- Email: [email protected]
The Anatomic Basis for Certain Reflex and Automatic Eye Movements*
THE ANATOMIC BASIS FOR CERTAIN REFLEX AND AUTOMATIC EYE MOVEMENTS* JOHN WOODWORTH HENDERSON,1"
Ann Arboi ·, Michigan
With progressive phylogenetic development, the dominant level of control of eye movement ascends from lower to higher brain centers and finally to the cerebral cortex. One of the more primitive mechanisms governing ocular movement is that of the vestibular system. The interaction between the vestibular nuclei and the nuclear masses serving the extraocular muscles by way of the median longitudinal fasciculi is present in all vertebrates which have eyes and ears, and extends back in the scale to certain of the Cyclostomes. As cerebral cortex develops, it assumes a controlling position over the more primitive vestibulo-ocular reflexes. Cortical inhibition has been shown to occur in the rabbit utilizing rotational and postrotational nystagmus as an indicator (Henderson, 1947). In this series of experiments definite inhibition of postrotational nystagmus was produced by allowing ocular function during rotation, probably acting by means of cortical participation in the ocular movement. Such inhibition can conceivably be either voluntary or automatic depending upon the needs of the organism at the moment. Midbrain dominance over extraocular movement reaches its highest expression in birds, where "consciousness" is said to lie at the mesencephalic level. Here all the sensory stimuli from the body, as well as visual, vestibular, and auditory impulses, are channelled into the tectum of the midbrain, and resultant responses are carried out by way of the tectospinal and tectotegmentospinal pathways. Since the "brain" of the bird above the level of the midbrain consists chiefly of highly developed basal ganglia, control from these higher centers is rela* From the Department of Ophthalmic Surgery, University of Michigan Medical School. t Walter R. Parker Scholar in Ophthalmology.
M.D.
tively nonspecific. In mammals, this pattern is reflected by the presence of direct fibers from the retinas which reach the tectum by way of the optic nerves without the interposition of a cortical arc. This makes possible subcortical ocular reflex movements. The midbrain pattern for ocular movement has been established anatomically in mammals by various workers. This is related to the arrangement of the incoming direct optic-nerve fibers on the one hand, and the nuclear arrangement of the oculomotor and trochlear nerves on the other. The nuclear arrangement is such that the impulse for elevating the eyes and raising the upper lids arises in the rostral portions of the oculomotor nuclei. The stimulus for turning the eyes downward takes origin in the more caudal portions (the neighboring trochlear nuclei also taking part). More recent studies (Bender and Weinstein, 1943, Szentagothai, 1942) show a partial reversal of the previously accepted anatomic pattern. These latter investigations have been based upon direct electrical stimulation using a Horsley-Clark type of apparatus where presumably the results could be produced by effects gained through the median longitudinal fasciculi, in which the nuclear masses are embedded. The position of the eyes after destruction of the individual nuclei was not mentioned by these workers. Experimental studies of the projection of the retinal quadrants on the optic tectum in the rabbit (Brouwer and Zeeman, 1926, Brouwer, 1927), and to a lesser extent in the monkey, have indicated that the inferior quadrants, which are stimulated from the superior visual field, are projected by the optic tracts on the medial and rostral portions of the superior colliculi, and that the superior quadrants, which are stimulated from the inferior visual field, are projected
232
ANATOMIC BASIS FOR EYE MOVEMENTS
on the lateral and caudal portions of the optic tectum. A comparable pattern of projection on this midbrain region was obtained in the rat by Lashley (1934). This pattern would confirm the nuclear localization of the earlier anatomic workers. It acts by direct oculomesencephalic reflex connections in lower mammals without the interposition of a cortical arc. Such direct fiber connections are fewer in number in primates, but it is probable that the pattern is much the same in the monkey. These connections seem to be inoperative or very greatly reduced in man. Nevertheless, their presence and arrangement in lower mammalian forms would serve to confirm the midbrain nuclear arrangement of the earlier workers. In primates, where the direct oculomidbrain reflex connections are much less important, a cortical arc assumes the major responsibility for reflex ocular movement. This is in disagreement with the older view that many reflex ocular movements in primates have a subcortical origin. Thus automatic eye movements at a cortical level appear to supersede and control the function of both the vestibular and midbrain arcs. Such movements are based upon visual stimuli which reach Area 17 (the striate cortex) by way of the visual pathways. Experimental work on the monkey (Crosby and Henderson, 1948) shows that a distinct pattern of cortical localization exists in both Area 17 and in Area 19 (the parastriate cortex) which can be related anatomically and functionally to the more primitive midbrain arrangement. The experiments were performed using a very light ether anesthesia and stimulating the brain areas concerned with a faradic current. The directions of ocular movement were recorded in each instance. Stimulation of the portion of the striate cortex above the calcarine fissure (F, fig. 1) produced a combined conjugate movement down and to the opposite side; of that below the fissure (E, fig. 1), a conjugate
233
movement up and to the opposite side. This result was that expected from the known cortical pattern of termination of the visual pathway, and confirmed the work of Walker and Weaver (1940). Area 19 (the parastriate cortex) was shown to have a definite pattern of ocular movement in response to stimulation. Upper Area 19 (A, fig. 1) produced upward conjugate movement, upper-intermediate Area 19 (Á', fig. 1) gave movements obliquely upward and toward the opposite side, and middle Area 19 (B, fig. 1) elicited conjugate deviation horizontally toward the opposite side. Stimulation of lower-intermediate Area 19 ( C , fig. 1) produced a conjugate deviation obliquely downward and toward the opposite side, and lower Area 19 (C, fig. 1) gave conjugate downward movement. It must be emphasized that such results required a level of ether anesthesia just below the point where voluntary ocular movement would occur and where the blink reflex to stimulation of the cilia was still present. Deeper anesthesia abolished the upward movements first, then the downward, leaving finally only the horizontal conjugate deviation. Sodium pentobarbital anesthesia was found to carry the monkeys to too deep a level to elicit satisfactory responses. This difference in level of anesthesia may explain the classical view that Area 19 produces only conjugate deviation of the eyes to the opposite side such as was described by Foerster (1931 and elsewhere) in man. The fiber pathways which link Areas 17 and 19 to the tectum of the midbrain have been termed the internal corticotectal tracts (Crosby and Henderson, 1948). Those from the striate area are designated the occipital division of the internal corticotectal tract, and are further subdivided into dorsal and ventral divisions on the basis of their origin from either above or below the calcarine fissure. These tracts sweep forward in a layer just outside the visual radiations and parallel them as far forward as the pulvinar of the
234
JOHN WOODWORTH HENDERSON
Fig. 1 (Henderson). The left side of the brain of a Macaca mulatta as shown in a photograph ( χ À . 8 ) . Areas 17, 18, 19, and 21 are designated. On Areas 17 and 19 the various points from which eye movements were elicited are indicated by letters (see t e x t ) . (Reproduced by permission of E. C. Crosby and J. W. Henderson : J. Comp. Neurol., 88:53-92,1948.)
ABBREVIATIONS FOR FIGURES
aud. a., auditory area, calc. f., calcarine fissure, caud. n., caudate nucleus, cer. ped., cerebral peduncle, cerebel., cerebellum, corp. cal., corpus callosum. cort. teg. tr., corticotegmental tract, cort. tect. tr., aud. div., corticotectal tract, auditory division, ext. cort. tect. tr., external corticotectal tract. F, fornix. fim., fimbria. hip., hippocampus, hip. g., hippocampal gyrus. int. cort. tect. tr., oc. div. dors, p., internal corticotectal tract, occipital division, dorsal part, int. cort. tect. tr., oc. div. vent, p., internal corticotectal tract, occipital division, ventral part, int. cort. tect. tr., preoc. div. dors, p., internal corticotectal tract, preoccipital division, dorsal part, int. cort. tect. tr., preoc. div., vent, p., internal
thalamus. Here they turn medially across the internal capsule, through the pulvinar, and
corticotectal tract, preoccipital division, ventral part. m. 1. f., medial longitudinal fasciculus. med. lem., medial lemniscus. med. tect. sp. tr., media] tectospinal tract. n. I l l , oculomotor nucleus. op. tr., optic tract. ped. inf. col., peduncle of inferior colliculus. pul., pulvinar. str. med. prof., deep medullary stratum. str. term., stria terminalis. sub. nig., substantia nigra. sup. cerebel. dec, decussation of superior cerebellar peduncle. sup. temp, f., superior temporal fissure. tect. oc. tr., tecto-oculomotor tract. tect. pont, tr., tectopontine tract. tect. teg. tr., tectotegmental tract. vis. rad., visual radiations. x, termination of occipital division of internal corticotectal tract in superior colliculus. y, termination of preoccipital division of internal corticotectal tract in superior colliculus.
terminate in the tectum of the midbrain (fig. 2). Those from the upper calcarine
235
ANATOMIC BASIS FOR EYE MOVEMENTS
pul. .
«gt.cort.tect.tr.
itr.imd.prof^
-
.
int.coft.tect.tr. mt.cort.ttct.tr. pr»oc.di».dor«p.»* oc.di'.don.p. .oc.d IT.Tent.p. int.cort.teet ^preoc.di'.Ttnt.p.
■
, med.tect »p.tr. tec r.oc.tr.V J
tict.ponl.lr.
ir*i»Wrai·
nlMjj
Top.tr.
|cort.trct.tr.,aud di1
i rod
* **
ÃÚÐÉ
R mid Icm
*■
>ped mt.col. crrped.
. utp.ccrc
JdecJ
T1-
1 jÊ^fJtfJk
HRltbuig
9
f'
I
j^SBSCfl m
Fig. 2 (Henderson). A photomicrograph of a section near the rostral end of the superior colliculus from a transverse series of a Macaca mulatta brain stained by the Weil technique (X4). For a more comprehensive series see Crosby and Henderson, 1948. (Reproduced by permission of E. C. Crosby and J. W. Henderson : J. Comp. NeuroL, 88.53-92, 1948.) See Fig. 1 for explanation of abbreviations. area (dorsal division) reach the caudal portions of the tectum, and those from the lower calcarine area terminate in the more rostral tectum of the midbrain. Thus the dorsal division relates inferior visual field, superior calcarine area, and caudal tectum to the more caudal portion of the oculomotor complex. Conversely, the ventral division relates superior visual field, inferior calcarine area,
and rostral tectum to the more rostral portion of the oculomotor nucleus. The expected responses in reflex ocular deviation to stimuli lying in the visual field can therefore be related anatomically. The internal corticotectal tracts from Area 19 have been designated the preoccipital division, which likewise is divided into dorsal and ventral parts based on origin either from
236
JOHN WOODWORTH HENDERSON
upper or lower parastriate cortex (fig. 2). These fibers course forward to pulvinar levels along with the occipital division in the same layer just outside the visual radiations. The dorsal portion can be traced to the rostral tectum, while the ventral part reaches the more caudal tectum. Thus an interrelationship between upper Area 19 and rostral oculomotor nucleus can be seen, and, conversely, between lower Area 19 and caudal oculomotor nucleus. The pathways described were traced both in normal anatomic preparations and by experimental degeneration. It has previously been noted (Kronfeld, 1929) that they follow the visual radiations forward, but the fact that cortical localization can be related to the anatomic pattern of arrangement of the extraocular muscle nuclei has, to the best of our knowledge, not been heretofore noted. It is interesting that the termination of such fiber tracts fails to confirm the more recent work on the arrangement of the oculomotor nuclear complex. The parallel course of the tecto-oculomotor fibers which carry the impulses into the various portions of the oculomotor nucleus speaks against any reversal of pattern within the midbrain itself. The fact that the pattern described for Area 19 is inverted from that of Area 17 can be explained by the presence of short association bundles which can be seen to connect lower Area 17 with upper Area 19, and vice versa. Both the occipital and preoccipital divisions of the internal corticotectal system were seen to give off fibers which turned into the tegmentum of the midbrain without reaching the tectal areas (cort. teg. tr., fig. 2). These lay midway between the dorsal and ventral portions of both divisions in their course forward from the occipital lobe and presumably relate the areas for horizontal movement with the abducens complex by means of tegmental pathways. They could be traced with certainty only as far as the inferior collicular level.
Judged by the relatively great number of corticotectal and corticotegmental pathways, a large percentage of normal eye movements can be explained as visual automatisms— cortical, yet subconscious in a voluntary sense. This would include the movements subserving fixation, since it is well known that injury to Area 19 interferes with the holding of fixed gaze. McCulloch (1944) has shown that cortical conduction occurs from Area 8 of the frontal cortex to the parastriate area, but not in the opposite direction. This places the cortical centers for automatic eye movements under the control of the voluntary motor centers, with Area 8 able either to utilize the direct corticobulbar pathway to the brain stem, or to exert a modifying effect upon the cortical ocular automatisms by way of the parastriate area. It should be stressed that higher centers utilize previously laiddown mechanisms for the control of ocular movement. In each instance, the more primitive pattern can be recognized, but is made use of by more recent phylogenetic brain centers. It should be noted that there is a difference in level between the internal corticotectal fibers entering the tectum of the midbrain and the corticobulbar fibers which lie just above the cerebral peduncles. Since the fibers from the occipital lobe are more superficial in the colliculus, pressure downward from above should affect the reflex ocular movements much earlier than those which have a voluntary origin from Area 8 of the frontal lobe. Thus there should be a difference noted between command movements of the eyes and following movements in such an instance. University
Hospital.
The writer expresses his gratitude and indebtedness to Prof. Elizabeth Crosby for the use of the facilities of her department, both microscopic material and experimental animals. Were it not for her constant aid and collaboration this work could never have been completed.
ANATOMIC BASIS FOR EYE MOVEMENTS
237
REFERENCES
Bender, M. B., and Weinstein, W. A. : Functional representation in oculomotor and trochlear nuclei. Arch. Neurol. & Psychiat., 49 :98-106, 1943. Brouwer, B. : Anatomical, phylogenetical, and clinical studies on the central nervous system. Lecture I. The projection of the retina on the brain. The Herter Lectures, Johns Hopkins University School of Medicine. Baltimore, Williams & Wilkins, 1927. Brouwer, B., and Zeeman, W. P. C. : The projection of the retina in the primary optic neuron in monkeys. Brain, 49 :l-35,1926. Crosby, E. C, and Henderson, J. W. : The mammalian midbrain and isthmus region. Part II. Fiber connections of the superior colliculus. B. Pathways concerned in automatic eye movements. J. Comp. Neurol., 88:53-92, 1948. Foerster, O. : The cerebral cortex in man. Lancet, 221:309-312, 1931. Henderson, J. W. : Optokinetic and other factors modifying vestibular nystagmus. Arch. Ophth., 37:459-471,1947. Kronfeld, P. C. : The central visual pathway. Arch. Ophth., 2:709-732,1929. Lashley, K. S. : The mechanism of vision. VII. The projection of the retina upon the primary optic centers in the rat. J. Comp. Neurol., 59:341-373,1934. " McCulloch, W. S. : Cortico-cortical connections. Chapt. VIII in Precentral Motor Cortex (edited by P. C. Bucy). 111. Monographs in Medical Sciences, Urbana, 111., Illinois Press, 1944, v. 4, pp. 212-242. Szentagothai, J. : Die innere Gliederung des Oculomotoriuskernes. Arch. f. Psychiat., 115 :127-13S, 1942. Walker, A. E., and Weaver, T. A., Jr. : Ocular movements from the occipital lobe in the monkey. J. Neurophysiol., 3 :3S3-3S7,1940.
DISCUSSION
D R . D A V I D G. COGAN (Boston, Massachu-
setts) : I would like to ask two specific questions a n d I hope they weren't covered in the paper. I w a s so interested in some of the parts I may have lapsed in the others. Did you mention what the threshold was in Areas 17 a n d 19? I t seems to m e there has been some conflict between what W a l k e r and Weaver and what others have found in the relative thresholds in 17 versus 18 and 19. Also, it seems to be anomalous that there should be such a reversal of vertical representation in 19 and 17. Y o u say that that is executed by means of intracortical association pathways but it seems to me curious in the economy of the nervous system that such a reversal should take place. D R . P . J. LEINFELDER ( I o w a City, I o w a ) : I want to congratulate D r . H e n d e r s o n on a very difficult piece of work. I am sure he has labored much more extensively than you might realize from seeing the few slides that he has shown. T h e importance of his contribution, I think, should not be estimated in terms of its applicability to any one lesion of the
nervous system, but rather in his confirmation of t h e intimate reflex association between vision, binocular vision, and the ocular motor system. H e h a s demonstrated the pathways that carry t h e impulses for adequate coordination of ocular movements a n d fixation. D R . P I E R R E D A N I S (Brussels, Belgium) :
I think the localization of the muscles he referred to is still open to question because I think you base your general opinion on •the work of Brouwer but you have other workers w h o gave a reverse pattern. Bach and von Biervliet gave a reverse pattern, too. D R . HENDERSON (closing) : I would like to answer D r . Cogan's questions first while I have them in m y mind more specifically. T h e difference in threshold actually does exist. I t is not something to be measured in any specific terms. If w e had t h e current and stimulation high enough, we would get movement which we attributed to A r e a 17 by a spread from A r e a 19, which was of that type. Also the work of W a l k e r and W e a v e r was performed under a light anesthesia, as I recall, which again brings the question of anesthesia into it.
238
JOHN WOODWORTH HENDERSON
The problem of the difference between Areas 17 and 19 bothered me, too. The pathways I think are there all right. There is no question about the association pathways being there but why two different areas so closely related should have inverse correlation with the midbrain arrangement I do not know. However, the fact that the stimulus which comes back and influences automatic movements comes from Areas 8 to 18 and then into 19 would indicate that perhaps 19 is more related to the voluntary centers while 17 is related to the visual receptive pattern. We know that there are the two different sets of pathways that run forward into the midbrain; this may have some bearing on the reversal of pattern. As Dr. Danis has said, there has been an argument about the nuclear localization all
along. This includes the work of Brouwer, of Bernheimer, of Starr, and several others, all of whom to a greater or lesser extent destroyed individual muscles and looked for individual nuclear degeneration. That, to the anatomist, is incontrovertible. To the physiologist, perhaps, it is not. It has also raised the question in my mind, which may be just "woolgathering," as to whether the inverse difference between these physiologic and anatomic patterns is going to make us change our conception of what is going on. Is the primary thing that is happening the contraction or is the primary thing the inhibition? Perhaps that might have some bearing on the ocular movements. I know there isn't a good way of reconciling the two views but we are hoping that further work will help in bringing the two views closer together.
Ann Arboi ·, Michigan
With progressive phylogenetic development, the dominant level of control of eye movement ascends from lower to higher brain centers and finally to the cerebral cortex. One of the more primitive mechanisms governing ocular movement is that of the vestibular system. The interaction between the vestibular nuclei and the nuclear masses serving the extraocular muscles by way of the median longitudinal fasciculi is present in all vertebrates which have eyes and ears, and extends back in the scale to certain of the Cyclostomes. As cerebral cortex develops, it assumes a controlling position over the more primitive vestibulo-ocular reflexes. Cortical inhibition has been shown to occur in the rabbit utilizing rotational and postrotational nystagmus as an indicator (Henderson, 1947). In this series of experiments definite inhibition of postrotational nystagmus was produced by allowing ocular function during rotation, probably acting by means of cortical participation in the ocular movement. Such inhibition can conceivably be either voluntary or automatic depending upon the needs of the organism at the moment. Midbrain dominance over extraocular movement reaches its highest expression in birds, where "consciousness" is said to lie at the mesencephalic level. Here all the sensory stimuli from the body, as well as visual, vestibular, and auditory impulses, are channelled into the tectum of the midbrain, and resultant responses are carried out by way of the tectospinal and tectotegmentospinal pathways. Since the "brain" of the bird above the level of the midbrain consists chiefly of highly developed basal ganglia, control from these higher centers is rela* From the Department of Ophthalmic Surgery, University of Michigan Medical School. t Walter R. Parker Scholar in Ophthalmology.
M.D.
tively nonspecific. In mammals, this pattern is reflected by the presence of direct fibers from the retinas which reach the tectum by way of the optic nerves without the interposition of a cortical arc. This makes possible subcortical ocular reflex movements. The midbrain pattern for ocular movement has been established anatomically in mammals by various workers. This is related to the arrangement of the incoming direct optic-nerve fibers on the one hand, and the nuclear arrangement of the oculomotor and trochlear nerves on the other. The nuclear arrangement is such that the impulse for elevating the eyes and raising the upper lids arises in the rostral portions of the oculomotor nuclei. The stimulus for turning the eyes downward takes origin in the more caudal portions (the neighboring trochlear nuclei also taking part). More recent studies (Bender and Weinstein, 1943, Szentagothai, 1942) show a partial reversal of the previously accepted anatomic pattern. These latter investigations have been based upon direct electrical stimulation using a Horsley-Clark type of apparatus where presumably the results could be produced by effects gained through the median longitudinal fasciculi, in which the nuclear masses are embedded. The position of the eyes after destruction of the individual nuclei was not mentioned by these workers. Experimental studies of the projection of the retinal quadrants on the optic tectum in the rabbit (Brouwer and Zeeman, 1926, Brouwer, 1927), and to a lesser extent in the monkey, have indicated that the inferior quadrants, which are stimulated from the superior visual field, are projected by the optic tracts on the medial and rostral portions of the superior colliculi, and that the superior quadrants, which are stimulated from the inferior visual field, are projected
232
ANATOMIC BASIS FOR EYE MOVEMENTS
on the lateral and caudal portions of the optic tectum. A comparable pattern of projection on this midbrain region was obtained in the rat by Lashley (1934). This pattern would confirm the nuclear localization of the earlier anatomic workers. It acts by direct oculomesencephalic reflex connections in lower mammals without the interposition of a cortical arc. Such direct fiber connections are fewer in number in primates, but it is probable that the pattern is much the same in the monkey. These connections seem to be inoperative or very greatly reduced in man. Nevertheless, their presence and arrangement in lower mammalian forms would serve to confirm the midbrain nuclear arrangement of the earlier workers. In primates, where the direct oculomidbrain reflex connections are much less important, a cortical arc assumes the major responsibility for reflex ocular movement. This is in disagreement with the older view that many reflex ocular movements in primates have a subcortical origin. Thus automatic eye movements at a cortical level appear to supersede and control the function of both the vestibular and midbrain arcs. Such movements are based upon visual stimuli which reach Area 17 (the striate cortex) by way of the visual pathways. Experimental work on the monkey (Crosby and Henderson, 1948) shows that a distinct pattern of cortical localization exists in both Area 17 and in Area 19 (the parastriate cortex) which can be related anatomically and functionally to the more primitive midbrain arrangement. The experiments were performed using a very light ether anesthesia and stimulating the brain areas concerned with a faradic current. The directions of ocular movement were recorded in each instance. Stimulation of the portion of the striate cortex above the calcarine fissure (F, fig. 1) produced a combined conjugate movement down and to the opposite side; of that below the fissure (E, fig. 1), a conjugate
233
movement up and to the opposite side. This result was that expected from the known cortical pattern of termination of the visual pathway, and confirmed the work of Walker and Weaver (1940). Area 19 (the parastriate cortex) was shown to have a definite pattern of ocular movement in response to stimulation. Upper Area 19 (A, fig. 1) produced upward conjugate movement, upper-intermediate Area 19 (Á', fig. 1) gave movements obliquely upward and toward the opposite side, and middle Area 19 (B, fig. 1) elicited conjugate deviation horizontally toward the opposite side. Stimulation of lower-intermediate Area 19 ( C , fig. 1) produced a conjugate deviation obliquely downward and toward the opposite side, and lower Area 19 (C, fig. 1) gave conjugate downward movement. It must be emphasized that such results required a level of ether anesthesia just below the point where voluntary ocular movement would occur and where the blink reflex to stimulation of the cilia was still present. Deeper anesthesia abolished the upward movements first, then the downward, leaving finally only the horizontal conjugate deviation. Sodium pentobarbital anesthesia was found to carry the monkeys to too deep a level to elicit satisfactory responses. This difference in level of anesthesia may explain the classical view that Area 19 produces only conjugate deviation of the eyes to the opposite side such as was described by Foerster (1931 and elsewhere) in man. The fiber pathways which link Areas 17 and 19 to the tectum of the midbrain have been termed the internal corticotectal tracts (Crosby and Henderson, 1948). Those from the striate area are designated the occipital division of the internal corticotectal tract, and are further subdivided into dorsal and ventral divisions on the basis of their origin from either above or below the calcarine fissure. These tracts sweep forward in a layer just outside the visual radiations and parallel them as far forward as the pulvinar of the
234
JOHN WOODWORTH HENDERSON
Fig. 1 (Henderson). The left side of the brain of a Macaca mulatta as shown in a photograph ( χ À . 8 ) . Areas 17, 18, 19, and 21 are designated. On Areas 17 and 19 the various points from which eye movements were elicited are indicated by letters (see t e x t ) . (Reproduced by permission of E. C. Crosby and J. W. Henderson : J. Comp. Neurol., 88:53-92,1948.)
ABBREVIATIONS FOR FIGURES
aud. a., auditory area, calc. f., calcarine fissure, caud. n., caudate nucleus, cer. ped., cerebral peduncle, cerebel., cerebellum, corp. cal., corpus callosum. cort. teg. tr., corticotegmental tract, cort. tect. tr., aud. div., corticotectal tract, auditory division, ext. cort. tect. tr., external corticotectal tract. F, fornix. fim., fimbria. hip., hippocampus, hip. g., hippocampal gyrus. int. cort. tect. tr., oc. div. dors, p., internal corticotectal tract, occipital division, dorsal part, int. cort. tect. tr., oc. div. vent, p., internal corticotectal tract, occipital division, ventral part, int. cort. tect. tr., preoc. div. dors, p., internal corticotectal tract, preoccipital division, dorsal part, int. cort. tect. tr., preoc. div., vent, p., internal
thalamus. Here they turn medially across the internal capsule, through the pulvinar, and
corticotectal tract, preoccipital division, ventral part. m. 1. f., medial longitudinal fasciculus. med. lem., medial lemniscus. med. tect. sp. tr., media] tectospinal tract. n. I l l , oculomotor nucleus. op. tr., optic tract. ped. inf. col., peduncle of inferior colliculus. pul., pulvinar. str. med. prof., deep medullary stratum. str. term., stria terminalis. sub. nig., substantia nigra. sup. cerebel. dec, decussation of superior cerebellar peduncle. sup. temp, f., superior temporal fissure. tect. oc. tr., tecto-oculomotor tract. tect. pont, tr., tectopontine tract. tect. teg. tr., tectotegmental tract. vis. rad., visual radiations. x, termination of occipital division of internal corticotectal tract in superior colliculus. y, termination of preoccipital division of internal corticotectal tract in superior colliculus.
terminate in the tectum of the midbrain (fig. 2). Those from the upper calcarine
235
ANATOMIC BASIS FOR EYE MOVEMENTS
pul. .
«gt.cort.tect.tr.
itr.imd.prof^
-
.
int.coft.tect.tr. mt.cort.ttct.tr. pr»oc.di».dor«p.»* oc.di'.don.p. .oc.d IT.Tent.p. int.cort.teet ^preoc.di'.Ttnt.p.
■
, med.tect »p.tr. tec r.oc.tr.V J
tict.ponl.lr.
ir*i»Wrai·
nlMjj
Top.tr.
|cort.trct.tr.,aud di1
i rod
* **
ÃÚÐÉ
R mid Icm
*■
>ped mt.col. crrped.
. utp.ccrc
JdecJ
T1-
1 jÊ^fJtfJk
HRltbuig
9
f'
I
j^SBSCfl m
Fig. 2 (Henderson). A photomicrograph of a section near the rostral end of the superior colliculus from a transverse series of a Macaca mulatta brain stained by the Weil technique (X4). For a more comprehensive series see Crosby and Henderson, 1948. (Reproduced by permission of E. C. Crosby and J. W. Henderson : J. Comp. NeuroL, 88.53-92, 1948.) See Fig. 1 for explanation of abbreviations. area (dorsal division) reach the caudal portions of the tectum, and those from the lower calcarine area terminate in the more rostral tectum of the midbrain. Thus the dorsal division relates inferior visual field, superior calcarine area, and caudal tectum to the more caudal portion of the oculomotor complex. Conversely, the ventral division relates superior visual field, inferior calcarine area,
and rostral tectum to the more rostral portion of the oculomotor nucleus. The expected responses in reflex ocular deviation to stimuli lying in the visual field can therefore be related anatomically. The internal corticotectal tracts from Area 19 have been designated the preoccipital division, which likewise is divided into dorsal and ventral parts based on origin either from
236
JOHN WOODWORTH HENDERSON
upper or lower parastriate cortex (fig. 2). These fibers course forward to pulvinar levels along with the occipital division in the same layer just outside the visual radiations. The dorsal portion can be traced to the rostral tectum, while the ventral part reaches the more caudal tectum. Thus an interrelationship between upper Area 19 and rostral oculomotor nucleus can be seen, and, conversely, between lower Area 19 and caudal oculomotor nucleus. The pathways described were traced both in normal anatomic preparations and by experimental degeneration. It has previously been noted (Kronfeld, 1929) that they follow the visual radiations forward, but the fact that cortical localization can be related to the anatomic pattern of arrangement of the extraocular muscle nuclei has, to the best of our knowledge, not been heretofore noted. It is interesting that the termination of such fiber tracts fails to confirm the more recent work on the arrangement of the oculomotor nuclear complex. The parallel course of the tecto-oculomotor fibers which carry the impulses into the various portions of the oculomotor nucleus speaks against any reversal of pattern within the midbrain itself. The fact that the pattern described for Area 19 is inverted from that of Area 17 can be explained by the presence of short association bundles which can be seen to connect lower Area 17 with upper Area 19, and vice versa. Both the occipital and preoccipital divisions of the internal corticotectal system were seen to give off fibers which turned into the tegmentum of the midbrain without reaching the tectal areas (cort. teg. tr., fig. 2). These lay midway between the dorsal and ventral portions of both divisions in their course forward from the occipital lobe and presumably relate the areas for horizontal movement with the abducens complex by means of tegmental pathways. They could be traced with certainty only as far as the inferior collicular level.
Judged by the relatively great number of corticotectal and corticotegmental pathways, a large percentage of normal eye movements can be explained as visual automatisms— cortical, yet subconscious in a voluntary sense. This would include the movements subserving fixation, since it is well known that injury to Area 19 interferes with the holding of fixed gaze. McCulloch (1944) has shown that cortical conduction occurs from Area 8 of the frontal cortex to the parastriate area, but not in the opposite direction. This places the cortical centers for automatic eye movements under the control of the voluntary motor centers, with Area 8 able either to utilize the direct corticobulbar pathway to the brain stem, or to exert a modifying effect upon the cortical ocular automatisms by way of the parastriate area. It should be stressed that higher centers utilize previously laiddown mechanisms for the control of ocular movement. In each instance, the more primitive pattern can be recognized, but is made use of by more recent phylogenetic brain centers. It should be noted that there is a difference in level between the internal corticotectal fibers entering the tectum of the midbrain and the corticobulbar fibers which lie just above the cerebral peduncles. Since the fibers from the occipital lobe are more superficial in the colliculus, pressure downward from above should affect the reflex ocular movements much earlier than those which have a voluntary origin from Area 8 of the frontal lobe. Thus there should be a difference noted between command movements of the eyes and following movements in such an instance. University
Hospital.
The writer expresses his gratitude and indebtedness to Prof. Elizabeth Crosby for the use of the facilities of her department, both microscopic material and experimental animals. Were it not for her constant aid and collaboration this work could never have been completed.
ANATOMIC BASIS FOR EYE MOVEMENTS
237
REFERENCES
Bender, M. B., and Weinstein, W. A. : Functional representation in oculomotor and trochlear nuclei. Arch. Neurol. & Psychiat., 49 :98-106, 1943. Brouwer, B. : Anatomical, phylogenetical, and clinical studies on the central nervous system. Lecture I. The projection of the retina on the brain. The Herter Lectures, Johns Hopkins University School of Medicine. Baltimore, Williams & Wilkins, 1927. Brouwer, B., and Zeeman, W. P. C. : The projection of the retina in the primary optic neuron in monkeys. Brain, 49 :l-35,1926. Crosby, E. C, and Henderson, J. W. : The mammalian midbrain and isthmus region. Part II. Fiber connections of the superior colliculus. B. Pathways concerned in automatic eye movements. J. Comp. Neurol., 88:53-92, 1948. Foerster, O. : The cerebral cortex in man. Lancet, 221:309-312, 1931. Henderson, J. W. : Optokinetic and other factors modifying vestibular nystagmus. Arch. Ophth., 37:459-471,1947. Kronfeld, P. C. : The central visual pathway. Arch. Ophth., 2:709-732,1929. Lashley, K. S. : The mechanism of vision. VII. The projection of the retina upon the primary optic centers in the rat. J. Comp. Neurol., 59:341-373,1934. " McCulloch, W. S. : Cortico-cortical connections. Chapt. VIII in Precentral Motor Cortex (edited by P. C. Bucy). 111. Monographs in Medical Sciences, Urbana, 111., Illinois Press, 1944, v. 4, pp. 212-242. Szentagothai, J. : Die innere Gliederung des Oculomotoriuskernes. Arch. f. Psychiat., 115 :127-13S, 1942. Walker, A. E., and Weaver, T. A., Jr. : Ocular movements from the occipital lobe in the monkey. J. Neurophysiol., 3 :3S3-3S7,1940.
DISCUSSION
D R . D A V I D G. COGAN (Boston, Massachu-
setts) : I would like to ask two specific questions a n d I hope they weren't covered in the paper. I w a s so interested in some of the parts I may have lapsed in the others. Did you mention what the threshold was in Areas 17 a n d 19? I t seems to m e there has been some conflict between what W a l k e r and Weaver and what others have found in the relative thresholds in 17 versus 18 and 19. Also, it seems to be anomalous that there should be such a reversal of vertical representation in 19 and 17. Y o u say that that is executed by means of intracortical association pathways but it seems to me curious in the economy of the nervous system that such a reversal should take place. D R . P . J. LEINFELDER ( I o w a City, I o w a ) : I want to congratulate D r . H e n d e r s o n on a very difficult piece of work. I am sure he has labored much more extensively than you might realize from seeing the few slides that he has shown. T h e importance of his contribution, I think, should not be estimated in terms of its applicability to any one lesion of the
nervous system, but rather in his confirmation of t h e intimate reflex association between vision, binocular vision, and the ocular motor system. H e h a s demonstrated the pathways that carry t h e impulses for adequate coordination of ocular movements a n d fixation. D R . P I E R R E D A N I S (Brussels, Belgium) :
I think the localization of the muscles he referred to is still open to question because I think you base your general opinion on •the work of Brouwer but you have other workers w h o gave a reverse pattern. Bach and von Biervliet gave a reverse pattern, too. D R . HENDERSON (closing) : I would like to answer D r . Cogan's questions first while I have them in m y mind more specifically. T h e difference in threshold actually does exist. I t is not something to be measured in any specific terms. If w e had t h e current and stimulation high enough, we would get movement which we attributed to A r e a 17 by a spread from A r e a 19, which was of that type. Also the work of W a l k e r and W e a v e r was performed under a light anesthesia, as I recall, which again brings the question of anesthesia into it.
238
JOHN WOODWORTH HENDERSON
The problem of the difference between Areas 17 and 19 bothered me, too. The pathways I think are there all right. There is no question about the association pathways being there but why two different areas so closely related should have inverse correlation with the midbrain arrangement I do not know. However, the fact that the stimulus which comes back and influences automatic movements comes from Areas 8 to 18 and then into 19 would indicate that perhaps 19 is more related to the voluntary centers while 17 is related to the visual receptive pattern. We know that there are the two different sets of pathways that run forward into the midbrain; this may have some bearing on the reversal of pattern. As Dr. Danis has said, there has been an argument about the nuclear localization all
along. This includes the work of Brouwer, of Bernheimer, of Starr, and several others, all of whom to a greater or lesser extent destroyed individual muscles and looked for individual nuclear degeneration. That, to the anatomist, is incontrovertible. To the physiologist, perhaps, it is not. It has also raised the question in my mind, which may be just "woolgathering," as to whether the inverse difference between these physiologic and anatomic patterns is going to make us change our conception of what is going on. Is the primary thing that is happening the contraction or is the primary thing the inhibition? Perhaps that might have some bearing on the ocular movements. I know there isn't a good way of reconciling the two views but we are hoping that further work will help in bringing the two views closer together.