AMER. ZOOL., 17:411-429 (1977).

Elasmobranch Central Nervous System Organization and Its Possible Evolutionary Significance

R. GLENN NORTHCUTT

Division of Biological Sciences, University of Michigan, Ann Arbor, Michigan 48109

SYNOPSIS. Examination of shark brain:body ratios reveals that these taxa possess relative

brain volumes in a range overlapping those of bony fish as well as birds and mammals. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 Much of the variation is due to relative development of the telencephalon and cerebellum. Telencephalic weights vary from 24% in Squalus to 52% in Sphyrna. Analysis of the cytoarchitectonics of the shark brains reveals at least two patterns of development. Squalomorph sharks possess low brain:body ratios, and the telencephalon of these taxa possess well developed lateral ventricles and poorly developed pallial areas. The dienceph- alon is characterized by prominent periventricular laminae, and the cerebellum lacks foliation. The lamniform and carcharhiniform sharks are characterized by high brain: body ratios, and there is marked hypertrophy of the telencephalon. The roof (pallial) regions, as well as the diencephalon, are characterized by extensive cellular migrations. The cerebella of these forms possess extensive complex foliation. These brain patterns are compared with the brain organization of Holocephali, and I conclude that the holocephalans are a sister radiation of the elasmobranchs. Comparisons with bony fish and land vertebrates suggest that elasmobranchs have independently developed complex pallial fields and cerebellar foliation as a result of parallel evolutionary trends.

INTRODUCTION neural features unique to any given ver- tebrate radiation and thus fail to consider One of these simple vertebrates is rep- resented by a selachian of the modern seas, the specific neural changes that are adap- somewhat specialized in certain directions, of tive. course, but retaining, withal, much of the ar- Thus I believe a major task of compara- chaic nervous organization from which higher tive neurobiology is to sample brain varia- brains have gradually evolved. Houser, 1901 tion among living taxa and to recognize

In the past, most comparative I am extremely grateful to Dr. Louise Luckenbill- neuroanatomical studies were framed Edds, Mr. Leonard Compagno, and the Steinhart within typological considerations. The Aquarium for furnishing some of the specimens used brains of non-mammalian vertebrates in this study. Mr. Daniel Moreno and the staff of the Cleveland Aquarium devoted considerable time and were assumed to represent earlier, thus effort to the initial phase of my shark work. I have simpler, stages in the evolution of mamma- been fortunate to utilize facilities at the Duke Univer- lian brains. Attention was focused on rec- sity Marine Laboratory, and at the Marine Field ognizing neural features common to all Station (University of Delaware College of Marine vertebrates, and on describing the Studies) where Dr. Robert Boord and I have spent many pleasant, hopefully productive hours studying "phylogenetic level" of different brain di- shark brains. I have benefited greatly from the assis- visions. Neural features common to all tance of Mr. Gerrit Klay of Marathon, Florida, whose vertebrates clearly tell us little about spe- enthusiasm for sharks is exceeded only by his talent cific adaptations and thus evolution. At for collecting and maintaining these animals. His- best, features common to widely divergent tological preparations were done by Mrs. Alice Hartman, Mr. Ronald Nicholes and Mrs. Elizabeth species offer clues to the initial adaptation Reed; and art work by Mr. Donald Luce. Dr. Mark and the origin of vertebrates. Braford read the manuscript and provided many helpful suggestions. Dr. Timothy Neary also read the Similarly, it is fallacious to characterize manuscript and applied his considerable expertise in the brains of various vertebrate species as helping me with the statistical calculations. This work points on a linear, simple-to-complex scale was supported by grants from the National Institutes with mammalian brains at the acme. Such of Health (NS11006) and the National Science Foun- unilinear hierarchies fail to recognize the dation (GB-40134).

411 412 R. GLENN NORTHCUTT common morphological patterns and their MATERIALS AND METHODS adaptive significance, rather than to recon- struct the probable phylogenetic history of Gross anatomy brains "from fish to man." Only by sampl- The genera utilized in this analysis are ing the existing variation can common listed in Table 1. Those examined by the adaptive patterns be recognized. Once author are indicated by an asterisk, while such patterns are identified, hypotheses published accounts exist for all other gen- regarding their biological value can be era listed. formulated and tested. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 In this paper, the gross variation in Brain:body data elasmobranch brains is described with par- ticular emphasis on sharks. Two patterns Brains of a number of elasmobranch or levels of neural organization are recog- species (Table 2) were perfused or fixed by nized, and our present knowledge regard- emersion in AFA. All specimens were ing shark CNS organization is reviewed. adults based on gonadal tissues and re- Neural similarities possibly due to parallel ported adult body lengths. AFA fixation evolution among sharks, birds and mam- results in an 8-9% reduction in brain mals are noted. weight, and all brain weights reported are

TABLE 1. Elasmobranch CNS in literature or examined by author. (Those examined by author are indicated by an asterisk.) Class Chondrichthyes *Etmoptenis hihanus Subclass Holocephali Callorhynchus antarcticus *Squalus acanlhms (Kuhlenbeck and Niimi, 1969) (Johnston, 1911; Holmgren, 1922; Backstrom, 1924; Leghissa, 1962; Chimaera monstrosa Smeets and Nieuwenhuys, 1967) (Holmgren, 1922; Faucette, 1969) Deania rostrata *Hydrolagus colliei (Okada rf a/., 1969) (Kuhlenbeck and Niimi, 1969) Centroscylhum ritteri Subclass Elasmobranchii (Okada et al., 1969)

Superorder Squalomorphii Order Pristiophoriformes

Order Hexanchiformes Pristiophorus japonicus (Okada et al., 1969) Chlamydoselachus anguineus (Masai, 1961) Superorder Batoidea Hexanchus (KlapperseJa/., 1936) Order Rajiformes

*Notorynchus maculatus *Rhinobatos produclus

Heptraruhias *Platyrhinoidis triseriata (Johnston, 1911; Backstrom, 1924) Raja clavata Order Squaliformes (Johnston, 1911; Backstrom, 1924; Leghissa, 1962; Veselkin, 1965) Eimopterus lucifer (Okada «* a/., 1969; Masai et *Raja eglanteria al., 1973) ELASMOBRANCH CNS ORGANIZATION 413

TABLE 1. Elasmobranch CNS in literature or examined by author, (con't.)

Order Pristiformes Lamna (Klapperse(a/., 1936) No known literature Order Carcharhiniformes Order Torpediniformes Scyliorhinus caniculus Torpedo ocellata (Haller, 1898; Edinger, 1901; (Backstrom, 1924; Hugosson, 1955; Johnston, 1911; Dart, 1920; Leghissa, 1962; Bruckmoser, 1973; Backstrom, 1924; Beccari, Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 Bruckmoser and Dieringer, 1973; 1930; Bruckmoser and Platte(a/., 1974) Dieringer, 1973; Platted al., 1974; Smeets and Nieuwenhuys, 1976) Order Myliobatiformes *Scyhorhinus retifer *Potamotrygon motoro Scyliorhinus stellans Myliobatis aquila (Johnston, 1911; Backstrom, 1924; (Johnston, 1911; Kappers el al., Leghissa, 1962) 1936) *Mustelus canis Superorder Squatinomorphii (Shaper, 1898; Houser, 1901; Backstrom, 1924; Gerlach, 1947; McCready and Boord, 1976) No known literature Mustelus laems Superorder Galeomorphii (Backstrom, 1924; Leghissa, 1962; P\att etal., 1974) Order Heterodontiformes *Heterodontus francisci *Triakis scyllia

Heterodontus japonicus *Galeocerdo cuivieri (Masai, 1962; Kusunoki el al., (Ebbesson and Ramsey, 1968) 1973) Scohodon Order Orectolobiformes (Johnston, 1911; Masai, 1962) *Ginglymostoma cirratum (Ebbesson and Ramsey, 1968; *Carcharhinus floridanus Ebbesson and Heimer, 1970; Ebbesson and Schroeder, 1971; *Carcharhinus leucas Ebbesson, 1972; Cohen, et al., 1973; Ebbesson and Campbell, 1973 *Carcharhinus milberti Schroeder and Ebbesson, 1974; Schroeder and Ebbesson, 1975) *Apnonodon isodon

Order Lamniformes *Negaprion brevirostris (Tester, 1963; Graeber and Ebbesson, 1972a) Odontaspis *Pnonace glauca (Okada e< a/., 1969) (Aronson, 1963; Okada etal, 1969) Mitsukurina owstoni (Masai et al., 1973) *Sphyrna lexvini Alopias *Sphyrna tiburo (Okada et al., 1969) Sphyrna zygaena (Okada etal., 1969) Carcharodon carcharias (Gilbert, 1963) Isurus oxyrinchus (Gilbert, 1963; Okada et al, 1969) 414 R. GLENN NORTHCUTT not corrected for this reduction. Reported they nor the meninges, blood vessels or body weights are from fresh, unfixed choroid plexus of the fourth ventricle were material. Additional data were utilized included in the brain division weights. from values cited by Crile and Quiring Each brain division was blotted im- (1940) and Ridet et al. (1973) and are mediately prior to weighing. A Mettler noted in Table 2. analytical balance (Model H10) was used Data for relative development of major for all measurements. The accuracy of ten brain divisions (Fig. 4) were obtained by repeated measurements on small brain di-

immersing AFA fixed brains in fixative visions (0.003 g) was ± 1.6%. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 and dissecting the following brain divisions for weighing: olfactory bulbs, telencepha- Histology lon (including olfactory peduncles), diencephalon, mesencephalon, cerebel- The brains of embryos as well as adults lum, and medulla. The caudal boundary were fixed in AFA and dissected from the of the telencephalon was considered to be heads, embedded in paraffin and sec- a plane extending from the rostral border tioned at 15 JK in the transverse plane. of the optic chiasm. The caudal boundary Sections were stained by Bodian silver im- of the diencephalon was considered to be a pregnations, Cresyl violet or Klu'ver- plane extending from the rostral pole of Barrera methods. Brain sections illus- the optic tectum to the caudal pole of the trated in Figures 5-7 are from late fetal infundibulum. The optic nerves were not stages of Squalus (9.5 cm snout-vent included in the weight of the diencepha- length) and Mustelus (13.5 cm snout-vent lon, but were transected within 2 mm of length). Individuals at this stage of de- the chiasm. The cerebellum was consi- velopment possess all cell groups recogniz- dered to include all tissue lying dorsal to a able in the adults, but the cell groups and rostro-caudal transection just below the their boundaries are not obscured by ventral lip of the cerebellar auricle. The further brain enlargement (24 fold) that caudal boundary of the medulla was set at subsequently occurs. the level of the first complete cervical spi- nal nerve. All cranial nerves were tran- sected at the base of the brain, and neither RESULTS

TABLE 2. Elasmobranch brain:body data. General considerations Brain Body The brains of sharks exhibit a wide wgt. wgt. range of variation, but generally speaking Species in g in kg they fall into two major patterns of de- Aprionodon isodon (Al) 18.75 10.87 velopment (Fig. 1). Hexanchiform, Carcharhinus falaformis (CF) 43.32 36.24 squaliform and pristiophoriform sharks Carcharhinns leucas (CL) 54.36 83.80 possess a non-convoluted corpus of the Dasyatis sabina (DS) 76.52 17.58 cerebellum, well developed and dorsally (Crile and Quiring, 1940) Galeocerdo cuvieri (G) 107.50 200.00 exposed optic tecta and a poorly de- Crile and Quiring, 1940) veloped telencephalon (Fig. 1A). Gtnglymostoma arratum (GC) 31.65 45.30 Galeomorph sharks as a rule possess a Heterodontusfrancisci (HF) 4.30 2.93 convoluted corpus of the cerebellum with Mustelus canis (MC) 8.31 6.50 Odonlaspis laurus (OT) 82.55 123.00 hypertrophy leading to asymmetry in (Crile and Quiring, 1940) many families (orectolobids, lamnids, car- Potamotrygon motoro (PM) 4.51 0.63 charhinids and sphyrnids), optic tecta Platyrhinoidis tnseriata (PT) 1.37 2.03 overlapped by the cerebellum, and hyper- Raja eglantena (RE) 1.66 1.10 trophy of the telencephalon (Fig. IB). Ex- Rhinobalos produclus (RP) 9.11 3.62 ceptions to these two general trends do Squalus acanthias (SA) 3.87 4.20 Sphyrna lewini (SL) 59.88 55.71 occur. Scyliorhinids possess the complex Scyliorhinns caniculus (SC) 1.38 0.57 telencephalic development characteristic (Ridet et al., 1973) of other galeomorphs, but their cerebella ELASMOBRANCH CNS ORGANIZATION 415 sphyrnid sharks. What little data presently alln exists on the myliobatiforms strongly Plln suggest that the advanced members of this group may possess the most complex neural development among living elasmo- mob branchs. The chimaeras of holocephalans possess brains very similar to those of elasmo-

branchs, but are clearly separated from Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 them by a number of neural characters. All chimaeras possess sessil olfactory bulbs arising from the rostral pole of the telen- cephalon, while those of elasmobranch s arise laterally and are connected by elon- gated olfactory peduncles (tracts). The chimaeras lack a specialized hypertrophy of the mid-dorsal telencephalic roof, termed the central nucleus, as well as pal- lial formations bridging the two telen- cephalic hemispheres (Fig. 5)—two fea- tures which characterize all living elasmo- branchs. Finally, all chimaeras examined to date possess a specialized elongated telen- FIG. 1 Dorsal view of the brain of an hexanchiform cephalon medium whose length may be shark, Notorynchus maculatus (A) and a car- half that of the entire brain. charhiniform shark, Sphyrna tiburo (B) illustrating the range of shark brain variation, al 11, anterior lateral line lobe; alln, anterior lateral line nerve; c, corpus Brain size of cerebellum; en, central nucleus of telencephalon; lob, lateral division of the olfactory bulb; lp, lateral The difference in brain volume or pallium; mob, medial division of the olfactory bulb; o, terminal nerve; oe, olfactory epithelium (sac); ot, weight among different radiations is one optic tectum; plln, posterior lateral line nerve. Bar important measure of brain evolution. Di- scales equal 1 cm. rect comparisons are obviously compli- cated by the wide range of body sizes are non-convoluted like those of encountered among vertebrates. However, squalomorph sharks. Heterodontus is a data for such comparisons can be obtained problematic taxon. Its general brain de- by making use of the allometric relation velopment suggests close links with the between brain weights and body weights squalomorph sharks with which it has fre- expressed by the equation E=kPa in which quently been grouped. However, Com- E and P are brain and body weights, re- pagno (1973) has assigned Heterodontus to spectively, and k and a are constants. The the galeomorph sharks on the basis of a logarithmic transformation of the above number of cranial and pectoral fin charac- equation becomes log E = log k + a log P. ters. This is a linear equation in log E and log P The batoids possess complex telenceph- with a slope a termed the coefficient of alic organization characterized by hyper- allometry. This coefficient is a measure of trophy and cellular migrations that reduce the rate of change in brain weight or the lateral ventricles to mere vestiges. volume for a given change in body weight Rajiforms and Torpediniforms possess or volume. Log k is the intercept, often slightly convoluted cerebella, while the termed the index of cephalization. Gould Myliobatiforms appear to have indepen- (1966, 1971) and Jerison (1973) have dis- dently evolved large brain size and com- cussed a number of problems associated plexly convoluted cerebella whose asym- with the concept of such an index, one of metry parallels that of carcharhinid and the most important being that it is a nu- 416 R. GLENN NORTHCUTT merical quantity whose biological sig- nificance is unknown. Fortunately, Jerison (1970, 1973) has critically reviewed the s problem of brain:body indices and has at (9 suggested that the philosophy of curve Z fitting based on the assumption that sam- I O 10 ples represent random deviations of a true UJ mean caused by measurement error, PM Z

should be replaced by a curve-fitting pro- < Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 cedure that assumes the samples represent a region within which a set of brain:body data exist for a taxon. Such a region is represented by a principal axis defined for 1 10 100 a set of points distributed rectangularly in BODY WEIGHT IN KILOGRAMS the area within which they lie. This area FIG. 3 Detailed elasmobranch minimum convex and its principal axis can be enclosed by a polygon illustrating position of various taxa. In- minimum convex polygon which then terspecific coefficient of allometry is 0.76 with a coefficient of determination of 0.86. Al, Aprionodon maps the area of the sample set. isodon; CF, Carcharhinus falciformis; CL, Carcharhmus Figure 2 illustrates Jerison's (1970) leucas; DS, Dasyatis sabina; G, Galeocerdo cuvieri; GC, Ginglymostoma cirratum; HF, Heterodontusfrancisa; MC, evaluation of the avian, osteichthyan and Mustelns cams; OT, Odontaspis taurus; PM, Potamotry- mammalian data collected by Crile and gon moloro; PT, Platyrhinoidis trisertata; RE, Raja eglan- Quiring (1940). The stippled polygon en- tena; RP, Rhinobatos productus; SA, Squalus acan- closes the elasmobranch brain:body data thias; SC, Scyhorhmus camculus; SL, Sphyrna lewmi. reported by Ebbesson and Northcutt (1976) as well as new data I have collected. same range of variation in brain size as do All the elasmobranch data are listed in the other major vertebrate classes. Table 2, and a more detailed plot is pre- These extremely high brain:body ratios sented in Figure 3. might be explained by elasmobranch car- The data in Figures 2 and 3 clearly tilaginous skeletons being lighter than demonstrate that elasmobranchs possess bony skeletons thus shifting the polygon large brains comparable to those of many upward. However, my analysis of Mustelus birds and mammals. Furthermore, elas- canis reveals that the skeleton accounts for mobranchs possess approximately the 15% of the total body weight, a figure that falls within the range of skeletal weight percentages for other vertebrates. Thus a 10,000- minimum correction factor of 15 fold would be necessary for elasmobranchs to 000 be placed on the same principal axis as / other anamniotic vertebrates. 100 / 1o / A The elasmobranch coefficient of al- z /•-'"Jm 10- lometry is also very high compared to that for other vertebrates. Based on the data >

WEIGH 1- presented in Table 2, I determined an overall elasmobranch coefficient of al- AIN ac 1- eo lometry (a) of 0.76 with a coefficient of determination (r2) of 0.86. The coefficient 01 of allometry for the sharks in this sample is 001 01 1 I 10 100 1,000 10.000 100.000 2 BODY WEIGHT IN KILOGRAMS 0.75 (r =0.96), while the coefficient for the skates and rays is even higher (a=1.04; FIG. 2 Brain and body weights for four vertebrate r2=0.67). Coefficients of allometry range classes expressed as minimum convex polygons after from: 0.63-0.65 for mammals, 0.56-0.60 Jerison (1973). Stippled polygon encloses elasmo- branch brain :body ratios and overlaps polygons for for amphibians, and 0.65 for- teleosts bony fishes, birds, and mammals. (Bauchot et al., 1976). Similar elasmo- ELASMOBRANCH CNS ORGANIZATION 417

branch data was reported by Bauchot et al. comparable to teleosts and amphibians, (1976). These workers reported an while the advanced galeomorph sharks elasmobranch coefficient of 0.939 but did possess forebrain development compara- not calculate separate coefficients for ble to that of endothermic vertebrates (Eb- m. sharks and rays. An error was made in besson and Northcutt, 1976). Similar data their calculations (personal communica- on advanced batoids does not exist, and we tion); and using the data listed in their do not know if these taxa possess relative Table 1, I calculated an overall elasmo- brain development similar to that of car- 2

branch coefficient of 0.80 (r =0.74), a charhinids and sphyrnids. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 shark coefficient of 0.73 (r2=0.78) and a 2 skate and ray coefficient of 1.38 (r =0.83). CNS organization These figures agree with my own data, and together they strongly suggest that the In elasmobranchs as in other vertebrates batoids possess iso- or positive allometry, a the greatest changes in the evolution of the condition thus far reported only for brain occur primarily in the roof of the hominids (Jerison, 1973). fore-, mid-, and hindbrain. The myelen- At present the sample of different taxa is cephalon or medulla is much more conser- too incomplete to clearly recognize trends vative, and homologous sensory and motor within the elasmobranchs that may have nuclei are easily recognized among verte- increased brain size (Fig. 3). However, brates. I have not examined medullar vari- comparison of species of comparable body ation in elasmobranchs, and it is beyond size such as Squalus acanthias, Mustelus canis the scope of this paper to report on the and Sphyrna tiburo suggests that the organization of this region. However, squalomorph sharks may be characterized Smeets and Nieuwenhuys (1976) recently by low brain:body ratios and that the described the brain stem of Squalus and evolution of the galeomorph sharks is Scyliorhinus and reviewed the earlier litera- characterized by a 1-3 fold increase in ture. Readers are referred to this excellent brain size. Similarly, the batoids range work for histological details regarding the throughout the polygon, but the rajiforms organization of the brain stem. are characterized by low brain:body ratios The telencephalon of elasmobranchs, and the more advanced myliobatiforms by like that of other verebrates except for the highest brain:body ratios presently actinopterygian fishes, consists of paired known for elasmobranchs. cerebral hemispheres formed by evagina- Further study will certainly change the tion and a more caudal telencephalon present boundaries of the elasmobranch medium representing the portion of the polygon as the samples to date are ex- telencephalon not carried laterally into the tremely small. Data on the advanced evaginating hemispheres. In all verte- batoids (myliobatids, rhinopterids and brates the olfactory bulbs arise by a secon- mobulids), in particular, may reveal even dary evagination from the cerebral hemi- higher brain:body data. spheres. Such is the case in elasmobranchs; The common conception that elasmo- however the olfactory bulbs and their branchs are small-brained creatures is peduncles (olfactory tracts) arise far later- clearly false, but how are the brains of ally (Fig. 1). The olfactory bulbs of elas- elasmobranchs organized? Do these ani- mobranchs possess distinct medial and lat- mals possess massive lower brain centers, eral divisions which receive olfactory in- or do they possess well developed fore- nervation from different parts of the olfac- brains like birds and mammals? An tory organ (Norris and Hughes, 1920). In analysis of the data presented in Figure 4 Squalus the medial division of the olfactory on the relative development of the major bulb appears to receive input from the divisions of the brain in a number of medial and lateral lamellae of the olfactory elasmobranchs reveals a wide range of organ, while the lateral division of the variation. Species toward the left of the olfactory bulb receives input from only the figure possess forebrain development lateral lamellae of the olfactory organ. 418 R. GLENN NORTHCUTT

OLFACTORY BULBS 7 6 1 3| 31 7

24 32 37

TELENCEPHALON 31 Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 35 45 51 32 52 7 7 DIENCEPHALON 15 6 14 13 MESENCEPHALON 10 18 4 20 17 11 13 21 14 6 CEREBELLUM 16 19 13 13 19 28 21 28 28 MEDULLA 20 17 18 17 12

Weight brain subdivisions as percent of total brain FIG. 4 Relative development of major brain divi- dogfish), Rhinobatos productus (guitarfish), lsurus sions in several cartilaginous fishes: Hydrolagus collwi oxyrinchus (mako shark), Pnonace glauca (blue shark), (ratfish), Squalus acanthias (spiny dogfish), Raja eglan- Carcharhinus milberti (sandbar shark), Sphyrna lewini tena (clearnosed skate), Mustelus cants (smooth (scalloped hammerhead shark).

However, Daniel (1934) argued that the zones, and the reduction in ventricular size medial and lateral divisions of the bulb that occur in galeomorph sharks (Figs. received input from the medial and lateral 5B,D,F). Holmgren (1922) stressed lamellae of the olfactory organ respective- examination of the embryology of sharks ly. This certainly appears to be the case in as a fruitful approach to these problems, Sphyrna (Fig. IB). Experimental studies are and fortunately he chose one of the needed to resolve this discrepancy. simplest shark brains {Squalus acanthias) to Until recently it was assumed that all study. I have similarly examined embryos parts of the elasmobranch telencephalon of Squalus and the telencephalic histology received direct secondary olfactory fibers of a number of squalomorph adults. Based from the olfactory bulb (Backstrom, 1924; on these studies I believe that elasmo- Kappers et al., 1936; Aronson, 1963). branchs, like many other vertebrates, pos- However, new experimental studies on sess three main roof or pallial formations both sharks and skates reveal that the (Figs. 5A,C,E). The lateral pallium receives olfactory telencephalic centers are as re- the main olfactory input and is probably stricted in these groups as in land verte- homologous to the lateral pallium or cor- brates (Ebbesson and Heimer, 1970; tex of land vertebrates. The dorsal pallium Bruckmoser and Dieringer, 1973; Ebbes- is divided into inner and outer laminae son and Northcutt, 1976). Two main telen- (Figs. 5A,C). In elasmobranchs the outer cephalic targets receive ipsilateral second- lamina, unlike that of other vertebrates, ary olfactory input: the lateral pallium continues across the midline forming an (lateral olfactory area) and the lateral por- interhemispheric bridge. The inner tion of the area superficialis basalis. lamina undergoes extensive evolution in Further analyses of the number of dis- elasmobranchs. In Notorynchus the inner tinct telencephalic areas and their possible lamina of the dorsal pallium is poorly homologies with other vertebrates have developed, forming only a slight bulge in been handicapped by the extensive cell the roof of the lateral ventricle. In squalids migrations, the loss of distinct cell free the inner lamina is better developed and Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021

FIG. 5 Photomicrographs of comparable transverse sharks. Bar scales equal 2 mm. as, area superficialis sections through rostral, mid and caudal levels of the basalis; en, central nucleus; dp, dorsal pallium; fb, right telencephalic hemisphere of the spiny dogfish, forebrain bundles; Is, lateral septum; lp, lateral pal- Squalus acanthias, (A,C,E) and the smooth dogfish, lium; mp, medial pallium; ms, medial septum; ob, Mustelus canis (B,D,F) illustrating the reduction in olfactory bulb; pa, preoptic area of hypothalamus; st, lateral ventricles and marked hypertrophy of the roof (pallial) neural groups that occur in carcharhiniform 420 R. GLENN NORTHCUTT caudally forms a thickened mass termed bly homologous to parts of the amygdaloid the central nucleus by Ebbesson (1972) complex (Northcutt, 1974; Northcutt and (Fig. 5E). In squalids the central nucleus Braford, 1977). does not fuse at the midline but remains a The telencephalic nomenclature and distinct and separate cell group. In homologies proposed here are viewed as a M galeomorphs the central nucleus is exten- series of hypotheses, not established facts, sively hypertrophied, resulting in a mas- and must be tested by further experimen- sively thickened interhemispheric bridge tal anatomical and histochemical studies.

(Figs. 5D,F). The central nucleus receives The diencephalon of elasmobranchs Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 substantial ascending sensory projections consists of three divisions: epithalamus, from the thalamus of the diencephalon thalamus, and hypothalamus. The (Ebbesson and Schroeder, 1971; Ebbesson, epithalamus is formed by the habenular 1972; Schroeder and Ebbesson, 1974). nuclei, habenular commissure and a com- This pallial center is now known to receive plex series of afferent and efferent path- visual, lateralis and trigeminal sensory in- ways (stria medullaris complex) related to puts (Cohen et al, 1973; Platt et al., 1974; the habenular nuclei. Little variation is Ebbesson, personal communication). The discernible among the various species. The topography and ascending thalamic pro- habenular nuclei consist of dorsal and ven- jections to the central nucleus strongly tral divisions (Figs. 6A,B). The ventral suggest that this center and the dorsal habenular nucleus fuses across the midline pallium are homologous to parts of isocor- below a much shortened habenular com- tex (neocortex) in land vertebrates. missure. The main efferent pathway of the A more medial pallial group (mp) bor- habenular nuclei (fasciculus retroflexus) ders the dorsal pallium in Squalus (Figs. terminates caudally in the interpeduncular 5A,C), and it also fuses across the in- nucleus (Fig. 7C). No experimental studies terhemispheric bridge. Nothing is pre- exist on the afferent pathways to the sently known regarding its connections, habenula in elasmobranchs. but the topography of the pallial forma- The thalamus of elasmobranchs is di- tion strongly suggests that it is homologous vided into dorsal (dt) and ventral (vt) divi- to the medial pallium (hippocampal com- sions (Figs. 6,7). The thalamus of plex) of land vertebrates. squalomorph sharks is similar to that of The telencephalic floor or subpallium is many other anamniotic vertebrates, but far more difficult to analyze. Two distinct the thalamus of the galeomorph sharks is cell masses are recognized ventromedially characterized by marked thickening of the (Fig. 5A) and probably represent the me- thalamic wall and considerable migration dial and lateral septal nuclei. In terms of and differentiation of its cellular nuclei. their topography and structure they Retinal and tectal afferents constitute the closely resemble similarly named nuclei in major inputs to both dorsal and ventral amphibians and reptiles. thalamic divisions. Experimental studies Finally, the ventrolateral telencephalic on the retinal projections in sharks (Ebbes- wall contains a number of cell groups son and Ramsey, 1968; Graeber and Eb- which I have tentatively labeled the besson, 1972a; Northcutt, 1976) reveal striatum on the basis of their topography that the optic projections are entirely and high acetylcholinesterase activity (un- crossed, and that both dorsal and ventral published observations). thalamic nuclei receive optic terminals. The telencephalon medium (Figs. 5E,F) The cell groups (dt, vt) at the tip of the is formed by the ascending and descend- arrows in Figure 6A both receive heavy ing forebrain bundles (fb), the preoptic optic inputs in Squalus (Northcutt, 1976). area (pa), and an unlabeled cell complex However the retinal terminals are re- termed nucleus taeniae by earlier workers stricted to the outer half of the cellular (Holmgren, 1922; Kappers et al, 1936). plates. These same thalamic targets are Based on our knowledge of this region in much enlarged and subdivided in most other vertebrates, nucleus taeniae is possi- galeomorph sharks. The ventral thalamic Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021

FIG. 6 Photomicrographs of comparable transverse thalamus; fb, forebrain bundles; h, habenular nuc- sections through rostral and caudal levels of the right lei; he, habenular commissure; itc, intertectal commis- diencephalon of Squalus acanthias (A,C) and Mustelus sure; on, optic nerve; ot, optic tectum; p, periven- canis (B,D) illustrating the hypertrophy of the tricular zone of optic tectum; pa, preoptic area of thalamic wall and extensive neural migrations that hypothalamus; s, superficial zone of optic tectum; sc, occur in carcharhiniform sharks. Bar scales equal 2 subcommissural organ; sp, superficial pretectal nuc- mm. c, central zone of optic tectum; dt, dorsal leus; vt, ventral thalamus. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021

t vt

ce

IC

i 1 •* I 1 FIG. 7 Photomicrographs of comparable transverse optic tectum; ce, corpus of cerebellum; hy, caudal sections through mid and caudal levels of the right hypothalamus; ic, intercollicular nucleus; np, nucleus mesencephalon of Squalus acanthias (A,C) and Mus- profundus mesencephali; p, periventricular zone of teluscanis (B,D) illustrating hypertrophy of tectal roof optic tectum; s, superficial zone of optic tectum; t, and migration of tectal periventricular zonal neurons mesencephalic tegmentum; ts, torus semicircularis; that occur in carcharhiniform sharks. Bar scales equal vt, ventral thalamus; III, oculomotor nucleus. 2 mm. bon, basal optic nucleus; c, central zone of ELASMOBRANCH CNS ORGANIZATION 423 retinal target continues caudally to reach consists of dorsal (optic tectum and torus the level illustrated in Figure 7A. However semicircularis) and ventral (tegmentum) the rostral dorsal thalamic retinal target is areas (Figs. 6,7). The optic tectum of replaced caudally by a series of nuclei sharks consists of multiple laminae or termed the pretectum. Two pretectal nuc- zones, but no agreement exists regarding lei receive retinal input, the superficial the exact number (Houser, 1901; Kappers pretectal nucleus (sp, Fig. 6C) and a etal., 1936; Leghissa, 1962; Schroeder and periventricular cell group immediately ad- Ebbesson, 1975). In Squalus and Mustelus I

jacent to the subcommissural organ (Fig. have recognized three zones: superficial, Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 6C). All of the thalamic and pretectal central, and periventricular (Figs. 6,7). nuclei receiving retinal input also receive The superficial zone consists of both fibers ascending tectal input (Ebbesson et al., and scattered cell bodies. The fibers of the 1972). Most of the remaining dorsal and superficial tectal zone were earlier thought ventral thalamic nuclei, medial to the to be optic fibers (Kappers et al., 1936), but thalamic and retinal recipient zones, re- more recent studies (Schroeder and Eb- ceive ascending cerebellar and spinal in- besson, 1975; Northcutt, 1976) have puts (Ebbesson et al., 1972; Ebbesson and shown that the optic fibers enter more Campbell, 1973). Thus the thalamus of deeply and turn dorsally to terminate in sharks receives a wide range of ascending the outer half of the optic tectum. The sensory pathways, and considerable sep- central zone consists of an outer dense aration of sensory modalities appears to cellular layer and an inner fiber layer. In exist. The thalamus of sharks is now Squalus the optic fibers course among the known to give rise to sizable ascending cells of the outer cellular layer, and termi- pathways that terminate primarily in the nate within this layer as well as in the central nucleus of the telencephalon (Eb- superficial zone. The outer cellular layer besson, 1972; Schroeder and Ebbesson, of the central zone contains the largest 1974). However, the main thalamic projec- number of neurons in the tectum of tion, unlike that of other vertebrates, is to Squalus and, according to Leghissa (1962), the contralateral telencephalic hemi- consists of pyramidal and bipolar cells. sphere. Heavy ascending thalamic projec- The inner fibrous layer of the central zone tions to the central nucleus suggest that contains scattered neurons, termed large thalamic hypertrophy in galeomorph multipolar cells by Leghissa, that send sharks is linked to hypertrophy of the their dendrites into the superficial zones telencephalic central nucleus and that and their axons deep and lateral into the these nuclei form the most rostral integra- tectal efferent tracts. The bulk of the inner tive centers of the ascending sensory layer of the central zone is composed of pathways arising throughout the central fibers that form the descending tectal ef- nervous system. ferents (Ebbesson, 1972). This fiber layer probably also contains ascending fibers At present little is known about the third carrying sensory information into the tec- division of the diencephalon, the hypo- tum as in other vertebrates. The tectum thalamus. It comprises a rostral preoptic projects rostrally into the pretectum and area (Fig. 6), a central or tubral area in- thalamus, terminating in nuclei that also cluding the inferior lobes (Fig. 7), and a receive retinal inputs, and caudally in the caudal or posterior hypothalamic area ipsilateral and contralateral medullar re- (Fig. 7C). Retinal projections are known to ticular formations (Ebbesson, 1972). the rostro-ventral preoptic area (Graeber and Ebbesson, 1972a; Northcutt, 1976), The periventricular tectal zone consists and telencephalic input to the preoptic of two to three cellular laminae separated area and inferior lobes has also been by fibrous layers (Figs. 6,7). Pyriform documented (Ebbesson, 1972). At present shaped cells predominate in this zone, and nothing is known regarding the efferent their apical dendrites branch dorsally into hypothalamic pathways. the central and superficial zones (Leghissa, The mesencephalon of elasmobranchs 1962). The axons of these cells arise from 424 R. GLENN NORTHCUTT the soma or a dendritic shaft and enter nent of the medial longitudinal fasciculus, either the tectal efferent tract or intertectal an important brain stem pathway involved commissure, or ramify in the central zone. in ocular and vestibular functions. More Considerable variation exists in the tec- caudally the oculomotor and trochlear tal lamination of sharks, but an insufficient nuclei are also located in the midbrain number of genera have been examined to tegmentum (Fig. 7). Finally, the inter- characterize major trends. In Sqxuilus (Fig. peduncular nucleus is seen ventrally (Fig. 7) and Scyliorhinus (Leghissa, 1962; Smeets 7). This nucleus receives input from the

and Nieuwenhuys, 1976) the central zone habenular nuclei via the fasciculus retro- Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 contains the highest number of neurons. flexus. While the output of the inter- However, in Ginglymostoma the highest peduncular nucleus in sharks is undeter- number of neurons is found in the super- mined, this nucleus forms extensive de- ficial zone (Schroeder and Ebbesson, scending medullar projections in other 1975). There is also considerable variation vertebrates. in the thickness or size of the tectum The cerebellum of elasmobranchs con- among sharks. Many galeomorph sharks sists of a central unpaired corpus and possess enlarged tecta, and the periven- laterally situated auricles (Fig. 1). Each tricular zone is reduced in these taxa. auricle is divided into a dorsomedial upper As the periventricular tectal zone is leaf and a ventrolateral lower leaf continu- traced laterally in sharks, the cellular ous with the acustico-lateralis region of the laminae lose their compactness and form a medulla. scattered nucleus termed the torus Earlier studies have emphasized that the semicircularis (Fig. 7C). The connections size of the corpus is correlated with body of this nucleus are unknown in sharks, but size and is thus related to somatic muscula- a similarly situated nucleus in other anam- ture (Kappers etal., 1936; Aronson, 1963), niotes is known to receive auditory (Page, but my own observations do not support 1970) and lateralis (Knudsen, 1976) input. this contention. Animals of the same size The tegmentum consists of several con- {e.g., Squalus acanthias, Mustelus canis and spicuous nuclei (Fig. 7). The lateral teg- Sphyrna tiburo) exhibit the total range of mentum is formed by a dorsally situated cerebellar complexity seen among sharks. nucleus profundus mesencephali which The distribution of complex cerebellar does not receive retinal input (Northcutt, foliation among elasmobranchs suggests 1976) but does appear to receive tectal that this condition has evolved a number fibers (Ebbesson et al., 1972). Its efferents of times independently. Chimerids and all are unknown. More ventrally a basal optic squalomorph sharks examined possess a nucleus forms the ventrolateral tegmental smooth corpus divided into anterior and floor (Fig. 7D). This nucleus receives optic posterior lobes (Figs. 1,8A), suggesting fibers from the contralateral eye, and its that this condition is ancestral for car- efferents are also unknown. In other ver- tilaginous fishes. A similar pattern is seen tebrates the basal optic nucleus appears to in heterodontids and scyliorhinids. How- project to the cerebellum. The central ever, lamniform and advanced car- tegmental region is occupied by the inter- charhiniform sharks possess a complexly collicular nucleus (Fig. 7) which receives convoluted corpus divided into three lobes spinal input (Ebbesson, 1972), and its ef- (Figs. 8C, 9). Batoids appear to have inde- ferents are also unknown. In other verte- pendently evolved a complex corpus. The brates this nucleus projects rostrally into rajoids and torpediniforms possess a non- the thalamus, forming an ascending soma- convoluted corpus, while the rhinobatoid tosensory pathway. corpus is divided into three lobes (Fig. 8B) as in many advanced sharks. The Medially and dorsally a nucleus in- myliobatiforms extend this trend and pos- terstitialis forms the rostral boundary of sess complex foliation as do .the car- the tegmentum (Figs. 7A,B). The afferents charhinid sharks. of this nucleus are unknown, but the axons of its cells form the most rostral compo- The functional significance of increased ELASMOBRANCH CNS ORGANIZATION 425 cerebellar volume in elasmobranchs is un- the auricle of the cerebellum, as do ves- known, but it is very likely related to an tibular fibers. Lesions of the auricle result increase in sensory inputs involved in in circus movements and locomotor im- motor control. Unfortunately, little infor- pairment (Aronson, 1963), but similar mation is available regarding sensory studies on the corpus have revealed no pathways to the cerebellum. Ascending clear-cut locomotor impairments. spino-cerebellar tracts to the corpus have Ebbesson and Campbell (1973) been demonstrated (Hayle, 1973), but di- examined the cerebellar efferents in rect lateralis projections to the corpus, Ginglymostoma and demonstrated both as- Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 described by earlier studies (Kappers el al., cending and descending cerebellar path- 1936), have not been confirmed experi- ways like those found in other vertebrates. mentally (Boord and Campbell, 1977). The Purkinje cells of the cerebellum of Boord and Campbell demonstrated that sharks, like those of other vertebrates, the lateral line nerves project directly to terminate on deep cerebellar nuclei; but

\

lcm

FIG. 8 Dorsal and midsagittal views of the cerebel- figure. A, anterior lobe; M, middle lobe; P, posterior lum in Mustelxts canis (A), Carcharinus milberti (B) and lobe. and Isurus oxyrinchus (C). Rostral is to the left of the 426 R. GLENN NORTHCUTT direct projections to the vestibular nuclei the trochlear and oculomotor nuclei and in or medulla, as suggested by earlier studies the posterior dorsal thalamus. Thus the (Kappers et al., 1936), were not confirmed. cerebellum possesses descending projec- The cerebellar nuclei terminate in the lat- tions, modulating the output of the reticu- eral and medial medullar reticular forma- lar formation to the cranial nerve motor tion, the red nucleus of the tegmentum, nuclei and to the spinal cord; and an Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021

1 cm FIG. 9 Dorsal and midsagittal views of the cerebel- Prionace glauca (C). Rostral is to the left of the figure. lum in Mustelus canis (A), Carcharinus milberti (B) andA, anterior lobe; M, middle lobe; P, posterior lobe. ELASMOBRANCH CNS ORGANIZATION 427 ascending brachium conjunctivum that relay. Until recently these neural features reaches dorsal thalamic levels. This last were considered exclusively mammalian projection is particularly interesting as it hallmarks; and their discovery in sharks, as suggests that thalamo-telencephalic relay well as in reptiles and birds, strongly of cerebellar afference may exist. In other suggests that isocortex may not be solely a vertebrates the thalamo-telencephalic pro- mammalian invention. jection is to a motor area of isocortex. While experimental studies have dem- Demonstration of such a pathway would onstrated that the optic tectum is a major further strengthen the probability of tel- visual center in sharks (Ebbesson and Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 encephalic involvement in direct motor Ramsey, 1968; Northcutt, 1976), Graeber control suggested by Ebbesson's demon- and Ebbesson (19726) have demonstrated stration of direct telencephalic pathways to that nurse sharks with extensive tectal medullar nuclei (Ebbesson, 1972). ablations learn visual discrimination tasks. This result suggests that other brain cen- DISCUSSION ters also mediate visual discriminations. Cerebellar size in elasmobranchs is Fifteen years ago elasmobranchs were clearly not correlated with body size in any characterized as primitive fishes with simple way. It is not true that only small small, simple brains and a decidedly limit- sharks possess smooth cerebella, while ed behavioral repertoire, particularly large sharks possess convoluted cerebella. when compared to teleosts or land verte- Complex, convoluted cerebella appear to brates. The telencephalon of sharks was characterize advanced galeomorph sharks believed to be dominated by olfactory in- and batoids irrespective of size. put, and its efferent projections were be- The cerebellum has traditionally been lieved to be primarily to epithalamic and considered to function as a coordinator of hypothalamic centers integrating and locomotion, but various vertebrates have mediating olfactory and gustatory be- revealed complex sensory representations haviors. The optic tectum was said to be in the cerebellar cortex. At present almost the highest visual center where integration nothing is known about such sensory in- of ascending somatic and visual sensations puts or their possible segregation in elas- occurred. The large cerebellum of sharks mobranchs. Studies of these inputs are was believed to be related to powerful, likely to provide the insights needed to well-coordinated trunk movements; yet understand cerebellar development in sharks were characterized as clumsy. elasmobranchs and the role of the cerebel- Ten years of experimental neurobiolog- lum in the integration of different sensory ical studies, and renewed interest in all modalities related to complex motor be- aspects of elasmobranch biology, are haviors. rapidly relegating these earlier conclusions Comparison of elasmobranch brain to the realm of myth. Elasmobranchs pos- evolution with that of other vertebrate sess large brains whose brain: body ratios groups suggests a number of similarities. fall within the range of birds and mam- Increase in brain size and differentiation mals. Their brains are not only large, but of roof areas receiving multiple sensory the relative development of major brain inputs clearly characterize elasmobranch divisions closely parallels that of birds and brain evolution. Similar trends charac- mammals (Ebbesson and Northcutt, 1976; terize advanced reptiles (Northcutt, 1977), Northcutt et al, 1977). teleosts (Northcutt and Braford, 1977), The olfactory projections in sharks are birds (Stingelin, 1958), and mammals restricted to a small portion of the telen- (Pearson and Pearson, 1977). cephalon as they are in land vertebrates One of the most striking trends in elas- (Ebbesson, 1972), and galeomorph sharks mobranch brain evolution is the elabora- and batoids possess enlarged telencephalic tion of the central nucleus of the telen- roof (pallial) regions that receive visual, cephalon (Figs. 1,5). Topographically and somatic and lateralis input via thalamic embryonically the central nucleus bears a 428 R. GLENN NORTHCUTT

number of similarities to the dorsal ven- elasmobranchs. In P. H. Greenwood, R. S. Miles, tricular ridge of sauropsid vertebrates or and C. Patterson (eds.), Interrelationships ojfishes, pp. 15-61. Academic Press, London. to parts of mammalian isocortex. All of Crile, G. and D. P. Quiring. 1940. A record of the these telencephalic structures arise from body weight and certain organ and gland weights dorsal and/or lateral telencephalic fields. of 3690 animals. OhioJ. of Sci. 40:219-259. They all receive various sensory inputs Daniel, J. F. 1934. The elasmobranch fishes. 3rd ed. from the thalamus, and each modality is University of California Press, Berkeley, California. Dart, R. A. 1920. A contribution to the morphology represented in a restricted portion of the of the corpus striatum. J. Anat., Lond. 55:1-26. telencephalic roof. The possibility that Ebbesson, S. O. E. 1972. New insights into the organi- Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 these diverse telencephalic specializations zation of the shark brain. Comp. Biochem. Physiol. are homologous to one another is tempt- 42A:121-129. ing, but it is much more likely that the Ebbesson, S. O. E. and C. B. G. Campbell. 1973. On the organization of cerebellar efferent pathways in elasmobranch pallial condition has inde- the nurse shark (Gmglymostoma cirratum). J. Comp. pendently evolved in parallel with the pal- Neur. 152:233-254. lia of advanced actinopterygian fishes and Ebbesson, S. O. E. and L. Heimer. 1970. Projections land vertebrates. Parallel evolution is par- of the olfactory tract fibers in the nurse shark ticularly probable if the squalamorph (Ginglymostoma cirratum) Brain Res. \l-Al-5b. Ebbesson, S. O. E., J. A.Jane, and D. M. Schroeder. sharks possess telencephalic characters 1972. A general overview of major interspecific which most closely resemble those of variations in thalamic organization. Brain, Behav. primitive cartilaginous fishes, a possibility Evol. 6:92-130. which seems very likely. Given the proba- Ebbesson, S. O. E. and R. G. Northcutt. 1976. ble monophyletic origin of gnathostome Neurology of anamniotic vertebrates. In R. B. Mas- terton, M. E. Bitterman, C. B. G. Campbell, and N. vertebrates sharing a common genome, Hotton (eds.), Evolution of brain and behavior in perhaps we are discovering that active ver- vertebrates, pp. 115-146. Lawrence Erlbaum As- tebrate predators have independently and sociates, Hillsdale, N. J. repeatedly evolved complex and very simi- Ebbesson, S. O. E. and J. S. Ramsey. 1968. The optic lar nervous systems to solve a similar array tracts in two species of sharks (Galeocerdo cuvien and Ginglymostoma cirratum). Brain Res. 8:36-53. of environmental problems. Ebbesson, S. O. E. and D. M. Schroeder. 1971. Connections of the nurse shark's telencephalon. Science 173:254-256. REFERENCES Edinger, L. 1901. Das Cerebellum von Scyllium canicula. Arch. Mikr. Anat. 58:661 .678. Aronson, L. R. 1963. The central nervous system of Faucette, J. R. 1969. The olfactory bulb and medial sharks and bony fishes with special reference to hemisphere wall of the Rat-fish, Chimaera. J. Comp. sensory and integrative mechanisms. In P. W. Gil- Neur. 137:377-406. bert (ed.), Sharks and survival, pp. 165-241. Heath, Gerlach, J. 1947. Beitrage zur vergleichenden Mor- Boston, Mass. phologie des Selachierhirnes. Anat. Anz. 96:79- Bauchot, R., R. Platel, and J.-M. Ridet. 1976. Brain- 165. body weight relationships in Selachii. Copeia Gilbert, P. 1976. The visual apparatus of sharks. In P. 1976:305-309. W. Gilbert (ed.), Sharks and survival, pp. 283-326. Backstrom, K. 1924. Contributions to the forebrain Heath, Boston, Mass. morphology in selachians. Acta Zool. 5:123-240. Gould, S. J. 1966. Allometry and size in ontogeny and Beccari, N. 1930. I centri tegmentali dell' asse cere- phylogeny. Biol. Rev. Cambridge Phil. Soc. brale dei Selaci. Arch. Zool., Ital. 14:411-429. 41:587-640. Boord, R. L. and C. B. G. Campbell. 1977. Structural Gould, S. J. 1971. Geometric similarity in allometric and functional organization of the lateral line sys- growth: A contribution to the problem of scaling in tem of sharks. Amer. Zool. 17:431-441. the evolution of size. Amer. Natur. 105:113-136. Bruckmoser, P. 1973. Beziehungen zwischen Struk- Graeber, R. C. and S. O. E. Ebbesson 1972a. Retinal tur und Funktion in der Evolution des Telencepha- projections in the Lemon Shark (Negapnon breviro- lon. Verh. d. Dtsch. Zool. Ges. 66:219-229. stris). Brain, Behav. Evol. 5:461-477. Bruckmoser, P. and N. Dieringer. 1973. Evoked Graeber, R. C. and S. O. E. Ebbesson. 19726. Visual potentials in the primary and secondary olfactory discrimination learning in normal and tectal- projection areas of the forebrain in Elasmo- ablated nurse sharks (Ginglymostoma cirratum). branchia. J. Comp. Physiol. 87:65-74. Comp. Biochem. Physiol. 42A: 131-140. Cohen, D. H., T. A. Duff, and S. O. E. Ebbesson. Haller, B. 1898. Vom Bau des Wirbelthiergehirns. I. 1973. Electrophysiological identification of a visual Salmo und Scyllium. Morphol. Jb. 26:345-641. area in shark telencephalon. Science 182:492-494. Hayle, T. H. 1973. A comparative study of spinocere- Compagno, L. J. V. 1973. Interrelationships of living bellar systems in three classes of poikilothermic ver- ELASMOBRANCH CNS ORGANIZATION 429

tebrates. J. Comp. Neur. 149:477-495. nificance. In N. Greenberg and P. MacLean (eds.), 149:477-495. The behavior and neurology of lizards. (In press) Holmgren, N. 1922. Points of view concerning fore- Northcutt, R. G., and M. R. Braford, Jr. 1977. New brain morphology in lower vertebrates. J. Comp. observations on the telencephalon of actinoptery- Neur. 34:391-459. gian fishes. In S. O. E. Ebbesson (ed.), Comparative Houser, G. L. 1901. The neurones and supporting neurology of the telencephalon. Plenum Press, New elements of the brain of a selachian. J. Comp. York. (In press) Neur. 11:65-175. Northcutt, R. G., T. J. Neary, and D. G. Senn. 1977. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021 Hugosson, R. 1955. Studien u'ber die Entwicklung Observations on the brain of the coelacanth, der longitudinalen Zellsaulen und der Anlagen der Latimena chalumnae: External anatomy and quan- Gehirnnervenkerne in der Medulla oblongata bei titative analysis. J. Morph. (In press) verschiedenen Vertebraten. Z. Anat. EntwGesch. Norris, H. W. and S. P. Hughes. 1920. The cranial, 118:543-566. occipital, and anterior spinal nerves of the dogfish, Jerison, H. J. 1970. Gross brain indices and the Squalus acanthias. J. Comp. Neur. 31:293-402. analysis of fossil endocasts. In C. R. Noback and W. Okada, Y., M Aoki, Y. Sato, and H. Masai. 1969. The Montagna (eds.), Advances in primatology, Vol. 1, The brain patterns of sharks in relation to habit. J. f. primate brain. Appleton-Century Crofts, New York. Hirnforsch. 11:347-365. Jerison, H. J. 1973. Evolution of the brain and intelli- Page, C. H. 1970. Electrophysiological study of audi- gence. Academic Press, New York. tory responses in the goldfish brain. J. Neurophys. Johnston, J. B. 1911. The telencephalon of selac- 33:116-128. hians. J. Comp. Neur. 21:1-113. Pearson, R. and L. Pearson. 1976. The vertebrate brain. Kappers, C. U. A., G. C. Huber, and E. C. Crosby. Academic Press, New York. 1936. The comparative anatomy of the nervous system, Platt, C. J., T. H. Bullock, G. Czeh, N. Kovacevic, Dj. including man. Macmillan, New York. Konjevic, and M. Gojkovic. 1974. Comparison of Knudsen, E. I. 1976. Topographical frequency rep- electroreceptor, mechanoreceptor, and optic resentation in the teleostean midbrain. Neurosci- evoked potentials in the brain of some rays and ence Absts. 2:23. sharks. J. Comp. Physiol. 95:323-355. Kuhlenbeck, H. and K. Niimi. 1969. Further observa- Ridet, J. M., R. Bauchot, C. Delfini, R. Platel, and M. tions on the morphology of the brain in the Thireau. 1973. L'encephale de Scyliorhinus camcula holocephalian elasmobranchs Chimaera and Cal- (Linne 1758) (Chondrichthyes, Selacii, Scyliorhini- lorhynchus. J. f. Hirnforsch. 11:267-314. dae). Recherche d'une grandeur de reference pour Kusunoki, T., Y. Tsuda, and F. Takashima. 1973. des etudes quantiatives. Cahiers Biol. Marine Ros- The chemoarchitectonics of the shark brain. J. f. coff 14:11-28. Hirnforsch. 14:13-26. Schroeder, D. M. and S. O. E. Ebbesson. 1974. Leghissa, S. 1962. La struttura della corteccia Nonolfactory telencephalic afferents in the nurse mesencefalica dei ciclostomi selaci ed urodeli. Ac- shark (Ginglymostoma arratum). Brain, Behav. Evol. cademia delle Scienze Dell' Istituto Di Bologna 9:121-155. Classe Di Scienze Fisiche 9:123-152. Schroeder, D. M. and S. O. E. Ebbesson. 1975. Masai, H. 1961. On the brain pattern of Chlamy- Cytoarchitecture of the optic tectum in the nurse doselachus anguineus. Yokohama Medical Bulletin shark. J. Comp. Neur. 160:443-462. 12:231-238. Shaper, A. 1898. The finer structure of the selachian Masai, H. 1962. On the external form of the brain of cerebellum (Mustelus vulgaris). J. Comp. Neur. Heterodontus japonicus. Yokohama Medical Bulletin 8:1-20. 13:249-257. Smeets, W. J. A. J. and R. Nieuwenhuys. 1976. Masai, H., Y Sato, and M. Aoki. 1973. The brain of Topological analysis of the brain stem of the sharks Mitsukunna owstoni. J. f. Hirnforsch. 14:493-500. Squalus acanthias and Scyliorhinus canicula. J. Comp. McCready, P. J. and R. L. Boord. 1976. The topog- Neur. 165:333-368. raphy of the superficial roots and ganglia of the Stingelin, W. 1958. Vergleichend morphologische Unter- anterior lateral line nerve of the smooth dogfish, suchungen am Vorderhirn der Vbgel auf cytologtscher Mustelus canis. J. Morph. 150:527-538. und cytoarchitecktonischer Grundlage. Verlag Helbing Northcutt, R. G. 1974. Some histochemical observa- & Lichtenhahn, Basel, Switzerland. tions on the telencephalon of the bullfrog, Rana Tester, A. L. 1963. Olfaction, gustation, and the catesbeiana Shaw. J. Comp. Neur. 157:379-390. common chemical sense in sharks. In P. W. Gilbert Northcutt, R. G. 1976. Retinofugal pathways in fetal (ed.), Sharks and survival, pp. 255-282. Heath, Bos- dogfish pups, Squalus acanthias: An autoradio- ton, Mass. graphic study. Anat. Rec. 184:489. Veselkin, N. P. 1965. Electrical responses in skate Northcutt, R. G. 1977. Forebrain and midbrain or- brain to photic stimulation. Fed. Proc. Trans. Supp. ganization in lizards and its phylogenetic sig- 24:368-370. Downloaded from https://academic.oup.com/icb/article/17/2/411/163619 by guest on 30 September 2021