A Comparison of the Size of a n Auditory Nucleus - (n. mesencephalicus lateralis, pars dorsalis) with the Size of the Optic Lobe in Twenty-seven Species of Birds'

STANLEY COBB Department of Neurology and Psychiatry, Harvard Medical School, Boston, Massachusetts and t h e M u s e u m of Comparative Zoology, Hnrvard University, Cambridge, Massachusetts; a n d t h e Luboratory of Psychiatric Research, Massachusetts General Hospital, Boston, Massachusetts

Quantitative methods have been used in the study of the comparative anatomy of the avian brain by only a few investigators. Three recent contributions are from Port- mann's laboratory in Easel (Portmann, '46; Fritz, '49; Stingelin, '58), from Munich (Winter, '63) and one from the United States (Cobb, '60). Two older papers are by Bumm (1883) and Turner (1891).

It seems to be evident in many phylo- genetic series that increase in the use of a part of the brain goes with increase in the size of that part, provided this use is ad- vantageous to the species. In this paper, measurements are reported which permit comparison of the volume of an auditory nucleus, the n. mesencephalicus lateralis, pars dorsalis, with the volume of the optic lobe in a phylogenetic series of avian brains .

The optic lobes of birds are remarkable not only because of the lamination of the tectum, but also because of their variation in size and shape in different species. A few authors have mentioned that the size of the lobe is correlated with visual func- tion; practically nothing has been written about its shape.

Like the corpora quadrigemina of mam- mals, the optic lobes of birds contain much gray matter related to vision and hearing. The most conspicuous of these gray struc- tures are the tectum, the lateral mesen- cephalic nucleus and the nucleus is thmi. The nucleus mesencepltalicus lateralis, pars dorsalis is considered by Ariens Kappers, Iluber and Crosby ( '36) to be an auditory center. receiving an important

tract from the acoustic nucleus of the hindbrain. In fact a sort of capsule is seen around the nucleus, made by the fibers of the lateral lemniscus (fig. 1 ), The nucleus is homologous with the Torus semicircu- lark of reptiles and with the inferior col- liculus of mammals. Since it is sometimes called the torus in birds this term will be used hereinafter for brevity.

The torus lies just below and mesial to the ventricle of the optic lobe. Its capsule aids in recognizing its boundaries. Its posi- tion within the optic lobe, mesial to, and half surrounded by tectum (figs. 1 and 2 ) makes it possible to compare the areas of torus and whole optic lobe in one section. The ventricle is a well developed lateral outpocketing of the aqueduct of the mid- brain; it is easily seen in the optic lobes of all birds so far examined.

MATERIALS AND METHOD

The brains of 27 different species of birds were collected and fixed in 10% formalin. They were embedded in celloidin and cut in serial sections which were stained for cell bodies, myelin and some for nerve fibers. Only the sections stained for nerve cells were used in this study. The stain was cresyl violet.

In serial sections made through the mid- brain, from before backward, the torus appears shortly after the ventricle of the optic lobe is reached and is found beside the ventricle for a varying distance back-

1 This investi ation has been aided by grant no. 03429-02 from t%e National Institute of Neurological Diseases and Blindness.

271

272 STANLEY COBB

ward, The ventricle is sometimes only a potential space lined with ependyma. Throughout the optic lobe, the concentric laminations of nerve cells in the tectum are conspicuous; in fact it is by these lamina- tions that one recognizes the lobe. They embrace the torus except on the mesial side of the lobe where it joins the tegmen- tum of the midbrain (fig. 1). In certain birds (e.g. , Otus, Steatornis) it was no- ticed that the mesial end of the torus passed beyond a line drawn to delimit the optic lobe (fig. 2 ) . This line is an arbitrary boundary laid down on drawings of each section by connecting the most mesial tips of the upper and lower ends of the laminae of cells (figs. 1 and 2 L-L). In each section the area lateral to this line is considered to be the area of the optic lobe. In those sections in which part of the torus is found, its area is subtracted from the total, the remainder being considered to be optic lobe. The arbitrary boundary causes a slight inaccuracy because several teg- mental nuclei lie wholly or partly within the optic lobe (as defined here) but their size is relatively small, and we consider the error negligible.

The serial sections of the 27 midbrains were projected and either drawn in outline or photographed. The areas of the struc- tures defined above as torus (auditory) and optic lobe were measured with a planim- eter. Knowing the magnification. the thickness of each section, and the number of sections, the approximate volumes of the torus and the lobe were calculated.’ To obtain more precise estimates of the vol- umes of these structures in fresh brain tis- sue, one would have to take into account the amount of shrinkage during imbedding and cutting. This is difficult to determine with accuracy. Fortunately, such absolute measurements were not necessary, because the significant data were not the absolute measurements of volume. but the relative sizes of torus and lobe in any one bird. A simple computation of relative volumes wa5 therefore made and expressed as an index, e.g. ,

1701. torus (auditory) vol. lobe (optic)

Per cent = x 100.

Because the brains varied so greatly in size and because fewer sections were saved in some cases, a varying number of scc-

tions was used in the computations of the different brains (see table 1). When the number of sections of an optic lobe (or torus) was small the error in approximat- ing the volume was greater than that for a larger number of sections and vice versa. The volumes were approximated by an adaptation of the well-known “trapezoidal rule” often used by egineers to estimate the area under an empirically-derived curve (Eshbach, ’36).

This was done by initially assuming that each section had sides perpendicular to its faces, so that the volume of each section is its thickness multiplied by the area of

Fig. 1 Section through brain of emu (Droma- ~ Z L S novae-7zolZandiae) cutting the midbrain at the level where the torus ( M ) is most extensive to correspond with midbrain sections of other species seen in figure 4. Note that the torus lies entirely within the optic lobe, as defined herc by the mesial boundary L-L, in contrast with the rela- tively larger torus of the oilbird (fig. 2). The position of this level of the midbrain relative to the cerebral hemispheres and cerebellum is much like that of the oilbird (fig.. 4 A ) except that a little less cerebrum is cut. Abbreviations used in figures 1 and 2 arc: C, cerebellum CT, corticoid area H, posterior tip of cerebral hemisphere HIP, hippocampus IIS, hyperstriatum I, nucleus interpeduncularis L-L, lateral boundary of optic lobe, line joining

tips of tectal laminae M, nucleus mesencephalicus lateralis, pars dor-

salis (Torus) MP, nucleus mesencephalicus profundulus NS, neostriatum 0, nucleus oculomotoris R, nuclcus ruber T, tectum npticum V, ventricle magnification x 5.5

Fig. 2 Section through brain of oilbird (Stea- tornis cnripensis) at a level, 1,200 ,u anterior to the section shown in figure 4A. The cut is riot quite at right angles to the cerebral axis so the left side is more caudal than the right. On the right the tectum is smaller and only the very tip of the Ventricle appcars, with no torus ad- jacent. At the left the ventrical is large and the torus ( M ) is remarkably large, extending across the boundary of the optic lobe (L-L) into the tegmentum. (For abbreviation see legend of fig. 1 ) . Nissl stain. Magnification x 6.3.

2 I wish to thank Mr. Theodore A. Kalin for helping me with the mathematical treatment of the area measurements. Also, I wish to thank Mr. J. Stanley Cobb for many computations.

VOLUME O F AVIAN TORUS AND TECTUM 273

274 STANLEY COBB

TABLE 1 ~ -~

Ratio of List of brains

Order Species

No. of slides

Torus Tectum

vol. of Torus to

optic lobe

Passeriformes

Coraciiformes

Apodiformes

Caprimulgiformes

Strigiformes

Cuculliformes

Psittaciformes

Columbiformes

Charadriiformes

Gruiformes

Galliformes

Falconiformes

Anserriformes

Ciconiiformes

Pelicaniformes

Procellariif ormes

Podicepediformes

Gaviiformes

Casuariiformes

Sphenisciformes

Mockingbird - Mimus polyglottos Canary - Serinus canaria Blue Jay - Cyanocitta cristata Woodpecker - Dendrocopos pubescens

Kingfisher - Megaceryle &yon

Swift - Chaetura pelagica

Oilbird - Steatornis caripensis (rt) Oilbird - Steatornis caripensis (It) Whippoorwill - Cuprimulgus vociferus Poorwill - Phalaenoptilus nuttallii

Screech Owl - Otus asio Saw-whet Owl - Aegolius acadicus (rt) Saw-whet Owl - Aegoliusacadicus (It)

Cuckoo - Coccyzus americanus

Parakeet - Melopsittacus undulatus

Pigeon - Columba livia

Skua - Catharacta skua maccormicki Gull - Larus argentatus

Rail - Rallus limicola

Turkey - Meleagris gallopavo

Hawk - Falco sparverius

Duck - Anas platyrhynchos

Heron - Butorides viriscens

Cormorant - Phalacrocorax pelagicus

Petrel - Oceanites oceanicus

Grebe - Podiceps auritus (rt ) Grebe - Podiceps auritus (It)

Loon - Gavia immer

Emu - Dromaeus novae-hollandiae

Penguin - Pygoscelis adeliae

3.4 4.9 5.0 4.2

3.3

6.7

7.5 8.7 5.3 4.3

8.2 7.0 7.8

3.5

3.0

3.8

3.1 3.5

5.1

2.5

2.7

4.9

4.4

4.1

4.6

2.9 2.8

2.0

5.4

2.8

6 13 6 13 6 11 6 15

6 15

5 10

9 18 11 19 6 14

10 29

8 14 9 18 9 18

7 13

5 14

4 10

8 16 8 17

7 14

7 17

6 20

9 18

5 12

7 15

9 17

5 10 5 10

7 15

9 22

11 25

Arrangement by orders according to Van Tyne and Berger ('59) reading upwards.

one face. If there are n sections the bot- tom face of one is the top face of the next one down, except for the extreme top and bottom faces, so that there are n + 1 faces distinct from one another. Now the modi- fied trapezoidal rule averages the top-most and bottom-most face areas, adds in the areas of the remaining n - I faces, and multiplies the result by the (constant) thickness of one section. This approxima-

tion method is error-free in the special (if unlikely) case where the rounded volume being estimated is, in fact, a paraboloid of revolution composed of a pair of parabo- loids joined base-to-base. This suggests that errors in approximating the volumes of the torus and the optic lobe, both of which are convex and roughly pear-shaped, will be small, and that the error in their ratio will be even less significant.

VOLUME O F AVIAN TORUS AND TECTUM 275

In order to test the statement that when the number of slides is smaller the error is greater, and to estimate approximately how great the error might be, the two birds with the largest number of sections through the torus (oilbird 11 and penguin 11) were chosen for a repeated evalulation. In each, the areas of every-other section were used to compute the ratio of “volume-torus’’ to “volume-lobe.’’ In the oilbird then there were two cases, the first with six torus sec- tions and ten lobe sections, the second (using the alternate faces of the blocks) with five torus sections and nine lobe sec- tions. In the penguin the two cases were, the first, with six torus sections and 13 lobe sections, the second (using the alter- nate faces) with five torus sections and 12 lobe sections. The results of these test computations were as follows: Oilbird

(all sections)

( f i s t case)

(second case)

11 torus and 19 lobe sections ratio = 8.7%

6 torus and 10 lobe sections ratio = 9.8%

5 torus and 9 lobe sections ratio = 8.0% Penguin

(all sections)

(first case)

(second case)

11 torus and 25 lobe sections ratio = 2.8%

6 torus and 13 lobe sections ratio = 2.5%

5 torus and 12 lobe sections ratio = 3.0%

That this method of measurement of small cerebral structures is only fairly con- sistent and accurate, is shown by three cases where both right and left sides were measured in the same bird (table 1). It is presumed (but not proved) that the two sides of one brain are made up of homol- ogous structures of about the same size. In the grebe (Podiceps) the ratios of torus to optic lobe of the right and left sides were almost identical, 2.8% and 2.9%. In the owl (Aegol ius) the ratios of right and left were rather far apart, 7% and 7.8% ; this was true also in Steatornis with 7.5% and 8.7%. This suggests that in birds with highly developed hearing the right and left sides tend to be asymmetrical (Pumphrey, ’48). In Mimus and Steatomis all the measurements were repeated for a check, and in each case the second counts gave the final ratio of torus to lobe within 2% of the first.

OBSERVATIONS The data are presented in table 1. In

the first column are the names of the orders to which the observed species be- long. These are arranged in the sequence published by Van Tyne and Berger (’59) reading from the bottom upwards. In the second column are the names of the species studied in the present report. In the third column is a figure, expressed in per cent ( % ), which indicates the ratio of the vol- ume of the torus to the volume of optic lobe. In the fifth column of table 1 is given the number of slides in each series of sections of the optic lobes; in the fourth column is the number of these sections that impinge on the torus. This is to give an idea as to the reliability of the different indices, although (as pointed out above) even where few sections are available the error in the index is reasonably small.

DISCUSSION

Inspection of the table shows that the ratio of the volume of the auditory torus to the volume of the optic lobe varies from 8.7% in Steatornis and 8.2% in Otus to 2.0% in Gavia. In other words, the torus is from about one-eleventh to one-fiftieth as large as the rest of the optic lobe. The largest single index of a torus in propor- tion to optic lobe is found in the left lobe of the oilbird, 8.7%, the average of the two sides being 8.1%. The average of all the Caprimulgiformes is 6.3% (4 observa- tions). The average of three measure- ments of Strigiformes is 7.6%, the closest to the oilbird being Otus with 8.2%. No other birds approach these figures except Chaetura with 6.7%. Birds with percent- ages between four and six are two passer- ines, (4.9% and 5.0% ), Rallus (5.1% ), Anas (4.9% ), Butorides (4.4% ), P h a h crocorax (4.1% ) and Dromaeus (5.4% ). The average of three passerines is 4.4%. In all the other birds the percentages fall between 2.0 and 3.9; this includes 13 spe- cies. The lowest five are Gavia (2.0% ), Podiceps (2.8% ), Pygoscelis (2.8%), Mele- agris (2.5% ) and Falco (2.7% ).

Figures of the kind exhibited in table 1 only become significant to the ornithologist

3 This spelling is preferred to . DROMICElUS and DROMAIUS because the former is the perpetuation of a graphological error, and the latter is a less proper latinization.

276

........................... ........... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................... ..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...... :..:: s.$. :,.... ::.:.:.:.:

GAPR I M U LG I APODI N = 5

STANLEY COBB

Oilbird Swift Poorw i II Whippoorwi II

- STRlGl

- 4.4 PASSER1 GRUl ANSERI PIC1 CASUARll PROGELLARII ClCONl PELICAN1 N- II

I O w l s

24J GALL1 SPHENlSGl FALCON1 PODlClPODl

GAVll N = 6

N= 3

Canary Mocking bird Kingfisher Woodpecker

Parakeet Cuckoo Pigeon

Turkey Falcon Penguin

Cormorant Jay Emu Petrel Rail Duck

Heron Skua Gull

Grebe Loon

~ ~~~

( Minimum: LOON, 2 % ; Maximum: OILBfRD, 8.7% ) Fig. 3 Bar diagram showing relative sizes of torus to optic lobe in the different orders

of birds (the ending FORMIES is omitted to save space). The area of each bar represents the size of the optic lobe relative to the torus (smaller shaded area). The ratio is expressed in per cent. For example the average of the three observations on Strigiformes shows that the volume of the torus is 7.4% of the volume of the rest of the optic lobe. The numher of observations used to arrive at the average is expressed by N = 3.

if they can be correlated with some be- havioral characteristics. This study was begun because it seemed to be a reasonable hypothesis that the oilbird (S ten torn is ) would be found to have an unusually large central auditory apparatus. The oilbird nests in dark caves and finds its way about in these caves by echolocation (Griffin, '53). The data in table 1 support the ex- pectation, at least for the auditorv nucleus (torus) of the midbrain. Likewise, it was supposed that owls would have larger auditory centers than most birds, because of the great size of their ears and because some species are known to locate their prey in complete darkness by auditory triangu- lation (Payne, .61). This supposition is also well supported by the findings. Winter ('63) finds similar enlargement of auditory nuclei in the hindbrain.

In figure 3 the birds are arranged in a rank order dependent on the ratio of torus to optic lobe, the largest at the top. Func-

tional significance is obvious in the owls and oilbird in the two upper bars. Other correlations are less definite, and must be looked upon as speculative, but perhaps worthy of mention to promote further in- vestigation. For example, the other two Caprimulgiformes, the Whippoorwill and Poorwill, both have larger indices than most of the birds on the list. Is this be-

Fig. 4 Sections through the midbrains of four birds at the approximate level of the greatest area of the torus. The species are chosen to show- the variation in the relations of the optic lobes to the cerebrum and cerebellum. Al l the sections are magnified x 4.6. In the jay (Cyanocitta cristata) the hemispheres of the cerebrum come far back over the midbrain, so a large slice of each oc- cipital pole is seen while no cerebellum is found in the section. In the falcon (Falco spawer ius) the reverse is seen. The oilbird (Steatornis cari- p e n s i s ) is intermcdiate, while in the owl (Otus asio) there is more cerebrum and less cerebellum. The shape of the midbrain is obviously affected by the relative size and position of cerebrum and cerebellum ( see text).

VOLUME O F AVIAN TORUS AND TECTUM 277

2 78 STANLEY COBB

cause members of this order all use their ears in some special way? It is of interest that the closely related swift (Chaetura) has a large torus, 6.7%. We have only one series of measurements on one species, so verification is needed, but other species of swifts are known to live in caves and prob- ably use echolocation (Medway, ’60). Chaetura pelagica is a bird of the twilight and utters high-pitchcd twitterings which might be used for echolocation. Here are some obvious problems for research.

One might expect that the song birds among the Passeriformes would have well developed auditory nuclei in their brains. Our figures suggest this, but many more species should be studied in this way before a definite statement can be made. Like- wise one wonders why water birds such as rails and ducks have higher indices than grebes, loons and penguins; perhaps it is because of their nocturnal feeding habits. Here too, more data are needed. The very low ratio in Falco may well be due to an excessively well developed visual apparatus rather than a poorly developed auditory apparatus. It is apparent that to continue this line of research some base-line for comparison must be devised so that one can compare not only two nuclei of dif- ferent function, but compare both to some constant, such as Portmann’s (’46) “Stammrest” from which he deduces de- grees of “encephalization” in birds.

A comparison of sections through the midbrains of different birds shows that there is great variation in the shape and relative position of the optic lobes. In fig- ure 4 sections of four birds are chosen to illustrate the types found in our series. The dorsal part of the tectum of the falcon (C) is seen to be high beside the cerebellum, and the tips of the laminae are turned downward and inward. This arrange- ment is less marked in the oilbird ( A ) where the whole midbrain appears to be flatter and wider. The flatness is also seen in the owl ( B ) but the ventral tips of the laminae are recurved to point a little up- ward. The extreme is seen in the jay ( D ) where the downward tilt of the optic lobes is striking, no cerebellum is seen in this section and the recurving of the ventral ends of the tectal laminae is conspicuous. In A and B the section passes through both

cerebrum and cerebellum; more cerebel- lum is cut in A and more cerebrum in B. This is due not primarily to a difference in the relative sizes of cerebrum and cere- bellum in oilbird and owl, but to the great bending of the cerebral axis in the owl, with foreshortening of the antero-posterior dimension of the whole brain, and crowd- ing of the optic lobes between forebrain and hindbrain. In the oilbird the brain has a straighter axis and more extended form (see Stingelin (’58), figs. 25 and 26 for comparison of Caprimulgi- and Strigi- formes),

A comparison of the brains of the falcon (C) and the jay (D) indicates that it is the size of the cerebral hemispheres that make the great difference in these two sections. Neither of these birds has a greatly bent cerebral axis, but the falcon has relatively small cerebral hemispheres, whereas those of the jay are large and extend back over the whole of the optic lobe and part of the cerebellum (see Cobb (‘60b), figs. 3 and 5).

From the point of view of the optic lobe, these sections are made at the same level, i.e., at the point where the section of the torus has its maximum area. But judging by the amount of cerebellum and cerebrum seen, these sections are at very different levels. All this merely goes to show that no simple formulation can define the posi- tion and size of the optic lobes in birds. It is a matter of first the relative develop- of forebrain, midbrain and hindbrain in each group of birds; second, the arrange- ment of these parts of the brain on a more or less bent axis; and third, the shape of the skull, size of the orbit, and habitual posture of the bird. Nevertheless, the optic lobe of the bird is a relatively enormous organ and finds room for its important de- velopment (see Cobb (’60b), fig. 2) be- cause all birds are more dependent on vision than upon any other sense.

SUMMARY

The avian optic lobe is remarkable for its size, and for the laminar arrangement of the nerve cells of its optic tectum. This midbrain structure more closely resembles the cerebral cortex of mammals than any part of the avian forebrain, because in birds, although superficial corticoid areas are found, there is no neocortex. In the

279 VOLUME O F AVIAN TORUS AND TECTUM

optic lobe there is also a large auditory nucleus, the torus (n. mesencephalicus lateralis, pars dorsalis). From measure- ments of serial sections of 27 different species of birds the volume of the torus and of the whole lobe have been computed. The volume of the torus (auditory) and of the lobe (optic) has been compared in each species, and the result expressed in per cent. The torus varies from being 2.0% of the size of the optic lobe in a loon (Gavia i m m e r ) , to being 8.7% in an oilbird (Steatornis caripensis). Taken by orders, the Strigiformes have the largest ratio of torus to optic (7.4%), next come the Capri- mulgiformes and Apodiformes with an average of 6.5%. These are the groups of birds in which hearing is very highly de- veloped either for echolocation (oilbirds and swifts) or for locating sounds made by their prey (owls). The large relative size of the torus thus seems to have a func- tional significance. The smallest ratio is found in Podicipodi-, Gavii-, Galli-, and Sphenisciformes (average 2.4% ). Between these extremes fall birds in all the 13 other orders studied, averaging 4.0%.

Variation in the position and shape of the optic lobes in different birds is shown to be a conspicuous feature of avian cere- bral morphology. These lobes of the mid- brain are more rounded and dorsolateral in those species in which the cerebral hemi- spheres do not come far back to overlap the midbrain (falcon and emu). The optic lobes are more flattened and ventrolateral in species in which the cerebral hemi- spheres do come far back over the mid- brain (e.g., jay). The size and position of the cerebellum is also important in deter- mining the shape and position of the optic lobes.

Quantitative methods, in the study of the anatomy of the avian brain, can give

significant information. The significance appears when the anatomical data are con- sidered in relation to the birds behavior.

LITERATURE CITED Ariens Kappers, C. V., G. C. Huber and E. C.

Crosby 1936 The Comparative Anatomy of the Nervous System of Vertebrates, including Man. Macmillan Co., New York. 2 vols.

Bumm, A. 1883 Das Grosshirn der Vogel. Ztschr. fur wissen. Zool., 38: 432.

Cobb, S. 1960a A note on the size of the avian olfactory bulb. Epilepsia, I : 394-402.

__ 1960b Observations on the comparative anatomy of the avian brain. Perspectives in Biol. and Med., Univ. of Chicago Press, Chicago, 3: 383-408.

Eshbach, 0. W. 1936 Handbook of Engineering Fundamentals. John Wiley & Sons, New York. Pp. 240.

Fritz, W. 1949 Vergleichende Studien uber den Anteil von Striatumteilen am Hemispharen- volumen des Vogelhirns. Rev. Suisse Zool., 56: 461491.

Griffin, D. R. 1953 Acoustic orientation in the oilbird (Steatornis). Proc. Nat. Acad. Sci., 39: 884.

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Turner, C. H. 1891 The morphology of the avian brain. J. Comp. Neur., I : 39; 107; 265.

Van Tyne, J., and A. J. Berger 1959 Funda- mentals of Ornithology. John Wiley & Sons,

1-15; 15: 162-171.

New York. Winter, P. 1963 Vergleichende qualitative und

quantitative Untersuchungen an der Horbahn von Vogeln. Z. Morph. 8kol. Tiere, 52: 365- 400.