each lesion. No cor- rection was made for tissue shrinkage or for progressive morphologic changes in lesion size which are known to occur with time after such electrolytic lesions (Wolf and DiCara, '69).

RESULTS

Several accounts briefly describe the morphology of nucleus rotundus in species of Crocodilia other than Caiman crocodilus (Huber and Crosby, '26; Kappers et al., '60). Nevertheless, a short description of nucleus rotundus in Caiman is presented because a correct interpretation of the lesions made in this experiment depends on the ability to identify this nucleus and to distinguish it from other diencephalic nuclei. The terminology adopted in this report is that of Huber and Crosby ('26) and Crosby ('17).

Descriptive morphology of nucleus rotundus

Nucleus rotundus is a prominent, oval shaped nucleus located in the caudal half of the diencephalon. It is bordered rostrally by nucleus dorsolateralis anterior; supe- riorly and caudally by nucleus medialis; and laterally, medially, and inferiorly by fibers of the lateral forebrain bundle. In transverse sections, this neuronal aggregate f m t appears at the rostral pole of the posterior commissure. As one continues anteriorly, i t enlarges and reaches a maximum size at the level of the habenular commissure. It continues as far rostral as nucleus dorsolateralis anterior. However, the boundary between these two neuronal masses is

TELENCEPHALIC PROJECTIONS OF NUCLEUS ROTUNDUS 325

often difficult to distinguish. In such in- stances, nucleus rotundus can be differen- tiated from nucleus dorsolateralis anterior because the neurons of the former are more loosely packed than those of the latter (see figs. 6, 11 of Huber and Crosby, ’26).

When stained with cresyl violet, the neurons of nucleus rotundus appear as loosely grouped, medium sized, oval cells. However, the distinct morphology of this nucleus in fiber stained preparations sets nucleus rotundus apart from all other diencephalic nuclei in Caiman. In such material, thick fascicles leave the center of nucleus rotundus and course diagonally to collect on its medial border. Some of these axons are destined for the telencephalon. This obser- vation is suggested by a comparison of the myeloarchitecture of nucleus rotundus in an unlesioned animal with the degenerated axon picture seen after a lesion of this nucleus (fig. 1).

Loci and extent of lesions Attempted lesions of nucleus rotundus

were easily identified in cell and fiber stained material and by a Prussian blue reaction in which they appeared turquoise. The morphology of such lesions was similar in all cases. The center of the lesion, which was either free of tissue or contained

necrotic tissue, was surrounded by a ring of gliosis which was encircled by a region of increased cellularity.

Reconstructions of the ablations revealed the following distribution of lesions. Ten lesions did not destroy nucleus rotundus or damage its efferent axons. These unsuccess- ful lesions injured structures on all sides of nucleus rotundus except at its lateral border. These ablations damaged nucleus dorsolateralis anterior, nucleus dorsomedialis anterior, area triangularis, nucleus medialis, the hypothalamus, and fibers of the lateral forebrain bundle that were located ventromedial to nucleus rotundus. None of these ablations produced terminal degeneration that overlapped the telencephalic projection area of nucleus rotundus. The re- maining eight lesions destroyed either nucleus rotundus or its exiting axons. Five of the eight lesions damaged the lateral forebrain bundle. However, these ablations not only injured axons of nucleus rotundus but also destroyed axons from other nuclei. Another lesion destroyed the dorsolateral segment of nucleus rotundus. Unfortunate- ly, this ablation also damaged a number of surrounding structures as well. The remain- ing two lesions were located solely within the confines of nucleus rotundus. These ablations provided an unambiguous inter-

Fig. 1 Morphology of nucleus rotundus in Caiman. Transverse sections of the left nucleus rotundus are shown. Dorsal is towards the top of the page while lateral is towards the left. Pho- tographs of sections stained with cresylviolet, a “normal” fiber stain, and a stain for degenerated axons are shown in the left, middle, and right panels. The degenerated axon picture seen after a lesion of nucleus rotundus (arrow, right panel) bears a marked resemblance to the “normal” axon picture (arrow, center panel). These similarities suggest that at least some of the fibers shown in the center panel are destined for the telencephalon. Bar scale represents 200 fi .

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pretation of the ascending trajectory and locus of termination of rotundal axons in the telencephalon.

Ascending connections of nucleus rotundus

The description of telencephalic projections of nucleus rotundus is based mainly on the two ablations illustrated in figures 2 and 3. These lesions, which were limited to the confines of nucleus rotundus, provide the major basis for the present interpretation of its ascending connections. In each case, coarse fascicles of degenerated axons were found to assemble on the ventromedial aspect of this nucleus (fig. 5F) and swing ventrolaterally to enter the dorsal peduncle of the lateral forebrain bundle (fig. 5E). These fibers continue rostrally in the dorsal peduncle of the lateral forebrain bundle to enter the telencephalon. Here they remain restricted to the lateral portion of the lateral forebrain bundle (fig. 5D). In more anterior sections, these fibers turn dorsally (fig. 5C), pass through, and may synapse on interposed cells of the ventrolateral area (fig. 5B). Eventually, these rotundal axons terminate massively in a lateral portion of the rosaal dorsolateral area (figs. 5A, 6). No terminal degeneration was ob- served in the contralateral hemisphere or

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in any other portion of the ipsilateral telencephalon.

Fiber stains (Fink and Schneider, '69) have proven inadequate to dlstinguish this anterolateral terminal zone from surrounding portions of the dorsolateral area. Easier identification has been accomplished with cresyl violet preparations. In more posterior sections, this visual area is difficult to dif- ferentiate from other parts of the telenceph- don on the basis of cytoarchitectonics. However, as one proceeds anteriorly, a cell free zone appears on the medial border of the visual area. This cell free region sep- arates the small, round, loosely packed, laterally placed neurons of the rotundal projection zone from the more medial, densely packed cells of the dorsolateral area (fig. 7). The other boundaries of this telencephalic visual region are indistinct.

DISCUSSION

lnterpretatwn of rotundo-telencephalic projec twns

The problem of idenufication of fibers of passage is common to all studies which use special stains to impregnate degenerated axons and axon terminals that emanate from a particular lesion site. In the present experiment, two sources of error are possible. One is that the electrode place-

Fig. 2 Locus and extent of a small lesion limited to the confines of nucleus rotundus in Caiman. In A, lesion (solid blackened area) is reconstructed on a horizontal section of nucleus rotundus that illustrates the brain levels, 1 through 3, of similarly labeled transverse sections shown in B. Abbreviations: A, anterior; Gv, ventral geniculate nucleus; H , hypothalamus; Hb, habenula; L, lateral; OT, optic tract; Rt, nucleus rotundus; SM, stria medullaris.


A B

Fig. 3 Locus and extent of a medium sized lesion limited to the confines of nucleus rotundus in Caiman. In A, lesion (solid blackened area) is reconstructed on a horizontal section of nucleus rotundus that illustrates the brain levels, 1 through 6, of similarly labeled transverse sections shown in B. Abbreviations: A, anterior; D, nucleus diagonalis; Gv, ventral geniculate nucleus; H, hypothalamus; L, lateral; OT, optic tract; Rc, nucleus reuniens pars centralis; Rd, nucleus reuniens pars diffusa; Rt, nucleus rotundus.

ment itself produced the terminal degeneration seen in the anterolateral part of the dorsolateral area. This is probably not the case because ten lesions which did not damage nucleus rotundus or its exiting axons failed to produce terminal degeneration in those parts of the telencephalon where terminals were found after rotundal lesions.

The other possibility is that axons which arise in other nuclei and pass through nucleus rotundus were destroyed by localized ablations of nucleus rotundus. The degeneration that resulted from restricted rotundal lesions was probably due to rotundal damage because of the following reasons. First, lesions were placed in nearly all bor-

328 MICHAEL B . PRITZ

cephalic visual area are difficult to determine for two reasons. First, successful lesions of nucleus rotundus were subtotal and did not damage the entire nucleus. Second, the telencephalic projection area of nucleus rotundus was not sharply demarcated in either cell or fiber stained material. Thus, extrapolation of the entire extent of this telencephalic visual area from those successful cases of nucleus rotundus ablations was not possible. The inability to note sharp subdivisions in the dorsolateral area was also encountered in a previous study that identified a telencephalic auditory area in Caiman (Pritz, '74b). Likewise, Crosby ('17) failed to identify distinct divisions of the dorsolateral area in the American alligator. However, others (Rose, '23; Riss et al., 'SS), who have examined the same as well as re- lated species of Crocodilia, have recognized subdivisions within an area that corresponds to the dorsolateral area in Caiman and Alligator mississipiensis. The difficul- ties in such comparisons, particularly when they are based primarily on cytoarchitec- tural features, were discussed previously (Pritz, '74b) and are also applicable to the present study.

Rose, who described the morphology of the telencephalon in certain reptiles ('23) and birds ('14), subdivided this brain region and labeled these areas with capital letters. One of these regions, field S (Rose, '14), corresponds to the ektostriatum of pigeons, which receives a direct and highly organized input from nucleus rotundus (Karten and Hodos, '70). One might then conclude that field S in reptiles (Rose, '23) also receives an input from nucleus rotundus. Based on the experimental determina- tion of the telencephalic connections of nucleus rotundus as well as on cytoarchi- tectural analysis of this visual area, I conclude that this is not the case in Caiman. Specifically, nucleus rotundus in Caiman crocodilus projects to that area of the telencephalon designated by Rose ('23) as field G and not field S. This is not meant to imply that a shift in the rotunda1 projection has occurred in crocodiles and birds but that Rose has erred in his identification of homologous fields in these two groups of amniotes. This telencephalic projection area of nucleus rotundus corresponds to zone 8 in the terminology of Riss et al. ('69).

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A B C D E F Fig. 4 OutlinedrawingsofCtrimczn brains drawn

to scale that illustrate the plane of section and the brain levels of similarly labeled transverse sections, A through F, in figure 5. Dorsal (a), lateral (b), and parasagittal (c) views are figured. The parasagittal illustration is taken at a level shown by the horizontal line in the drawing of the dorsal aspect. Abbre- viations: Cb, cerebellum; DLA, dorsolateral area; OB, olfactory bulb; Tel, telencephalon; TeO, optic tectum; TS, torus semicircularis; VLA, ventrolateral area.

ders of nucleus rotundus in this experiment and previous ones (Pritz, '74a,b). After such ablations, no degenerated axons were ever seen to pass through nucleus rotundus or to terminate in the telencephalic visual area described in this study. Second, lesions which did not destroy cells in nucleus rotundus but which did damage its exiting axons produced a pattern of degeneration identical to that seen after localized ablations of nucleus rotundus.

Telencephalic projections of nucleus rotundus

Terminal field in the dorsolateral area. The locus and entire extent of this telen-


Fig. 5 Ascending connections of nucleus rotundus of Caiman as viewed in transverse sections. Dia- grams A through F correspond to the levels and plane of section shown in figure 4. Chartings are from the case whose lesion is illustrated in figure 2. Dots represent terminal degeneration while short line segments indicate degenerated fibers. Abbreviations: DLA, dorsolateral area; Dla, nucleus dorsolateralis anterior; Dma, nucleus dorsomedialis anterior; dp, dorsal peduncle of the lateral forebrain bundle; Gv, ventral geniculate nucleus; H, hypothalamus; Hb, habenula; LFB, lateral forebrain bundle; MFB, medial forebrain bundle; OC, optic chiasm; OT, optic tract; Rt, nucleus rotundus; SM, stria medullaris; VLA, ventrolateral area.

Ventrolateral area. Lesions that dam- generation cannot be positively identified age nucleus rotundus or its exiting axons in the ventrolateral area because of the dif- produce degenerated fibers which course ficulty in the identification of terminal de- through the lateral portion of the ventro- generation within a field of degenerated lateral area before they terminate in the axons with the light microscope. Proof of overlying dorsolateral area. Terminal de- direct connections between nucleus rotun-

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C

Fig. 6 Telencephalic projection area of nucleus rotundus in Caiman. Outline drawings of Caiman brains drawn to scale are shown on lateral (A) and parasagittal (B) views. A and B illustrate the plane of section and the brain levels, 1 through 3, of similarly labeled transverse sections in C. The parasagittal drawing is taken at a level depicted by the horizontal line in the drawing of the dorsal aspect of the Caiman brain in figure 4. Chartings are from the case whose lesion is illustrated in figure 3. Dots represent terminal degeneration while short line segments indicate degenerated fibers. Abbreviations: Cb, cerebellum; DLA, dorsolateral area; n 11, optic nerve; OB, olfactory bulb; Tel, telencephalon; TeO, optic tectum; TS, torus semicircularis; VLA, ventrolateral area.

dus and the ventrolateral area must await more conclusive evidence.

Thalamotelencephalic connections of nucleus rotundus in crocodiles

and in other reptiles With the exception of a single study (Hall

and Ebner, '70a), previous attempts to determine the ascending connections of nucleus rotundus in crocodiles and in other reptiles have been of two types. One approach, which is purely descriptive, uses various silver stains to impregnate myeli- nated and unmyelinated fibers. Based on this method, connections between nucleus rotundus and the telencephalon by way of the dorsal peduncle of the lateral forebrain bundle were described in alligators

(Huber and Crosby, '26) and in other r e p tiles (for example: Johnston, '15; Cairney, '26; Shanklin, '30; Papez, '35). However, no specific portion of the telencephalon was recognized as interconnected with nucleus rotundus on the basis of these studies. Since nearly all fiber systems are equally stained by this technique, a reliable deter- mination of the trajectory and direction of conduction between specific nuclear groups is almost impossible. Because of these prob- lems, this method has been replaced by var- iants of the Nauta method and by auto- radiography. The other approach is to identify those regions of the brain that un- dergo retrograde cell changes after a localized ablation. By means of this technique retrograde degeneration was found in nu-

TELENCEPHALIC PROJECTIONS OF NUCLEUS ROTUNDUS 33 1

Fig. 7 Cytoarchitecture of the telencephalic projection areaofnucleusrotundusin Caiman. This photograph is a cresyl violet stained section that corresponds to figure 6, C-2. Boxed area encloses a portion of this telencephalic visual area. Abbrevin- t ions: DLA, dorsolateral area; VLA, ventrolateral area. Bar scale represents 1 mm.

cleus rotundus after large ablations that destroyed areas comparable to the dorsolateral and ventrolateral areas of Caiman in Alligator mississipiensis (Kruger and Berkowitz, '60) and in Lacerta uiridis (Powell and Kruger, '60). More restricted ablations of the dorsolateral area in Alli- gator, however, failed to produce retrograde cell changes in neurons of nucleus rotundus (Kruger and Berkowitz, '60). The ex- planation for this latter phenomenon, the failure of restricted ablations of the dorsolateral area to cause retrograde cell changes in nucleus rotundus, is not known. One sug- gestion is that axon collaterals to the ventrolateral area and/or to other nontelen- cephalic structures sustain the cells in nucleus rotundus after ablations of the dorsolateral area (Kruger and Berkowitz, '60). Another possibility is that even though ablations of the dorsolateral area were large, they may not have destroyed a suf- ficient volume of this telencephalic projection area of nucleus rotundus to cause retrograde cell changes in nucleus rotundus.

Nucleus rotundus in Pseudemys and nucleus rotundus in Caiman are similar in gross morphology (Kappers et al., 'SO), topographic location in the diencephalon (Kap- pers et al., 'SO), input from the optic tectum (Hall and Ebner, '70b; Braford, '72), and lack of input from the retina (Hall and Ebner, '70b; Burns and Goodman, '67). Nucleus rotundus in these two groups of reptiles is also similar in its efferent connections. After lesions restricted to nucleus rotundus in Pseudemys, degenerated axons travel through the diencephalon in the dorsal peduncle, course rostrally and laterally in the lateral forebrain bundle, swing dorsally through the basal telencephalic nuclei, and terminate densely in the core of the dorsal ventricular ridge (Hall and Ebner, '70a). Similarly, as found in the present study, lesions of nucleus rotundus in Cai- m a n produce degenerated axons that travel through the diencephalon in the dorsal peduncle, course rostrally and laterally in the lateral forebrain bundle, swing dorsally through the ventrolateral area, and ter-

Fig. 8 Terminal degeneration in the anterolat- era1 part of the dorsolateral area of Caiman after a lesion of nucleus rotundus. This photograph is from the region indicated by the box in figure 7. Bar scale represents 10 p.

332 MICHAEL B. PRITZ

minate heavily in an anterolateral part of the dorsolateral area. These similarities between nucleus rotundus in Pseudemys and Caiman strongly suggest that these nuclei are derivatives of the same embryonic field, and probably derivatives of an identical population of neurons, in some reptilian group common to both crocodiles and turtles. Although the present data are still incomplete, a similar relationship probably exists between the telencephalic projection areas of nucleus rotundus in Pseudemys and Caiman.

Comparison of telencephalic projections of nucleus rotundus between

Caiman and pigeons Nucleus rotundus in Caiman and nucleus

rotundus in pigeons have several features in common. Among these are similarities in topographic location in the thalamus (Kappers et al., '60), gross morphology (Kappers et al., 'SO), input from the optic tectum (Braford, '72; Karten and Revzin, '66), and lack of input from the retina (Bums and Goodman, '67; Cowan et al., '61; Karten and Nauta, '68; Meier et al., '74). A comparison between the telencephalic projections of nucleus rotundus in Cai- m a n and pigeons demonstrates additional parallels. In pigeons, efferent axons of nucleus rotundus form the lateral part of the fasciculus prosencephali lateralis, pass through the lateral portion of the paleostri- atal complex, and terminate in the central core of the ektostriatum (Karten and Hodos, '70). In an analogous fashion, the efferent axons of nucleus rotundus in Caiman form the lateral portion of the lateral forebrain bundle, pass through the lateral portion of the ventrolateral area, and terminate in an anterolateral part of the dorsolateral area (present experiment). These data strongly suggest that nucleus rotundus of Caiman and nucleus rotundus of pigeons are derivatives of the same embryonic field, and probably derivatives of an identical population of neurons, in some archosaurian reptilian group common to both crocodiles and birds.

Other than input from nucleus rotundus, these telencephalic visual areas (central core of the ektostriatum in pigeons and anterolateral part of the dorsolateral area in Caiman) are similar in topographic location,

in exhibiting high succinate dehydrogenase activity (Baker-Cohen, '68), and as derivatives of similar migration layers (Kiillen, '53, '62). Such parallels suggest that these two areas are also derivatives of the same embryonic field, and possibly derivatives of an identical population of neurons, in some archosaurian reptilian group ancestral to both crocodiles and birds. The cyto- and myelc-architecture of the ektostriatum have been described in detail in pigeons (Karten and Hodos, '70). A comparable description of the rotunda1 projection area in Caiman would provide important evidence to assess further the similarities between these telencephalic visual areas in Caiman and pigeons. Unfortunately, efforts to describe the cyto- and myelo-architecture of this visual area in Caiman have not yielded the dis- tinc tive features noted by Karten and Hodos ('70) that distinguish the ektostriatum of pigeons from surrounding parts of the telencephalon. Thus, the present comparison between the telencephalic visual areas in Caiman and pigeons would rest on consid- erably stronger ground should other similarities in morphology, physiology, and role in behavior be uncovered. Nevertheless, the experimentally proven evidence of a rotundo-telencephalic projection in species as diverse as turtles (Hall and Ebner, '70a), crocodiles (present study), and pigeons (Karten and Hodos, '70) suggests that this pathway may be common to all nonmam- malian amniotes.

Comparison of thalamotelencephulic connections between Caiman and

certain mammals A major difficulty in a comparison of the

results of the present experiment with similar studies in mammals is knowing which nucleus in mammals is comparable to nucleus rotundus of Caiman. Identification of a homologous neuronal aggregate in mammals solely on the basis of cyto- and myelo- architectonic properties is hazardous. One has only to examine the diversity of nomen- clature that has resulted from such descrip tive studies of the thalamus in different mammals to know that this approach is unsatisfactory. Other than its telencephalic projections and its appearance in cell and fiber stained preparations, the only other feature that distinguishes nucleus rotundus


from other nuclei in the dorsal thalamus of Caiman is that it receives input from the optic tectum (Braford, ’72) but not from the retina (Burns and Goodman, ’67). A similar pattern of afferents to certain nuclear groups in the thalamus also occurs in mammals. Accordingly, such a relationship of afferent connections can serve as a start- ing point for a comparison between Caiman and certain mammals.

The optic tectum of Caiman and the superior colliculus of mammals probably are derivatives of the same embryonic field in some reptilian group ancestral to both crocodiles and mammals. However. additional comparisons between subdivisions of the optic tectum of C a i m a n and the superior colliculus of mammals are unclear. Such comparisons are important because the superior colliculus of mammals is not a homogeneous structure but a heterogene- ous area whose physiologic and anatomic properties vary according to depth. For example, receptive field properties of neurons in the most superficial layers of the superior colliculus differ from those of cells located in the intermediate and deep layers (cat: Straschill and Hoffinann, ’69; Stein and Arigbede, ’72; Gordon, ‘73; monkey: Cyna- der and Berman, ’72; rabbit; Masland et al., ’71; mouse: Drager and Hubel, ’75).

Not only are there differences in recep tive field properties between various layers of the superior colliculus but there are also differences in afferent and efferent fiber connections. These anatomical features have been studied in greatest detail in tree shrew and bushbaby and to a lesser extent in rhesus monkey. These studies demonstrate the presence of a direct visual channel from the retina to the superficial layers of the superior colliculus (tree shrew: Tigges, ’66; Campbell et al., ’67; Laemle, ’68; monkey: Wilson and Toyne, ’70; Lund, ’72; bushbaby: Campos-Ortega and Cluver, ’68; Tigges and Tigges, ’70) and from here to the “pulvinar”2 (tree shrew: Harting, Hall et al., ’73; rhesus monkey: Benevento and Fallon, ’75; bushbaby: Glendenning et al., ’75). The “pulvinar,” in turn, projects to a region of cortex located between stri- ate cortex (area 17) and auditory cortex (tree shrew: Harting et al., ’73; rhesus monkey: Rezak and Benevento. ’75; bushbaby: Glendenning et al., ’75).

In Caiman, nucleus rotundus is the only neuronal aggregate in the dorsal thalamus that receives input from the optic tectum (Braford, ’72) but not from the retina (Burns and Goodman, ’67). Although this input to nucleus rotundus may represent a direct visual channel via the superficial strata of the optic tectum, direct evidence in support of this statement is not yet avail- able in Caiman. However, preliminary evidence in lizards, Iguana iguuna (Foster et al., ’73), suggest that laminar projections of the optic tectum in this reptile are similar to the efferent connections of the superior colliculus described for tree shrew (Harting, Hall et al., ’73), monkey (Bene- vento and Fallon, ’75), and bushbaby (Glendenning et al., ’75). In Iguana, retinal ganglion cell axons terminate in the superficial layers of the optic tectum (Butler and Northcutt, ’71). Lesions of this retinal re- cipient zone produce diffuse, sparse degeneration in nuc1,eus rotundus. However, when the tectal lesion extends slightly deeper, more dense degeneration is seen in nucleus rotundus (Foster et al., ’73). If one extrapo- lates these findings in Iguana to suggest that an analogous situation exists in Cai- man, then nucleus rotundus of Caiman and the “pulvinar” of certain mammals are quite similar in terms of their afferent organization.

A continuation of this comparison between nucleus rotundus of crocodiles and the “pulvinar” of mammals demonstrates similarities as well as differences between the loci of termination of their efferents. Both nucleus rotundus and the “pulvinar” send a major projection to the telenceph- don. Those areas in mammals which receive input from the “pulvinar” are highly laminated cortical zones located on the brain surface between the meninges and the lateral ventricle. On the other hand, that part of the telencephalon in Caiman that receives input &om nucleus rotundus is not organized as a cortex but as a nucleus. Fur- thermore, this telencephalic visual area in Caiman is located deep within the brain and is in close relationship with the lateral ventricle but not with the meninges. Sim-

2 In this and subsequent discussion, “pulvinar” re- fers to that part of the thalamus in tree shrew, rhesus monkey, and bushbaby, that receives input from the superficial layers of the superior colliculus but not hom the retina.

334 MICHAEL B . PRITZ

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Figure 9


ilar differences in morphology and topographic location of telencephalic projection areas of thalamic auditory areas in Caiman and certain mammals were also noted in a previous study (Pritz, '74b).

Organization of auditory and visual systems in Caiman

The torus semicircularis pars centralis, the midbrain auditory area, and the optic tectum, the midbrain visual region, share similarities in topographic location, ascending connections, and certain physiological properties (summarized in Pritz, '74a). The results of the present experiment to- gether with those of a previous study (Pritz, '74b) demonstrate parallels between nucleus reuniens pars centralis, a diencephalic auditory area, and nucleus rotundus, a diencephalic visual region. Each of these nuclei, which share similar inputs from the midbrain and similar topographic location in the caudal thalamus, exhibit similar outputs to the telencephalon. Ascending axons from each respective nucleus enter the dorsal peduncle of the lateral forebrain bundle, swing dorsally through the ventrolateral area, and terminate in the ipsilateral dorsolateral area. Furthermore, in each case the trajectory and locus of telencephalic termination of axons from these sensory nuclei reflect the topographic location in the thalamus of each respective nucleus. Ac- cordingly, axons from nucleus reuniens pars centralis, which is located in a caudal and medial part of the thalamus, remain restricted to a medial part of the lateral fore-

Fig. 9 Summary of ascending connections of auditory and visual systems that synapse in the midbrain of Caiman. A and B are outline drawings of Caiman brains drawn to scale that illustrate the plane of section and brain levels, 1 through 4, of similarly labeled transverse sections in C. Lateral (A) and parasagittal (B) views are figured. C is a diagram of composite transverse sections, 1 through 4, that show the auditory (solid lines) and visual (broken lines) pathways from the midbrain and their major connections. Abbreviations: Cb, cerebellum; D, nucleus diagonalis; DLA, dorsolateral area; Gv, ventral geniculate nucleus; H, hypothalamus; LFB, lateral forebrain bundle; LL, lateral lemniscus; MFB, medial forebrain bundle; MLF, medial longi- tudinal fasciculus; N 111, oculomotor nucleus; n 11, optic nerve; OB, olfactory bulb; OT, optic tract; PC, posterior commissure; PGF, periventncular gray and fibers; Rc, nucleus reuniens pars centralis; Rd, nucleus reunienspars diffisa; Rt, nucleusrotundus; SOD, supraoptic decussation; Tel, telencephalon; TeO, optic tectum; TS, torus semicircularis; VLA, ventrolateral area; 3, lamina 3 of the optic tectum; 5, lamina 5 of the optic tectum.

brain bundle and end in a caudal and m e dial part of the dorsolateral area (Pritz, '74b). On the other hand, axons from nucleus rotundus, which is located anterior and lateral to nucleus reuniens pars centralis, remain restricted to a lateral part of the lateral forebrain bundle and terminate in an anterior and lateral part of the dorsolateral area (present study). No overlap in the telencephalic projections of nucleus reuniens pars centralis and nucleus rotundus could be demonstrated. Therefore, audition and vision are segregated in the telencephalon. Those parts of the dorsolateral area in Caiman that receive auditory and visual input from the thalamus correspond to the dorsal ventricular ridge of other reptiles and birds. A summary of these ascending connections of auditory and visual systems that synapse in the midbrain of Caiman is illustrated in figure 9.

These results emphasize certain features relative to the organization of these two sensory systems in Caiman. First, audition and vision, which remain separate in the midbrain, are also segregated in the diencephalon and telencephalon. Second, several parallels are present between ascending connections of midbrain and thalamic auditory and visual areas. Third, further similarities in the more peripheral synaptic elements of these two sensory systems can also be demonstrated (table 1).

These parallels in fiber connections and synaptic elements are not unique to auditory and visual systems in Caiman. Similar fiber paths have been identified in other amniotes.

In other reptiles and birds, those portions of the telencephalon that ultimately receive sensory information by way of the midbrain are also located in the dorsal ventricular ridge (Hall and Ebner, '70a; Foster and Peele, '75; Karten, '68; Karten and Hodos, '70). This region of the forebrain is not only readily identifiable in most reptiles and birds but also is easily distinguished from cortex on the basis of its cytoarchitecture and location. Cortex possesses distinct lami- nae that include a surface fiber layer and neurons with dendritic trees that are polar- ized towards the pial surface. Furthermore, cortex is a surface structure that is located between the meninges and the lateral ventricle. The dorsal ventricular ridge, on the other hand, lacks the characteristic lami- nation and orientation of dendrites and a p


TABLE 1

Generalized pattern ofsynaptic elements of sensory systems that synapse in the midbrain and the specijic structurc.s in the auditory and visual systems of Caiman

that correspond to this generalized scheme

Generalized pattern Vision of synaptic elements Audition

Rods and cones Receptor cells Hair cells Retinal bipolar cells Bipolar cells Spiral ganglion cells Retinal ganglion cells Long axon cells Cochlear nuclei cells Optic tectum Midbrain Central nucleus of the torus semicircularis Nucleus rotundus Thalamus Nucleus reuniens pars centralis Dorsal ventricular ridge Telencephalon Dorsal ventricular ridge

pears to be organized as a nucleus (which in certain reptiles is ensheathed by a band of neurons). In addition, the dorsal ventricular ridge is located deep within the brain and lies near the lateral ventricle. The dorsal ventricular ridge is never bordered by the meninges. Differences in neuronal morphology and topographic location are not the only feature that distinguish the dorsal ventricular ridge from cortex in these r e p tiles and birds. Sensory systems that synapse in the midbrain proceed into the dorsal ventricular ridge (Hall and Ebner, '70a; Pritz, '74 b, present experiment; Foster and Peele, '75; Karten, '68; Karten and Hodos, '70) whereas sensory systems that bypass the midbrain to synapse directly in the thalamus proceed into cortex (Hall and Ebner, '70a; Hunt and Webster, '72; Karten et al., '73; Meier et al., '74; Reperant et d., '74).

The division of sensory systems into those that synapse in the midbrain and those that bypass the midbrain to terminate directly in the thalamus adequately describes all thalamotelencephalic connections that have thus far been examined in reptiles and birds. However, only the modalities of audition and vision have been investigated in only a few groups of reptiles and birds. Therefore, hrther experimentation will be necessary to determine whether other amniotes and other sensory systems follow this pattern.

ACKNOWLEDGMENTS

I am grateful to Professor M. Singer for providing the facllities and support that al- lowed me to complete this research. I also thank T. J. Voneida, M. R. Braford, Jr., R. G. Northcutt, E. M. Pritz ;and R. B. Freeman. A portion of this study was fund- ed by PHS grant GM-00820-11 and NIH grant NS-08417-03.

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Anatomical identification of a telencephalic visual area in crocodiles: Ascending connections of nucleus rotundus inCaiman crocodilus