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The area of the nucleus isthmo-opticus in the American kestrel (Falco sparverius) and the red-tailed hawk (Buteo jamacensis)
Brain Research, 88 (1975) 525-531 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
525
The area of the nucleus isthmo-opticus in the American kestrel
(Falco sparverius) and
the red-tailed hawk
(Buteo jomoicensis)
G E O R G E K. SHORTESS AND ELAINE F. KLOSE
Bioelectric Laboratory, Psychology Department, Lehigh University, Bethlehem, Pa. 18015 (U.S.A.) (Accepted January 27th, 1975)
The avian nucleus isthmo-opticus (10) contains cell bodies of efferent fibers which form the tractus isthmo-opticus (IOT) and which synapse on amacrine cells in the contralateral retinal,6,12. In the pigeon (Columba livia) the IO is located at the medial border of the optic rectum, along the dorsal boundary of the mesencephalon at about the level of the nucleus of the fourth nerve. At the medial border of the IO is the radix mesencephalicus nervi trigemini. The IO is bounded laterally by the two divisions of the nucleus isthmi, pars principalis (Ipc-Imc) and ventrally by the nucleus lemniscus lateralis, pars dorsalis (Groebbels) (LLd). Ventral to the LLd are the nucleus lemniscus lateralis pars ventralis (Groebbels) (LLv) caudally, and the nucleus semilunaris (SLu) rostrally2, 9. In addition, descriptions of a well differentiated IO have been made in the chicken
(Gallus domesticus)S,H, in various passeriformes7,10,15 and in the humming bird (Chrysolampis mosquitus Linn. and Chlorostilbon earibaeus lawr.) 4. Showers and Lyons 13 also reported a well defined IO in the guinea hen (Numida melagis), in the turkey buzzard (Cathartes aura Wied.), in the duck (Anas domestica) and in the pheasant (Phasianus torquatus Gruel.). A more detailed IO description in the duck (Anasplatyrhynchos) has been presented by Sohal and Narayanan 14. However, it was reported that the IO does not exist in the kiwi (Apteryx australis) ~ and is poorly differentiated or non-existent in the ibis (Myeteria americana Linn.) ~3. The degree of differentiation and the number of cells of the IO have been described in only a few species. Huber and Crosby 7 reported that the IO of the sparrow tended to be oval in shape and not convoluted as in the pigeon and chicken. More recently Cowan and Powell z counted 8100, 8400 and 9400 cells in three pigeon nuclei while Cowan and Wenger 3 counted 10,700 in the 18-day-old chick. Sohal and Narayanan a4 described the duck IO as having two convoluted layers of cells somewhat similar to the pigeon IO, but with only approximately 3600 cells. In order to further expand the comparative understanding of the IO, the following study in two species of the order falconiformes was undertaken. As a basis of comparison, results from the pigeon are included.
526 '1' f ' ~
A :.<;
B
C
Fig. l. The area of the nucleus isthlno-opticus (IO) (indicated b) the 3 arro~s) m (A) pigeon, (B) red-tailed hawk, and (C) American kestrel. Nucleus isthmi, pars principalis, parvocellularis (Ipc). Nucleus lemniscus latcralis pars dorsa/is (Groebbels) (LLd). Scale 500/m. Thionin stain.
527 Brains from 2 white carneaux pigeons (Columba livia Gruel.), 3 red-tailed hawks (Buteo jamaicensis Gruel.) and 2 American kestrels (Falco sparverius Linn.) were examined. They were all obtained alive and perfused through the left ventricle with physiological saline and 10 ~ formalin using Equi-Thesin as the anesthetic. The wild birds had wing or leg damage which precluded their survival in a natural environment. Brains were soaked in 10~o formalin with sucrose prior to being frozen and sectioned frontally at 20 or 42/zm. Blocking of the brain was done by establishing a horizontal plane along the dorsal surface of the forebrain and cerebellum, and cutting through the ventral surface of the brain at an angle of 80° to the horizontal plane. This blocking angle approximates the angle used by Karten and Hodos 9 for the pigeon, Alternate serial sections were stained for Nissl material with thionin. The remaining sections were stained using a modified Weil procedure. Counts were made of cells in the 20-/~m thionin sections based on two criteria. They should be deeply stained and have a minimum cross-sectional diameter of 5 #m. No correction factor was used since one was not used in the pigeon 2 and since the area of the counts could only be approximated for the birds of prey. We are thus reporting only the relative cell counts. The major result of the examination of the available material is illustrated in Fig. I. in the position of the IO, in both wild species examined, there is a poorly differentiated cluster of cells which appears to be an extension of the LLd. The pigeon IO, by comparison, is clearly differentiated by a border of deeply staining cells of 5-25 #m diameter. Both portions of the nucleus isthmi pars principalis are clearly differentiated in all species, with the magnocellularis portion retaining the significantly larger cell size. The two portions of nucleus lemniscus lateralis (Groebbels) appear to be equally evident in all species including the pigeon. This nucleus is composed of small poorly staining cells which comprise relatively undifferentiated cell groupings. The nucleus semilunaris (SLu) is a well differentiated cell group ventral to the LLd in the American kestrel and the red-tailed hawk. The area of the IO does not form an extension of the SLu in either species examined, which differs apparently from the ibis ta. In the sections stained for fibers, the radix mesencephalicus nervi trigemini appeared to course through the area of the lO in the birds of prey. Higher magnification of the area of the IO in all species is shown in Fig. 2. While all show large cells up to 25 #m in diameter, the density of such cells is less in the hawk than in the kestrel. This would appear to be a result of the larger brain volume of the hawk in comparison to the kestrel and pigeon. In addition, the formation of cells into rows, clearly seen in the pigeon, is only just noticeable in the birds of prey. The extent to which these fragmentary laminae result from developmental processes similar to those in the chick or duck remains to be evaluated. Fig. 3 shows the region occupied by the pigeon IOT, where it is clearly evident as a compact bundle of myelinated fibers. However, the birds of prey show only isolated fiber bundles which appear to be fragments of an lOT (indicated by the arrows); yet, tracing these fibers rostrally, through the serial sections, shows that they appear to be part of the intratectal fiber system and do not join the optic tract as the pigeon lOT fibers do.
528
A
4
Fig, 2. The area of the nucleus isthmo-opticus in (A) pigeon, (B) red-tailed hawk. and (C) American kestrel. Scale 200 l~m. Thionin stain,
529
A
13
C
Fig. 3. The area of the tractus isthmo-opticus (lOT) in (A) pigeon, (B) red-tailed hawk, and (C) American kestrel. Scale - 500/~m. Hematoxylin stain.
530 The results of the cell counts for the American kestrels were 1600 and 1400 cells and for the red-tailed hawks were 1500 and 2000. The figu,es for the pigeon were 9200 and 10,100 alld agree ~ith Cowan and Powell e to within 10°,0. Becaubc of the poor differentiation of the IO in the hawks and kestrels, somewhat arbitrary limits had to be imposed and thus the counts are only approximate. However, the limits imposed probably included too many cells rather than too few. It would appear, therefore, that the efferent system to the retina is considerably less well developed in these birds of prey and probably functionally less significant than in the pigeon. Only further histological, behavioral and electrophysiological techniques can conclusively determine their relative importance. Our results do emphasize the difficulty of generalizing, concerning efferent function, even within the class ayes. However, several limiting statements concerning function can be suggested on the basis of the absence of a well developed IO in the hawk and kestrel, it would appear that the I 0 is not simply associated with flight, or with general acuity, given the high level of acuity of the hawk ~. Possible functions consistent with the comparative data include involvement with ground feeding, pecking, search behavior, and the detection of predators. Since Showers and Lyons ~:~ apparently report a well differentiated 10 in the turkey buzzard there would appear to be differences in 10 development among falconiformes. Further detailed examination of this order would appear to be necessary to understand the significance of such differences. It should be clear, however, that any complete theory of the function of efferents to the retina will need to account for all of these comparative differences. We express our deep appreciation to Mr. Thomas Mutchler, Bethlehem, Pa. for his cooperation in providing the wild birds and for his interest in this work and to Mr. Glenn L Bowers of the Pennsylvania Game Commission for cooperating in issuing the permit to possess protected birds. Supported by NIH Grant R01 EY00679.
1 COWA•, W. M., Centrifugal fibers to the avian retina, Brit. reed. Bull., 26 (1970) 112-118. 2 COWAN,W. M., ANt) POWELL, T. P. S., Centrifugal fibers in the avian visual system, Proc. roy. Soc. B, 158 (1963) 232 252. 3 COWAN,W. M., AND WENC-ER,E., The development of the nucleus of origin of centrifugal fibres to the retina in the chick, J, comp. Neurol., 133 (1968) 207-240. 4 CRA1GIE, E. H., Observations on the brain of the humming bird (Chrysolantpis mosquitus Linn. and Chlorostilbon caribaeus Lawr.), J. comp. NeuroL, 45 (1928) 377-483. 5 CRAICJE,E. H., Studies on the brain of the kiwi (Apteryx australis), J. comp. Neurol., 49 (1930) 223-357. 6 GALIFRET, Y., CONDI~--COuRTINE,F., REPI~RANT,J., AND SERVI]ERE,J., Centrifugal control in the visual system of the pigeon, Vision Res., l l, Suppl. 3 (1971) 185-200. 7 HUBER,G. C., ANDCROSaY,E, C., The nuclei and fiber paths of the avian diencephalon, with consideration of telencephalic and certain mesencephalic centers and connections, J. comp. Neurol., 48 (1929) 1-225. 8 JUNGHERR, E., Certain nuclear groups of the avian mesencephalon, J. comp. Neurol., 82 (1945) 55-75.
531 9 KARTEN, H. J., AND HODOS, W., A Stereotaxic Atlas of the Brain of the Pigeon, Columba livia, John Hopkins Press, Baltimore, Md., 1967. 10 PAPEZ, J., Comparative Neurology, Crowell, New York, 1929. 11 PERLIA,R., Ueber ein neues optieus Centrum beim Huhn, Albrecht v. Graefes Arch. Ophthal., 35 (1889) 20-24. 12 RODIECK,R. W., The Vertebrate Retina, Freeman, San Francisco, Calif., 1973. 13 SHOWERS, M. J, C., AND LYONS, P., Avian nucleus isthmi and its relation to hippus, J. comp. Neurol., 132 (1968) 589-616. 14 SOHAL,G. S., AND NARAYANAN,C. H., The development of the isthmo-optic nucleus in the duck (Anas platyrhynchos). I. Changes in cell number and cell size during normal development, Brain Research, 77 (1974) 243-255. 15 TURNER,C. H., Morphology of the avian brain, J. eomp. Neurol., 1 (1891) 107-133. 16 WALLS, G. L., The Vertebrate Eye and its Adaptive Radiation, Cranbrook Inst. Sci., Bloomfield Hills, Mich., 1942.
525
The area of the nucleus isthmo-opticus in the American kestrel
(Falco sparverius) and
the red-tailed hawk
(Buteo jomoicensis)
G E O R G E K. SHORTESS AND ELAINE F. KLOSE
Bioelectric Laboratory, Psychology Department, Lehigh University, Bethlehem, Pa. 18015 (U.S.A.) (Accepted January 27th, 1975)
The avian nucleus isthmo-opticus (10) contains cell bodies of efferent fibers which form the tractus isthmo-opticus (IOT) and which synapse on amacrine cells in the contralateral retinal,6,12. In the pigeon (Columba livia) the IO is located at the medial border of the optic rectum, along the dorsal boundary of the mesencephalon at about the level of the nucleus of the fourth nerve. At the medial border of the IO is the radix mesencephalicus nervi trigemini. The IO is bounded laterally by the two divisions of the nucleus isthmi, pars principalis (Ipc-Imc) and ventrally by the nucleus lemniscus lateralis, pars dorsalis (Groebbels) (LLd). Ventral to the LLd are the nucleus lemniscus lateralis pars ventralis (Groebbels) (LLv) caudally, and the nucleus semilunaris (SLu) rostrally2, 9. In addition, descriptions of a well differentiated IO have been made in the chicken
(Gallus domesticus)S,H, in various passeriformes7,10,15 and in the humming bird (Chrysolampis mosquitus Linn. and Chlorostilbon earibaeus lawr.) 4. Showers and Lyons 13 also reported a well defined IO in the guinea hen (Numida melagis), in the turkey buzzard (Cathartes aura Wied.), in the duck (Anas domestica) and in the pheasant (Phasianus torquatus Gruel.). A more detailed IO description in the duck (Anasplatyrhynchos) has been presented by Sohal and Narayanan 14. However, it was reported that the IO does not exist in the kiwi (Apteryx australis) ~ and is poorly differentiated or non-existent in the ibis (Myeteria americana Linn.) ~3. The degree of differentiation and the number of cells of the IO have been described in only a few species. Huber and Crosby 7 reported that the IO of the sparrow tended to be oval in shape and not convoluted as in the pigeon and chicken. More recently Cowan and Powell z counted 8100, 8400 and 9400 cells in three pigeon nuclei while Cowan and Wenger 3 counted 10,700 in the 18-day-old chick. Sohal and Narayanan a4 described the duck IO as having two convoluted layers of cells somewhat similar to the pigeon IO, but with only approximately 3600 cells. In order to further expand the comparative understanding of the IO, the following study in two species of the order falconiformes was undertaken. As a basis of comparison, results from the pigeon are included.
526 '1' f ' ~
A :.<;
B
C
Fig. l. The area of the nucleus isthlno-opticus (IO) (indicated b) the 3 arro~s) m (A) pigeon, (B) red-tailed hawk, and (C) American kestrel. Nucleus isthmi, pars principalis, parvocellularis (Ipc). Nucleus lemniscus latcralis pars dorsa/is (Groebbels) (LLd). Scale 500/m. Thionin stain.
527 Brains from 2 white carneaux pigeons (Columba livia Gruel.), 3 red-tailed hawks (Buteo jamaicensis Gruel.) and 2 American kestrels (Falco sparverius Linn.) were examined. They were all obtained alive and perfused through the left ventricle with physiological saline and 10 ~ formalin using Equi-Thesin as the anesthetic. The wild birds had wing or leg damage which precluded their survival in a natural environment. Brains were soaked in 10~o formalin with sucrose prior to being frozen and sectioned frontally at 20 or 42/zm. Blocking of the brain was done by establishing a horizontal plane along the dorsal surface of the forebrain and cerebellum, and cutting through the ventral surface of the brain at an angle of 80° to the horizontal plane. This blocking angle approximates the angle used by Karten and Hodos 9 for the pigeon, Alternate serial sections were stained for Nissl material with thionin. The remaining sections were stained using a modified Weil procedure. Counts were made of cells in the 20-/~m thionin sections based on two criteria. They should be deeply stained and have a minimum cross-sectional diameter of 5 #m. No correction factor was used since one was not used in the pigeon 2 and since the area of the counts could only be approximated for the birds of prey. We are thus reporting only the relative cell counts. The major result of the examination of the available material is illustrated in Fig. I. in the position of the IO, in both wild species examined, there is a poorly differentiated cluster of cells which appears to be an extension of the LLd. The pigeon IO, by comparison, is clearly differentiated by a border of deeply staining cells of 5-25 #m diameter. Both portions of the nucleus isthmi pars principalis are clearly differentiated in all species, with the magnocellularis portion retaining the significantly larger cell size. The two portions of nucleus lemniscus lateralis (Groebbels) appear to be equally evident in all species including the pigeon. This nucleus is composed of small poorly staining cells which comprise relatively undifferentiated cell groupings. The nucleus semilunaris (SLu) is a well differentiated cell group ventral to the LLd in the American kestrel and the red-tailed hawk. The area of the IO does not form an extension of the SLu in either species examined, which differs apparently from the ibis ta. In the sections stained for fibers, the radix mesencephalicus nervi trigemini appeared to course through the area of the lO in the birds of prey. Higher magnification of the area of the IO in all species is shown in Fig. 2. While all show large cells up to 25 #m in diameter, the density of such cells is less in the hawk than in the kestrel. This would appear to be a result of the larger brain volume of the hawk in comparison to the kestrel and pigeon. In addition, the formation of cells into rows, clearly seen in the pigeon, is only just noticeable in the birds of prey. The extent to which these fragmentary laminae result from developmental processes similar to those in the chick or duck remains to be evaluated. Fig. 3 shows the region occupied by the pigeon IOT, where it is clearly evident as a compact bundle of myelinated fibers. However, the birds of prey show only isolated fiber bundles which appear to be fragments of an lOT (indicated by the arrows); yet, tracing these fibers rostrally, through the serial sections, shows that they appear to be part of the intratectal fiber system and do not join the optic tract as the pigeon lOT fibers do.
528
A
4
Fig, 2. The area of the nucleus isthmo-opticus in (A) pigeon, (B) red-tailed hawk. and (C) American kestrel. Scale 200 l~m. Thionin stain,
529
A
13
C
Fig. 3. The area of the tractus isthmo-opticus (lOT) in (A) pigeon, (B) red-tailed hawk, and (C) American kestrel. Scale - 500/~m. Hematoxylin stain.
530 The results of the cell counts for the American kestrels were 1600 and 1400 cells and for the red-tailed hawks were 1500 and 2000. The figu,es for the pigeon were 9200 and 10,100 alld agree ~ith Cowan and Powell e to within 10°,0. Becaubc of the poor differentiation of the IO in the hawks and kestrels, somewhat arbitrary limits had to be imposed and thus the counts are only approximate. However, the limits imposed probably included too many cells rather than too few. It would appear, therefore, that the efferent system to the retina is considerably less well developed in these birds of prey and probably functionally less significant than in the pigeon. Only further histological, behavioral and electrophysiological techniques can conclusively determine their relative importance. Our results do emphasize the difficulty of generalizing, concerning efferent function, even within the class ayes. However, several limiting statements concerning function can be suggested on the basis of the absence of a well developed IO in the hawk and kestrel, it would appear that the I 0 is not simply associated with flight, or with general acuity, given the high level of acuity of the hawk ~. Possible functions consistent with the comparative data include involvement with ground feeding, pecking, search behavior, and the detection of predators. Since Showers and Lyons ~:~ apparently report a well differentiated 10 in the turkey buzzard there would appear to be differences in 10 development among falconiformes. Further detailed examination of this order would appear to be necessary to understand the significance of such differences. It should be clear, however, that any complete theory of the function of efferents to the retina will need to account for all of these comparative differences. We express our deep appreciation to Mr. Thomas Mutchler, Bethlehem, Pa. for his cooperation in providing the wild birds and for his interest in this work and to Mr. Glenn L Bowers of the Pennsylvania Game Commission for cooperating in issuing the permit to possess protected birds. Supported by NIH Grant R01 EY00679.
1 COWA•, W. M., Centrifugal fibers to the avian retina, Brit. reed. Bull., 26 (1970) 112-118. 2 COWAN,W. M., ANt) POWELL, T. P. S., Centrifugal fibers in the avian visual system, Proc. roy. Soc. B, 158 (1963) 232 252. 3 COWAN,W. M., AND WENC-ER,E., The development of the nucleus of origin of centrifugal fibres to the retina in the chick, J, comp. Neurol., 133 (1968) 207-240. 4 CRA1GIE, E. H., Observations on the brain of the humming bird (Chrysolantpis mosquitus Linn. and Chlorostilbon caribaeus Lawr.), J. comp. NeuroL, 45 (1928) 377-483. 5 CRAICJE,E. H., Studies on the brain of the kiwi (Apteryx australis), J. comp. Neurol., 49 (1930) 223-357. 6 GALIFRET, Y., CONDI~--COuRTINE,F., REPI~RANT,J., AND SERVI]ERE,J., Centrifugal control in the visual system of the pigeon, Vision Res., l l, Suppl. 3 (1971) 185-200. 7 HUBER,G. C., ANDCROSaY,E, C., The nuclei and fiber paths of the avian diencephalon, with consideration of telencephalic and certain mesencephalic centers and connections, J. comp. Neurol., 48 (1929) 1-225. 8 JUNGHERR, E., Certain nuclear groups of the avian mesencephalon, J. comp. Neurol., 82 (1945) 55-75.
531 9 KARTEN, H. J., AND HODOS, W., A Stereotaxic Atlas of the Brain of the Pigeon, Columba livia, John Hopkins Press, Baltimore, Md., 1967. 10 PAPEZ, J., Comparative Neurology, Crowell, New York, 1929. 11 PERLIA,R., Ueber ein neues optieus Centrum beim Huhn, Albrecht v. Graefes Arch. Ophthal., 35 (1889) 20-24. 12 RODIECK,R. W., The Vertebrate Retina, Freeman, San Francisco, Calif., 1973. 13 SHOWERS, M. J, C., AND LYONS, P., Avian nucleus isthmi and its relation to hippus, J. comp. Neurol., 132 (1968) 589-616. 14 SOHAL,G. S., AND NARAYANAN,C. H., The development of the isthmo-optic nucleus in the duck (Anas platyrhynchos). I. Changes in cell number and cell size during normal development, Brain Research, 77 (1974) 243-255. 15 TURNER,C. H., Morphology of the avian brain, J. eomp. Neurol., 1 (1891) 107-133. 16 WALLS, G. L., The Vertebrate Eye and its Adaptive Radiation, Cranbrook Inst. Sci., Bloomfield Hills, Mich., 1942.