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Identification of avian brain regions responsive to retinal slip using 2-deoxyglucose
Brain Research, 210 (1981) 455-460 © Elsevier/North-Holland Biomedical Press
455
Identification of avian brain regions responsive to retinal slip using 2-deoxyglucose
OLIVIA C. McKENNA and JOSH WALLMAN Department of Biology, City College of the City University of New York, New York, N.Y. 10031 (U.S.A.)
(Accepted November 13th, 1980) Key words: accessory optic system -- pretectum -- retinal slip - - optokinetic nystagmus
In optokinetic nystagmus (OKN) retinal slip, that is, movement of the visual world on the retina, results in stabilizing eye movements which reduce the retinal slip velocity almost to zero. The visual input for this compensatory reflex seems to be transmitted along anatomically distinct pathways to the pretectal nuclei and accessory optic system in both birds and mammals. In mammals, one of the pretectal nuclei, the nucleus of the optic tract (NOT), appears to receive visual input necessary for horizontal O K N from a class of retinal ganglion cells that respond to slow horizontal movement and presumably project directly to the NOTS,7,15. Cells of the NOT are excited by slow whole-field horizontal movement in a temporal to nasal direction and either are not activated or are inhibited by movement in the opposite directionS, 7. The most convincing evidence for the role of NOT is the finding that electrical stimulation of the NOT produced horizontal O K N while lesioning the nucleus eliminated this type of nystagmus 6. In the mammalian accessory optic system, the medial and lateral terminal nuclei ( M T N and L T N respectively), appear to be involved in retinal signalling of vertical OKN. Retinal ganglion cells that are direction-selective and respond to slow stimulus movement14,15 are thought to terminate in the MTN. The cells of the M T N have large receptive fields and respond to slow vertical stimuli moving upward and posteriorlS, 20. Physiological properties of LTN are similar except that the cells prefer downward and posterior movement. The third terminal nucleus, the dorsal nucleus (DTN), is best modulated by horizontal movement in a temporal to nasal direction, a property of cells in the NOTS,7, is. In birds the nuclei considered homologous to the mammalian accessory terminal nuclei are the nuclei of the basic optic root (nBOR) 1,11which consist of the nBOR pars dorsalis (nBORd), nBOR pars lateralis (nBOR1) and the nBOR proper. As in mammals, two of the three nuclei appear to receive vertical, or near vertical, retinal slip signals, as shown by electrophysiological studiesZ,a,12,1L Neurons of the nBOR responsive to slow whole-field upward movement are concentrated in the nBORd while neurons responsive to slow whole-field downward and anterior movement are
456 concentrated in the nBOR proper 3. Electrophysiological properties of neurons in the nBORI have not been reported. The suggestion has been made that the lentiform nucleus of the mesencephalon (LM) of birds is homologous to the NOT of mammals on the basis of its position in the diencephalong, 10. Nothing, however, is known about whether the LM is similar in function to NOT. The present study was undertaken to reveal what nuclei in the avian brain are involved in signalling horizontal retinal slip and to confirm a role of the nBOR in signalling vertical retinal slip by using the metabolic mapping technique of Sokoloff et a119. The chick is a particularly useful experimental animal for this type of study since its optic nerves are completely or almost completely crossed and its eyes placed laterally; consequently, different visual stimuli presented to each eye would be expected to result in differences in labeling of equivalent structures on each side of the brain. Here, we confirm that the nBORd and nBOR proper are responsive to vertical retinal slip, and we report for the first time that the nBOR1 and LM are involved in processing horizontal retinal slip. These results suggest that homologous structures in birds and mammals serve analogous functions in the optokinetic system.
L
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Fig. 1. Horizontal brain sections after slow horizontal movement stimulation, a: autoradiogram displays label in LM (double arrow) and in nBOR1 (single arrow), b: adjacent stained section, x 5.8. Fig. 2. Transverse brain section after slow vertical movement stimulation, a: autoradiogram of section at the level of nBOR (arrows) reveals heavier labeling in the left nBOR which was contralateral to eye viewing up vertical movement, b: same section stained after autoradiogram was made. x 4.3.
457 Chicks, 3-7 days old, were placed in a container fitted with a device to restrain the head. The container was suspended in an evenly lit striped drum rotating either vertically or horizontally at 2-4 °/sec. In experiments using vertical whole-field movement the control eye was either covered with a translucent occluder or exposed to stationary stripes oriented vertically. In one experiment using horizontal whole-field movement the control eye was covered by an occluder; otherwise, both eyes were open so that one eye viewed movement in the temporal to nasal direction, and the other eye viewed movement in the nasal to temporal direction. Two animals viewed upward movement, two animals viewed downward movement and 6 animals viewed horizontal movement. After a 10 min pretrial in the rotating drum, birds were removed, injected intracardially with [14C]2-deoxyglucose (0.16 #Ci/g) and returned to the apparatus. After a 45 min trial, animals were either perfused with 3 ~ paraformaldehyde in 0.1 M phosphate buffer (pH 7.4) or decapitated without prior fixation. Brains were immedia-
nBORI nBOR Fig. 3. Tracings of autoradiograms of transverse brain sections from chick viewing slow horizontal movement. Sectionsrun in a caudal to rostral direction from the bottom to the top of the page. Heavy asymmetric labeling seen in the nBORI can be traced rostrally until it appears to merge with the label of the LM. Abbreviations for all figures: LH, lamina hyperstriatica, LM, nucleus lentiformis mesencephali; nBOR, nucleus of the basal optic root; nBORl, nucleus of the basal optic root, pars lateralis; Rt, nucleus rotundus; TeO, rectum opticum, TrO, tractus opticus.
458 tely removed and frozen in isopentane cooled by liquid nitrogen. Cryostat sections (20 #m) were placed against X-ray film. After autoradiography the same sections or adjacent sections were stained with cresyl violet and were used to identify the nuclei that had accumulated label. Photographs of the autoradiograms are presented here as negatives. Autoradiograms were examined for differences in density in structures on the right and left sides of the diencephalon and mesencephalon. Since the optic nerves are crossed, an increase in metabolic activity produced by stimulation of one eye should be seen in the contralateral brain. In experiments using vertical movement, the nBORd and nBOR proper contralateral to the stimulated eye displayed heavier labeling in the autoradiograms (Fig. 2). In one experiment, when the difference in labeling between the two sides of the brain was measured using a densitometer (Joyce Loebl 3CS), the average difference in optical density was 0.09 A (t z 3.03, P~0.02). In all 4 experiments conducted, the density of label in the control nBOR was always less than that of the experimental nBOR whether the control eye viewed stationary stripes or was covered with a translucent occluder. The LM on both sides of the brain were labeled equally. Although electrophysiological studies indicate that neurons in nBORd respond to upward movement and those in nBOR proper to downward and anterior movement, this distinction was not apparent in our original experiments; however, results of more recent experiments using 3-4-week-old birds indicate that nBORd is differentially labeled during upward movement while nBOR proper was differentially labeled during downward movement. Slow horizontal temporal to nasal movement caused the contralateral LM to become heavily labeled in all 6 experiments conducted (Figs. 1 and 3). Labeling in the opposite LM, which received retinal projections from the eye viewing nasal to temporal movement, either was very light or could not be detected, even though the LM could be seen in the adjacent stained sections. In contrast, labeling o f n B O R d and nBOR proper on both sides of the brain appeared equal. These results suggest that the LM and NOT may serve similar physiological functions in addition to being homologous to one another 9,1°. The finding of little or no discernible label in the LM presented with nasal to temporal movement is in agreement with the finding that in mammals, cells of the NOT are excited by movement in the temporal to nasal direction and inhibited by movement in the opposite direction 5,7. In chickens 21, as in rabbits 4, horizontal OKN displays the same asymmetry, being stronger in the temporal to nasal direction. In addition, the contralateral nBOR1 became differentially labeled in response to the horizontal movement stimulus in 4 of the 6 experiments whereas no differences in the labeling of the other regions of the nBOR complex on the two sides of the brain could be distinguished. The strong labeling of the nBOR1 in response to horizontal movement suggests that the nBORi is homologous to the D T N of mammals. Surprisingly, when the density of label in nBOR1 was traced rostrally section by section, it appeared continuous with the label in LM (Fig. 3); histological examination of sections from which the autoradiograms were made confirmed that these two nuclei merge with one another.
459 I n s u m m a r y , we have s h o w n t h a t the L M is similar in function to the N O T . I n a d d i t i o n , this study, t a k e n t o g e t h e r with the e l e c t r o p h y s i o l o g i c a l studies, suggests t h a t each division o f the n B O R processes different directions o f retinal slip; the n B O R I r e s p o n d s to h o r i z o n t a l m o v e m e n t , the n B O R d to vertical u p w a r d m o v e m e n t a n d the n B O R p r o p e r to d o w n w a r d a n d a n t e r i o r m o v e m e n t . These results are consistent with the i d e a t h a t each o f the 3 nuclei r e s p o n d to the same directions o f m o v e m e n t as the 3 semicircular canals 3,17,18. Finally, o u r results suggest t h a t the displaced retinal ganglion cells which project directly to the n B O R c o m p l e x 8,16 m a y be divided on the basis o f their function into 3 physiological subtypes each o f which r e s p o n d s to a different f o r m o f retinal slip a n d each o f which projects to a p a r t i c u l a r division o f the n B O R complex. W e are grateful to Drs. N i c h o l a s Brecha a n d A n t o n Reiner for helping in the identification o f neural structures a n d to Dr. Reiner for m a k i n g the densitometric readings. This w o r k was s u p p o r t e d by grants f r o m the N a t i o n a l Eye Institute, EY02937 a n d f r o m N I H , 5 S07 R R 07132.
1 Ariens Kappers, C. U., Huber, G. C. and Crosby, E. C., The Comparative Anatomy of the Nervous System of Vertebrates, Including Man, Hafner, New York, 1939. 2 Burns, S. and Wallman, J., Neurons in the nucleus of the basal optic root (accessory optic system) of birds respond preferentially to vertical stimulus movement, Neurosci. Abstr., 5 (1979) 779. 3 Burns, S. and Wallman J., Relations of single unit properties to the oculomotor function of the nucleus of the basal optic root (accessory optic system) in chickens, Exp. Brain Res., in press. 4 Collewijn, H., The optokinetic system of the rabbit, Docum. ophthaL (Den Haag), 30 (1971) 205-226. 5 Collewijn, H., Direction-selective units in the rabbit's nucleus of the optic tract, Brain Research, 100 (1975) 489-508. 6 Collewijn, H., Ocuiomotor areas in the rabbit's midbrain and pretectum, J. NeurobioL, 6 (1975) 3-22. 7 Hoffmann, K. P. and Schoppmann, A., Retinal input to direction selective cells in the nucleus tractus opticus of the cat, Brain Research, 99 (1975) 359-366. 8 Karten, H. J., Fite, K. V. and Brecha N., Specific projection of displaced retinal ganglion ceils upon the accessory optic system in the pigeon (Columba livia). Proc. nat. Acad. Sci. (Wash.), 74 (1977) 1753-1756. 9 Kuhlenbeck, H., The development and structure of the pretectai cell masses in the chick, J. comp. NeuroL, (1939) 361-387. 10 Kuhlenbeck, H. and Miller, R. N., The pretectal region of the rabbit's brain, J. comp. NeuroL, 76 (1942) 323-365. 11 Marburg, O., Basale Opticuswurzel und Tractus peduncularis transversus. Arb. neurol, lnst. Univ. Wein. 10 (1903) 66-80. 12 Morgan, B. and Frost, B. J., Single unit behavioral assessment of ectomamillary nucleus function, NeuroscL Abstr., 5 (1979) 799. 13 Morgan, B. and Frost, B. J., Visual response characteristics of pigeon ectomamillary nucleus neurons, Exp. Brain Res., in press. 14 Oyster, C. W. and Barlow, H. B., Direction-selective units in rabbit retina: distribution of preferred directions, Science, 155 (1967) 841-842. 15 Oyster, C. W., Takahashi, E. and Collewijn, H., Direction-selective ganglion cells and control of optokinetic nystagmus in the rabbit, Vision Res., 12 (1972) 183-193. 16 Reiner, A., Brecha, N. and Karten, H. J., A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken, Neuroscience, 4 (1979) 1679-1688.
460 17 Simpson, J. I. and Hess, R., Complex and simple visual messages in the flocculus. In R. Baker and A. Berthoz (Eds.), Control of Gaze by Brain Stem Neurons, Elsevier/North-Holland Biomedical Press, pp. 351-360, 1977. 18 Simpson, J. I., Soodak, R. E. and Hess, R., The accessory optic system and its relation to the vestibulocerebellum. In R. Granit and O. Pompeiano (Eds.), Reflex Control of Posture and Movement, Progress in Brain Research, 50, 1979, pp. 715-724. 19 Sokoloff, L., Reivich, M., Kennedy, C., Des Rosiers, M. H., Patlak, C. S., Pettigrew, K. D., Sakurada, O. and Shinohara, M., The (14C) deoxyglucose method for measurement of local cerebral glucose utilization: theory, procedure and normal values in the conscious and anesthetized albino rat, J. Neurochem., 28 (1977) 897-916. 20 Walley, R. E., Receptive fields in the accessory optic system of the rabbit, Exp. neurol., 17 (1967) 27~,3. 21 Wallman, J., Turkel, J., Eastzer, D. H. and Hin-Kiu, M., Interactions between the eyes in optokinetic nystagmus of chickens, Neurosci. Abstr., 3 (1977) 158.
455
Identification of avian brain regions responsive to retinal slip using 2-deoxyglucose
OLIVIA C. McKENNA and JOSH WALLMAN Department of Biology, City College of the City University of New York, New York, N.Y. 10031 (U.S.A.)
(Accepted November 13th, 1980) Key words: accessory optic system -- pretectum -- retinal slip - - optokinetic nystagmus
In optokinetic nystagmus (OKN) retinal slip, that is, movement of the visual world on the retina, results in stabilizing eye movements which reduce the retinal slip velocity almost to zero. The visual input for this compensatory reflex seems to be transmitted along anatomically distinct pathways to the pretectal nuclei and accessory optic system in both birds and mammals. In mammals, one of the pretectal nuclei, the nucleus of the optic tract (NOT), appears to receive visual input necessary for horizontal O K N from a class of retinal ganglion cells that respond to slow horizontal movement and presumably project directly to the NOTS,7,15. Cells of the NOT are excited by slow whole-field horizontal movement in a temporal to nasal direction and either are not activated or are inhibited by movement in the opposite directionS, 7. The most convincing evidence for the role of NOT is the finding that electrical stimulation of the NOT produced horizontal O K N while lesioning the nucleus eliminated this type of nystagmus 6. In the mammalian accessory optic system, the medial and lateral terminal nuclei ( M T N and L T N respectively), appear to be involved in retinal signalling of vertical OKN. Retinal ganglion cells that are direction-selective and respond to slow stimulus movement14,15 are thought to terminate in the MTN. The cells of the M T N have large receptive fields and respond to slow vertical stimuli moving upward and posteriorlS, 20. Physiological properties of LTN are similar except that the cells prefer downward and posterior movement. The third terminal nucleus, the dorsal nucleus (DTN), is best modulated by horizontal movement in a temporal to nasal direction, a property of cells in the NOTS,7, is. In birds the nuclei considered homologous to the mammalian accessory terminal nuclei are the nuclei of the basic optic root (nBOR) 1,11which consist of the nBOR pars dorsalis (nBORd), nBOR pars lateralis (nBOR1) and the nBOR proper. As in mammals, two of the three nuclei appear to receive vertical, or near vertical, retinal slip signals, as shown by electrophysiological studiesZ,a,12,1L Neurons of the nBOR responsive to slow whole-field upward movement are concentrated in the nBORd while neurons responsive to slow whole-field downward and anterior movement are
456 concentrated in the nBOR proper 3. Electrophysiological properties of neurons in the nBORI have not been reported. The suggestion has been made that the lentiform nucleus of the mesencephalon (LM) of birds is homologous to the NOT of mammals on the basis of its position in the diencephalong, 10. Nothing, however, is known about whether the LM is similar in function to NOT. The present study was undertaken to reveal what nuclei in the avian brain are involved in signalling horizontal retinal slip and to confirm a role of the nBOR in signalling vertical retinal slip by using the metabolic mapping technique of Sokoloff et a119. The chick is a particularly useful experimental animal for this type of study since its optic nerves are completely or almost completely crossed and its eyes placed laterally; consequently, different visual stimuli presented to each eye would be expected to result in differences in labeling of equivalent structures on each side of the brain. Here, we confirm that the nBORd and nBOR proper are responsive to vertical retinal slip, and we report for the first time that the nBOR1 and LM are involved in processing horizontal retinal slip. These results suggest that homologous structures in birds and mammals serve analogous functions in the optokinetic system.
L
. . . . . . . . . . . .
Fig. 1. Horizontal brain sections after slow horizontal movement stimulation, a: autoradiogram displays label in LM (double arrow) and in nBOR1 (single arrow), b: adjacent stained section, x 5.8. Fig. 2. Transverse brain section after slow vertical movement stimulation, a: autoradiogram of section at the level of nBOR (arrows) reveals heavier labeling in the left nBOR which was contralateral to eye viewing up vertical movement, b: same section stained after autoradiogram was made. x 4.3.
457 Chicks, 3-7 days old, were placed in a container fitted with a device to restrain the head. The container was suspended in an evenly lit striped drum rotating either vertically or horizontally at 2-4 °/sec. In experiments using vertical whole-field movement the control eye was either covered with a translucent occluder or exposed to stationary stripes oriented vertically. In one experiment using horizontal whole-field movement the control eye was covered by an occluder; otherwise, both eyes were open so that one eye viewed movement in the temporal to nasal direction, and the other eye viewed movement in the nasal to temporal direction. Two animals viewed upward movement, two animals viewed downward movement and 6 animals viewed horizontal movement. After a 10 min pretrial in the rotating drum, birds were removed, injected intracardially with [14C]2-deoxyglucose (0.16 #Ci/g) and returned to the apparatus. After a 45 min trial, animals were either perfused with 3 ~ paraformaldehyde in 0.1 M phosphate buffer (pH 7.4) or decapitated without prior fixation. Brains were immedia-
nBORI nBOR Fig. 3. Tracings of autoradiograms of transverse brain sections from chick viewing slow horizontal movement. Sectionsrun in a caudal to rostral direction from the bottom to the top of the page. Heavy asymmetric labeling seen in the nBORI can be traced rostrally until it appears to merge with the label of the LM. Abbreviations for all figures: LH, lamina hyperstriatica, LM, nucleus lentiformis mesencephali; nBOR, nucleus of the basal optic root; nBORl, nucleus of the basal optic root, pars lateralis; Rt, nucleus rotundus; TeO, rectum opticum, TrO, tractus opticus.
458 tely removed and frozen in isopentane cooled by liquid nitrogen. Cryostat sections (20 #m) were placed against X-ray film. After autoradiography the same sections or adjacent sections were stained with cresyl violet and were used to identify the nuclei that had accumulated label. Photographs of the autoradiograms are presented here as negatives. Autoradiograms were examined for differences in density in structures on the right and left sides of the diencephalon and mesencephalon. Since the optic nerves are crossed, an increase in metabolic activity produced by stimulation of one eye should be seen in the contralateral brain. In experiments using vertical movement, the nBORd and nBOR proper contralateral to the stimulated eye displayed heavier labeling in the autoradiograms (Fig. 2). In one experiment, when the difference in labeling between the two sides of the brain was measured using a densitometer (Joyce Loebl 3CS), the average difference in optical density was 0.09 A (t z 3.03, P~0.02). In all 4 experiments conducted, the density of label in the control nBOR was always less than that of the experimental nBOR whether the control eye viewed stationary stripes or was covered with a translucent occluder. The LM on both sides of the brain were labeled equally. Although electrophysiological studies indicate that neurons in nBORd respond to upward movement and those in nBOR proper to downward and anterior movement, this distinction was not apparent in our original experiments; however, results of more recent experiments using 3-4-week-old birds indicate that nBORd is differentially labeled during upward movement while nBOR proper was differentially labeled during downward movement. Slow horizontal temporal to nasal movement caused the contralateral LM to become heavily labeled in all 6 experiments conducted (Figs. 1 and 3). Labeling in the opposite LM, which received retinal projections from the eye viewing nasal to temporal movement, either was very light or could not be detected, even though the LM could be seen in the adjacent stained sections. In contrast, labeling o f n B O R d and nBOR proper on both sides of the brain appeared equal. These results suggest that the LM and NOT may serve similar physiological functions in addition to being homologous to one another 9,1°. The finding of little or no discernible label in the LM presented with nasal to temporal movement is in agreement with the finding that in mammals, cells of the NOT are excited by movement in the temporal to nasal direction and inhibited by movement in the opposite direction 5,7. In chickens 21, as in rabbits 4, horizontal OKN displays the same asymmetry, being stronger in the temporal to nasal direction. In addition, the contralateral nBOR1 became differentially labeled in response to the horizontal movement stimulus in 4 of the 6 experiments whereas no differences in the labeling of the other regions of the nBOR complex on the two sides of the brain could be distinguished. The strong labeling of the nBOR1 in response to horizontal movement suggests that the nBORi is homologous to the D T N of mammals. Surprisingly, when the density of label in nBOR1 was traced rostrally section by section, it appeared continuous with the label in LM (Fig. 3); histological examination of sections from which the autoradiograms were made confirmed that these two nuclei merge with one another.
459 I n s u m m a r y , we have s h o w n t h a t the L M is similar in function to the N O T . I n a d d i t i o n , this study, t a k e n t o g e t h e r with the e l e c t r o p h y s i o l o g i c a l studies, suggests t h a t each division o f the n B O R processes different directions o f retinal slip; the n B O R I r e s p o n d s to h o r i z o n t a l m o v e m e n t , the n B O R d to vertical u p w a r d m o v e m e n t a n d the n B O R p r o p e r to d o w n w a r d a n d a n t e r i o r m o v e m e n t . These results are consistent with the i d e a t h a t each o f the 3 nuclei r e s p o n d to the same directions o f m o v e m e n t as the 3 semicircular canals 3,17,18. Finally, o u r results suggest t h a t the displaced retinal ganglion cells which project directly to the n B O R c o m p l e x 8,16 m a y be divided on the basis o f their function into 3 physiological subtypes each o f which r e s p o n d s to a different f o r m o f retinal slip a n d each o f which projects to a p a r t i c u l a r division o f the n B O R complex. W e are grateful to Drs. N i c h o l a s Brecha a n d A n t o n Reiner for helping in the identification o f neural structures a n d to Dr. Reiner for m a k i n g the densitometric readings. This w o r k was s u p p o r t e d by grants f r o m the N a t i o n a l Eye Institute, EY02937 a n d f r o m N I H , 5 S07 R R 07132.
1 Ariens Kappers, C. U., Huber, G. C. and Crosby, E. C., The Comparative Anatomy of the Nervous System of Vertebrates, Including Man, Hafner, New York, 1939. 2 Burns, S. and Wallman, J., Neurons in the nucleus of the basal optic root (accessory optic system) of birds respond preferentially to vertical stimulus movement, Neurosci. Abstr., 5 (1979) 779. 3 Burns, S. and Wallman J., Relations of single unit properties to the oculomotor function of the nucleus of the basal optic root (accessory optic system) in chickens, Exp. Brain Res., in press. 4 Collewijn, H., The optokinetic system of the rabbit, Docum. ophthaL (Den Haag), 30 (1971) 205-226. 5 Collewijn, H., Direction-selective units in the rabbit's nucleus of the optic tract, Brain Research, 100 (1975) 489-508. 6 Collewijn, H., Ocuiomotor areas in the rabbit's midbrain and pretectum, J. NeurobioL, 6 (1975) 3-22. 7 Hoffmann, K. P. and Schoppmann, A., Retinal input to direction selective cells in the nucleus tractus opticus of the cat, Brain Research, 99 (1975) 359-366. 8 Karten, H. J., Fite, K. V. and Brecha N., Specific projection of displaced retinal ganglion ceils upon the accessory optic system in the pigeon (Columba livia). Proc. nat. Acad. Sci. (Wash.), 74 (1977) 1753-1756. 9 Kuhlenbeck, H., The development and structure of the pretectai cell masses in the chick, J. comp. NeuroL, (1939) 361-387. 10 Kuhlenbeck, H. and Miller, R. N., The pretectal region of the rabbit's brain, J. comp. NeuroL, 76 (1942) 323-365. 11 Marburg, O., Basale Opticuswurzel und Tractus peduncularis transversus. Arb. neurol, lnst. Univ. Wein. 10 (1903) 66-80. 12 Morgan, B. and Frost, B. J., Single unit behavioral assessment of ectomamillary nucleus function, NeuroscL Abstr., 5 (1979) 799. 13 Morgan, B. and Frost, B. J., Visual response characteristics of pigeon ectomamillary nucleus neurons, Exp. Brain Res., in press. 14 Oyster, C. W. and Barlow, H. B., Direction-selective units in rabbit retina: distribution of preferred directions, Science, 155 (1967) 841-842. 15 Oyster, C. W., Takahashi, E. and Collewijn, H., Direction-selective ganglion cells and control of optokinetic nystagmus in the rabbit, Vision Res., 12 (1972) 183-193. 16 Reiner, A., Brecha, N. and Karten, H. J., A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken, Neuroscience, 4 (1979) 1679-1688.
460 17 Simpson, J. I. and Hess, R., Complex and simple visual messages in the flocculus. In R. Baker and A. Berthoz (Eds.), Control of Gaze by Brain Stem Neurons, Elsevier/North-Holland Biomedical Press, pp. 351-360, 1977. 18 Simpson, J. I., Soodak, R. E. and Hess, R., The accessory optic system and its relation to the vestibulocerebellum. In R. Granit and O. Pompeiano (Eds.), Reflex Control of Posture and Movement, Progress in Brain Research, 50, 1979, pp. 715-724. 19 Sokoloff, L., Reivich, M., Kennedy, C., Des Rosiers, M. H., Patlak, C. S., Pettigrew, K. D., Sakurada, O. and Shinohara, M., The (14C) deoxyglucose method for measurement of local cerebral glucose utilization: theory, procedure and normal values in the conscious and anesthetized albino rat, J. Neurochem., 28 (1977) 897-916. 20 Walley, R. E., Receptive fields in the accessory optic system of the rabbit, Exp. neurol., 17 (1967) 27~,3. 21 Wallman, J., Turkel, J., Eastzer, D. H. and Hin-Kiu, M., Interactions between the eyes in optokinetic nystagmus of chickens, Neurosci. Abstr., 3 (1977) 158.