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Figure 1. Neuroanatomical connections of the accessory optic system. The brainstem is depicted from the front (with the left-hand side of the animal on the right-hand side of the drawing). Accessory terminal nuclei include the dorsoterminal nucleus (DTN), which lies adjacent to the nucleus of the optic tract (NOT); medial terminal nucleus (MTN); lateral terminal nucleus (LTN); and principal part of the inferior olive (IOp). Optokinetic input from the right retina crosses to the left accessory optic nuclei (depicted), which send ipsilateral projections to the left dorsal cap (DC) of the inferior olive and then back to the right flocculus (not shown), resulting in a double decussation of motion pathways from each eye. Adapted with permission from Simpson et al. CP indicates posterior commissure; D, nucleus of Darkschewitsch; DMNm, deep mesencephalic nucleus, pars medialis; EW, nucleus of Edinger-Westphal; INC, interstitial nucleus of Cajal; inSFp, intersitial nucleus of the superior fasciculus, posterior fibers; MAO, medial accessory nucleus, inferior olivary complex; ML, medial lemniscus; MLF, medial longitudinal fasciculus; PAGm, periaqueductal gray, medial part; pdl, dorsolateral division, basal pontine complex; pm, medial division, basal pontine complex; pv, ventral division, basal pontine complex; PVG, periventricular gray; RN, red nucleus; rpc, pontine reticular nucleus, pars caudalis; rpo, pontine reticular nucleus, pars oralis; vl, lateral vestibular nucleus; VLO, ventrolateral outgrowth, inferior olivary complex; vm, medial vestibular nucleus; vs, superior vestibular nucleus; vsp, spinal vestibular nucleus; VTRZ, visual tegmental relay zone; β, nucleus β of the inferior olive; 3n, oculomotor nerve; 4n, trochlear nerve; and 6n, abducens nerve.

Figure 1. Neuroanatomical connections of the accessory optic system. The brainstem is depicted from the front (with the left-hand side of the animal on the right-hand side of the drawing). Accessory terminal nuclei include the dorsoterminal nucleus (DTN), which lies adjacent to the nucleus of the optic tract (NOT); medial terminal nucleus (MTN); lateral terminal nucleus (LTN); and principal part of the inferior olive (IOp). Optokinetic input from the right retina crosses to the left accessory optic nuclei (depicted), which send ipsilateral projections to the left dorsal cap (DC) of the inferior olive and then back to the right flocculus (not shown), resulting in a double decussation of motion pathways from each eye. Adapted with permission from Simpson et al.12 CP indicates posterior commissure; D, nucleus of Darkschewitsch; DMNm, deep mesencephalic nucleus, pars medialis; EW, nucleus of Edinger-Westphal; INC, interstitial nucleus of Cajal; inSFp, intersitial nucleus of the superior fasciculus, posterior fibers; MAO, medial accessory nucleus, inferior olivary complex; ML, medial lemniscus; MLF, medial longitudinal fasciculus; PAGm, periaqueductal gray, medial part; pdl, dorsolateral division, basal pontine complex; pm, medial division, basal pontine complex; pv, ventral division, basal pontine complex; PVG, periventricular gray; RN, red nucleus; rpc, pontine reticular nucleus, pars caudalis; rpo, pontine reticular nucleus, pars oralis; vl, lateral vestibular nucleus; VLO, ventrolateral outgrowth, inferior olivary complex; vm, medial vestibular nucleus; vs, superior vestibular nucleus; vsp, spinal vestibular nucleus; VTRZ, visual tegmental relay zone; β, nucleus β of the inferior olive; 3n, oculomotor nerve; 4n, trochlear nerve; and 6n, abducens nerve.

Figure 2. Spatial orientation of preferred axes of 3-dimensional rotation for dorsal cap neurons in the right inferior olive recorded during optokinetic stimulation in a spherical enclosure. Adapted with permission from Van der Steen et al. VA indicates vertical axis.

Figure 2. Spatial orientation of preferred axes of 3-dimensional rotation for dorsal cap neurons in the right inferior olive recorded during optokinetic stimulation in a spherical enclosure. Adapted with permission from Van der Steen et al.27 VA indicates vertical axis.

Figure 3. Sensitivity to monocular optokinetic stimulation in a spherical enclosure. A, Responses of posterior axis climbing fiber Purkinje cells to stimulation presented to the ipsilateral left eye. B, Responses of anterior axis climbing fiber Purkinje cells to stimulation presented to the contralateral eye. CCW indicates counterclockwise optokinetic rotation; CW, clockwise optokinetic rotation. Adapted with permission from Van der Steen et al.

Figure 3. Sensitivity to monocular optokinetic stimulation in a spherical enclosure. A, Responses of posterior axis climbing fiber Purkinje cells to stimulation presented to the ipsilateral left eye. B, Responses of anterior axis climbing fiber Purkinje cells to stimulation presented to the contralateral eye. CCW indicates counterclockwise optokinetic rotation; CW, clockwise optokinetic rotation. Adapted with permission from Van der Steen et al.27

1.
Brodsky MC. Dissociated vertical divergence: a righting reflex gone wrong.  Arch Ophthalmol. 1999;117(9):1216-1222PubMedArticle
2.
Brodsky MC. Visuo-vestibular eye movements: infantile strabismus in 3 dimensions.  Arch Ophthalmol. 2005;123(6):837-842PubMedArticle
3.
Brodsky MC. Dissociated horizontal deviation: clinical spectrum, pathogenesis, evolutionary underpinnings, diagnosis, treatment, and potential role in the development of infantile esotropia (an American Ophthalmological Society thesis).  Trans Am Ophthalmol Soc. 2007;105:272-293
4.
Brodsky MC, Donahue SP. Primary oblique muscle overaction: the brain throws a wild pitch.  Arch Ophthalmol. 2001;119(9):1307-1314PubMedArticle
5.
Brodsky MC. Dissociated vertical divergence: cortical or subcortical in origin?  Strabismus. 2011;19(2):67-70PubMedArticle
6.
Marg E. The accessory optic system.  Ann N Y Acad Sci. 1964;117:35-52PubMedArticle
7.
Simpson JI, Soodak RE, Hess R. The accessory optic system and its relation to the vestibulocerebellum.  Prog Brain Res. 1979;50:715-724PubMed
8.
Simpson JI, Leonard CS, Soodak RE. The accessory optic system: analyzer of self-motion.  Ann N Y Acad Sci. 1988;545:170-179PubMedArticle
9.
Simpson JI. The accessory optic system.  Annu Rev Neurosci. 1984;7:13-41PubMedArticle
10.
Gudden B. Ueber einen bisher nicht eschriebenen Nervenfasernstrang im Gehirne der Säugethiere und des Menschen.  Arch Psychiat. 1870;2:364-366Article
11.
Gudden B. Ueber den Tractus peduncularis transversus.  Arch Psychiat. 1881;11:415-423Article
12.
Simpson JI, Giolli RA, Blanks RH. The pretectal nuclear complex and the accessory optic system.  Rev Oculomot Res. 1988;2:335-364PubMed
13.
Giolli RA, Blanks RHI, Lui F. The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function.  Prog Brain Res. 2006;151:407-440PubMed
14.
Takeda T, Maekawa K. The origin of the pretecto-olivary tract: a study using the horseradish peroxidase method.  Brain Res. 1976;117(2):319-325PubMedArticle
15.
Maekawa K, Takeda T. Afferent pathways from the visual system to the cerebellar flocculus of the rabbit. In: Baker R, Berthoz A, eds. Control of Gaze by Brain Stem Neurons: Developments in Neuroscience. Amsterdam, the Netherlands: Elsevier/North-Holland Biomed; 1977:187-195
16.
Maekawa K, Simpson JI. Climbing fiber activation of Purkinje cells in the flocculus by impulses transferred through the visual pathway.  Brain Res. 1972;39(1):245-251PubMedArticle
17.
Maekawa K, Simpson JI. Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system.  J Neurophysiol. 1973;36(4):649-666PubMed
18.
Ebbesson SO. On the organization of central visual pathways in vertebrates.  Brain Behav Evol. 1970;3(1):178-194PubMedArticle
19.
Cooper HM, Magnin M. A common mammalian plan of accessory optic system organization revealed in all primates.  Nature. 1986;324(6096):457-459PubMedArticle
20.
Fredericks CA, Giolli RA, Blanks RH, Sadun AA. The human accessory optic system.  Brain Res. 1988;454(1-2):116-122PubMedArticle
21.
Simpson JI, Leonard CS, Soodak RE. The accessory optic system of rabbit. II. Spatial organization of direction selectivity.  J Neurophysiol. 1988;60(6):2055-2072PubMed
22.
Oyster CW. The analysis of image motion by the rabbit retina.  J Physiol. 1968;199(3):613-635PubMed
23.
Soodak RE, Simpson JI. The accessory optic system of rabbit. I. Basic visual response properties.  J Neurophysiol. 1988;60(6):2037-2054PubMed
24.
Leonard CS, Simpson JI, Graf W. Spatial organization of visual messages of the rabbit's cerebellar flocculus. I. Typology of inferior olive neurons of the dorsal cap of Kooy.  J Neurophysiol. 1988;60(6):2073-2090PubMed
25.
Simpson JI, Graf W, Leonard CS. Three-dimensional representation of retinal image movement by climbing fiber activity. In: Strata P, ed. The Olivocerebellar System in Motor Control. Berlin, Germany: Springer Verlag; 1989:323-337. Experimental Brain Research Series 17
26.
Graf W, Simpson JI, Leonard CS. Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells.  J Neurophysiol. 1988;60(6):2091-2121PubMed
27.
Van der Steen J, Simpson JI, Tan J. Representation of three-dimensional eye movements in the cerebellar flocculus of the rabbit. In: Schmid R, Zambarbieri D, eds. Oculomotor Control and Cognitive Processes. Amsterdam, the Netherlands: Elsevier; 1991:63-77
28.
Tan HS, van der Steen J, Simpson JI, Collewijn H. Three-dimensional organization of optokinetic responses in the rabbit.  J Neurophysiol. 1993;69(2):303-317PubMed
29.
Simpson JI, Van der Steen J, Tan J, Graf W, Leonard CS. Representations of ocular rotations in the cerebellar flocculus of the rabbit.  Prog Brain Res. 1989;80:213-223
30.
Ito M, Nisimaru N, Yamamoto M. Specific patterns of neuronal connexions involved in the control of the rabbit's vestibulo-ocular reflexes by the cerebellar flocculus.  J Physiol. 1977;265(3):833-854PubMed
31.
Grasse KL, Cynader MS. Response properties of single units in the accessory optic system of the dark-reared cat.  Brain Res. 1986;392(1-2):199-210PubMed
32.
Grasse KL, Cynader MS. The accessory optic system of the monocularly deprived cat.  Brain Res. 1987;428(2):229-241PubMed
33.
Grasse KL, Cynader MS, Douglas RM. Alterations in response properties in the lateral and dorsal terminal nuclei of the cat accessory optic system following visual cortex lesions.  Exp Brain Res. 1984;55(1):69-80PubMedArticle
34.
Hoffmann KP. Cortical vs subcortical contributions to the optokinetic reflex in the cat. In: Lennerstrand G, Zee DS, Keller EL, eds. Functional Basis of Ocular Motility Disorders. Oxford, England: Pergamon; 1982:303-310
35.
Brodsky MC, Tusa RJ. Latent nystagmus: vestibular nystagmus with a twist.  Arch Ophthalmol. 2004;122(2):202-209PubMedArticle
36.
Simpson JI, Graf W. The selection of reference frames by nature and its investigators.  Rev Oculomot Res. 1985;1:3-16PubMed
37.
Hamasaki D, Marg E. Microelectrode study of accessory optic tract in the rabbit.  Am J Physiol. 1962;202:480-486PubMed
38.
Schiller PH. Parallel information processing channels created in the retina.  Proc Natl Acad Sci U S A. 2010;107(40):17087-17094PubMedArticle
39.
Yanagihara D, Watanabe S, Takagi S, Mitarai G. Neuroanatomical substrate for the dorsal light response. II. Effects of kainic acid-induced lesions of the valvula cerebelli on the goldfish dorsal light response.  Neurosci Res. 1993;16(1):33-37PubMedArticle
40.
Chavesse FB, Worth CA, Lyle TK. The Binocular Reflexes and Treatment of Strabismus. Philadelphia, PA: Blakeston; 1950
Special Article
Aug 2012

The Accessory Optic SystemThe Fugitive Visual Control System in Infantile Strabismus

Author Affiliations

Author Affiliation: Departments of Ophthalmology and Neurology, Mayo Clinic and Mayo Foundation, Rochester, Minnesota.

Arch Ophthalmol. 2012;130(8):1055-1058. doi:10.1001/archophthalmol.2011.2888
Abstract

Infantile strabismus inaugurates a constellation of dissociated eye movements that correspond to visuovestibular reflexes in lateral-eyed animals. These visual reflexes are generated by subcortical visual pathways that use binocular visual input to modulate central vestibular tone. In this article, I present evidence that the accessory optic system is uniquely suited to provide an innervational substrate for visuovestibular eye movements in humans with infantile strabismus.

Infantile strabismus is characterized by dissociated binocular vision, which is the normal condition in lateral-eyed animals.1,2 Early binocular misalignment gives rise to dissociated eye movements (changes in eye position evoked by unequal visual input to the 2 eyes).3 These include latent nystagmus, dissociated vertical divergence, and dissociated horizontal deviation,13 all of which have a prominent torsional component. Primary oblique muscle overaction, which accompanies infantile strabismus but is not dissociated in nature, is also characterized by a torsional misalignment of the eyes.4

These binocular deviations all correspond to normal visuovestibular reflexes that are operative in lateral-eyed animals.14 Evolutionarily, these visual reflexes antedate development of the visual cortex, which does not generate torsional eye movements in humans.5 Therefore, any attempt to anatomize infantile strabismus must explain the reemergence of these atavistic reflexes, as well as their prominent torsional components. I propose that the accessory optic system (AOS), an atavistic subcortical visual motion detection system, could generate the dissociated and nondissociated torsional eye movements that accompany human infantile strabismus.

WHAT IS THE AOS?

The AOS consists of 3 nuclei at the mesodiencephalic border that receive direct retinal input from the accessory optic tract (AOT)69 (Figure 1). The AOT comprises an inferior and a superior fasciculus, with its superior fasciculus divided into a posterior branch, a middle branch, and an anterior branch that is identical to the original transpeduncular tract (tractus peduncularis transversus) discovered in 1870 by Gudden.10,11 The number of accessory optic fibers is small.7 In almost all mammalian species, most optic fibers reach the accessory optic nuclei via the transpeduncular tract, which is visible as it courses over the brachium of the superior colliculus.12

In most mammalian species, the AOS is composed of 3 paired terminal nuclei, namely, the dorsoterminal nucleus (DTN), the lateroterminal nucleus (LTN), and the medioterminal nucleus (MTN), which receive innervation from primary optic fibers.79 Input to these 3 accessory optic terminal nuclei is predominantly from the contralateral eye.79,11,12 Along with the nucleus of the optic tract (NOT), these 3 terminal nuclei project differentially to the dorsal cap of the inferior olive,1316 which provides the only source of climbing fibers to the flocculonodular lobe of the cerebellum.79,1317 In this way, cells of the AOS converge with those of the vestibular system in the vestibulocerebellum.79

Despite its name, the AOS is a primary visual system receiving direct visual information from the retina via 1 or more AOTs13 that are responsible for visuovestibular interaction in afoveate animals.7,16,17 Its retinal input is derived from ON–type direction-sensitive ganglion cells. The AOS neurons have large receptive fields (averaging about 40° vertically and 60° horizontally), are direction selective, and have a preference for slow-moving stimuli.79,12,13 The AOS processes information about the speed and direction of movement of large textured parts of the visual world.79 The AOS signals self-motion as a function of slip of the visual world over the retinal surface and generates corrective eye movements to stabilize the retinal image.79 As an analyzer of self-motion, the AOS subserves visual proprioception in the afoveate animal.79

The AOS is a visual system that is organized in vestibular coordinates.79 According to results of experimental studies by Simpson and colleagues, visual and vestibular signals that produce compensatory eye movements are organized about a common set of axes derived from the orientation of the semicircular canals (Figure 2).7,9,12,16,17 Because the AOS is directionally sensitive to low-velocity movements while the vestibular system typically responds to movements of higher velocity, the AOS and vestibular labyrinths form 2 complementary systems to detect self-motion and promote image stabilization so that objects in the visual world can be quickly and accurately analyzed.7,8,12,13

The AOS exists in all vertebrate classes,6,7,18,19 including humans,20 but it has been studied most extensively in the rabbit. The 3 preferred directions for cells in the accessory optic terminal nuclei define 3 directions in visual space, namely, horizontally from posterior to anterior for the DTN, vertically up and down for the MTN, and vertically down for the LTN.79,1114,21 Its 3 pretectal accessory optic nuclei are closely related to the NOT and receive input predominantly from the contralateral eye.79,12,13 Direction-sensitive ON–type retinal ganglion cells encode retinal image slip22,23 and transmit this information to the AOS, inferior olive24 floccular climbing fibers,25 and floccular Purkinje cells.26 These 3 pairs of channels remain anatomically distinguishable within the AOS, inferior olive, and floccular zones, which (when stimulated) elicit eye movements organized in a canal-like coordinate system.18,2729 Each pair conveys signals about flow of the visual surround about 1 of 3 rotation axes, which are approximately collinear with the best -response axes of the semicircular canals and the rotation axes of the extraocular muscles.28

The rabbit flocculus ipsilateral to the seeing eye is optimally sensitive to optokinetic stimulation about a 135° axis, while the flocculus contralateral to the seeing eye is optimally sensitive to optokinetic stimulation around a horizontal 45° axis (Figure 3).2629 For horizontal stimulation, the DTN and its adjacent NOT are selectively sensitive to nasally directed optokinetic stimulation presented to the contralateral eye.7,8,12,13 Conversely, electrical microstimulation in the alert rabbit's flocculus produces abduction of the ipsilateral eye27,29,30 or dissociated torsional and vertical rotations of the 2 eyes, corresponding to the plane of 1 semicircular canal.2630 Because floccular motion detection for each eye is not fully represented on its own side of the body, monocular optokinetic responses must be derived from the synthesis of bilateral floccular representations.28 Therefore, the flocculus provides a subcortical binocular visual system that generates asymmetrical torsional eye movements under dissociated conditions of optokinetic stimulation.28

Studies using decortication have revealed contributions from the visual cortex to the AOS. Disruption of contributions from the visual cortex to the AOS by strabismus may alter the inherent biases of the accessory optic nuclei.3133 The ipsilateral visual cortex is necessary for several response properties that distinguish DTN and LTN neurons in the cat from those in the rabbit. Following decortication, cat DTN and LTN neurons lose their binocularity and become almost totally dominated by the contralateral eye.33 For example, LTN neurons excited by upward movement, which in the cat are equal in number to those excited by downward movement, become less numerous so that the cat LTN becomes like that of the rabbit, consisting of neurons excited by slow downward movements to the contralateral eye.33 Unlike the LTN and DTN, neurons in the cat MTN are largely monocular and similar to those in the rabbit.12 The monocular nasotemporal optokinetic asymmetry that characterizes infantile strabismus is known to result from monocular cortical input to the NOT and DTN,34 unmasking a subcortical visuovestibular bias that generates latent nystagmus.35 The AOS provides a neuroanatomical substrate whereby vertical monocular subcortical motion biases could generate the canal-based torsional eye movements that characterize primary oblique muscle overaction and dissociated vertical divergence.2,4 Although we observe and analyze these eye movements in yaw, pitch, and roll,2 they are encoded in a canal-oriented push-pull bilateral coordinate system that detects optokinetic flow in every direction.36

Photic stimulation can activate the AOT in the rabbit.4,37 The AOS neurons show the same responses to retinal illumination as ON–type direction-sensitive retinal ganglion cells, being excited only at the onset of retinal stimulation,23 and generate a firing response that is related to light intensity.32 In this way, the AOS may implement the visuovestibular reflexes that characterize infantile strabismus.1,2 However, because the AOS is primarily a motion detector, central modulation of the primitive luminance reflexes that characterize infantile strabismus may require input from additional subcortical visual pathways. It is possible that other primitive luminance pathways may provide parallel subcortical luminance input to the visuovestibular system.38 Like the AOS, luminance input that modulates the dorsal light reflex in fish (which corresponds to dissociated vertical divergence and primary oblique muscle overaction in humans with infantile strabismus)1,2 is transmitted to the central pretectal nucleus in the contralateral midbrain and then down to the vestibulocerebellum, which integrates visual and vestibular input.39 These luminance and motion pathways may constitute the subcortical equivalents of the “what” and “where” visual streams within the association visual cortex. How these subcortical visual streams intercommunicate to consolidate spatial and temporal summation of visual information at the subcortical levels remains a mystery. But the likelihood that they provide the innervational substrate for the atavistic eye movements that characterize infantile strabismus should not be ignored.

CONCLUSIONS

The AOS provides a critical piece of the puzzle for infantile strabismus by serving as a neuroanatomic substrate for visuovestibular eye movements. The AOS is atavistic, present in humans, subcortical, crossed, and sensitive to optokinetic motion. It operates in a canal-based coordinate system and generates dissociated torsional eye movements. For these reasons, the AOS is uniquely suited to generate the dissociated eye movements that characterize infantile strabismus. The fact that its retinal fibers terminate in the 3 nuclei of the AOT along with the adjacent NOT (a part of the pretectal nuclear complex that generates latent nystagmus) lends further credence to this hypothesis. Dissociated binocular vision in infancy may unlock this atavistic visual system, generating canal-based ocular rotations that we anthropomorphize to diagnose “torsion” in the frontal plane.

This analysis implies that mutations involving the AOS or its target zones within the cerebellar flocculus could provide a potential template for infantile strabismus. If so, then the age-old dichotomy postulated by Worth (congenital defect in cortical fusion) and Chavesse (early binocular misalignment)40 could be explained by binocular subcortical dysfunction intrinsic to the visuovestibular system.

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Article Information

Correspondence: Michael C. Brodsky, MD, Department of Ophthalmology, Mayo Clinic and Mayo Foundation, 200 First St SW, Rochester, MN 55905 (Brodsky.michael@mayo.edu).

Submitted for Publication: October 27, 2011; final revision received October 27, 2011; accepted November 18, 2011.

Financial Disclosure: None reported.

Funding/Support: This study was supported in part by an unrestricted grant from Research to Prevent Blindness to the Department of Ophthalmology, Mayo Clinic.

Additional Contributions: John Simpson, PhD, and Alfredo Sadun, MD, PhD, provided invaluable advice and guidance in developing the translational proposal of a role for the accessory optic system in infantile strabismus.

This article was corrected for errors on August 21, 2012.

REFERENCES
1.
Brodsky MC. Dissociated vertical divergence: a righting reflex gone wrong.  Arch Ophthalmol. 1999;117(9):1216-1222PubMedArticle
2.
Brodsky MC. Visuo-vestibular eye movements: infantile strabismus in 3 dimensions.  Arch Ophthalmol. 2005;123(6):837-842PubMedArticle
3.
Brodsky MC. Dissociated horizontal deviation: clinical spectrum, pathogenesis, evolutionary underpinnings, diagnosis, treatment, and potential role in the development of infantile esotropia (an American Ophthalmological Society thesis).  Trans Am Ophthalmol Soc. 2007;105:272-293
4.
Brodsky MC, Donahue SP. Primary oblique muscle overaction: the brain throws a wild pitch.  Arch Ophthalmol. 2001;119(9):1307-1314PubMedArticle
5.
Brodsky MC. Dissociated vertical divergence: cortical or subcortical in origin?  Strabismus. 2011;19(2):67-70PubMedArticle
6.
Marg E. The accessory optic system.  Ann N Y Acad Sci. 1964;117:35-52PubMedArticle
7.
Simpson JI, Soodak RE, Hess R. The accessory optic system and its relation to the vestibulocerebellum.  Prog Brain Res. 1979;50:715-724PubMed
8.
Simpson JI, Leonard CS, Soodak RE. The accessory optic system: analyzer of self-motion.  Ann N Y Acad Sci. 1988;545:170-179PubMedArticle
9.
Simpson JI. The accessory optic system.  Annu Rev Neurosci. 1984;7:13-41PubMedArticle
10.
Gudden B. Ueber einen bisher nicht eschriebenen Nervenfasernstrang im Gehirne der Säugethiere und des Menschen.  Arch Psychiat. 1870;2:364-366Article
11.
Gudden B. Ueber den Tractus peduncularis transversus.  Arch Psychiat. 1881;11:415-423Article
12.
Simpson JI, Giolli RA, Blanks RH. The pretectal nuclear complex and the accessory optic system.  Rev Oculomot Res. 1988;2:335-364PubMed
13.
Giolli RA, Blanks RHI, Lui F. The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function.  Prog Brain Res. 2006;151:407-440PubMed
14.
Takeda T, Maekawa K. The origin of the pretecto-olivary tract: a study using the horseradish peroxidase method.  Brain Res. 1976;117(2):319-325PubMedArticle
15.
Maekawa K, Takeda T. Afferent pathways from the visual system to the cerebellar flocculus of the rabbit. In: Baker R, Berthoz A, eds. Control of Gaze by Brain Stem Neurons: Developments in Neuroscience. Amsterdam, the Netherlands: Elsevier/North-Holland Biomed; 1977:187-195
16.
Maekawa K, Simpson JI. Climbing fiber activation of Purkinje cells in the flocculus by impulses transferred through the visual pathway.  Brain Res. 1972;39(1):245-251PubMedArticle
17.
Maekawa K, Simpson JI. Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system.  J Neurophysiol. 1973;36(4):649-666PubMed
18.
Ebbesson SO. On the organization of central visual pathways in vertebrates.  Brain Behav Evol. 1970;3(1):178-194PubMedArticle
19.
Cooper HM, Magnin M. A common mammalian plan of accessory optic system organization revealed in all primates.  Nature. 1986;324(6096):457-459PubMedArticle
20.
Fredericks CA, Giolli RA, Blanks RH, Sadun AA. The human accessory optic system.  Brain Res. 1988;454(1-2):116-122PubMedArticle
21.
Simpson JI, Leonard CS, Soodak RE. The accessory optic system of rabbit. II. Spatial organization of direction selectivity.  J Neurophysiol. 1988;60(6):2055-2072PubMed
22.
Oyster CW. The analysis of image motion by the rabbit retina.  J Physiol. 1968;199(3):613-635PubMed
23.
Soodak RE, Simpson JI. The accessory optic system of rabbit. I. Basic visual response properties.  J Neurophysiol. 1988;60(6):2037-2054PubMed
24.
Leonard CS, Simpson JI, Graf W. Spatial organization of visual messages of the rabbit's cerebellar flocculus. I. Typology of inferior olive neurons of the dorsal cap of Kooy.  J Neurophysiol. 1988;60(6):2073-2090PubMed
25.
Simpson JI, Graf W, Leonard CS. Three-dimensional representation of retinal image movement by climbing fiber activity. In: Strata P, ed. The Olivocerebellar System in Motor Control. Berlin, Germany: Springer Verlag; 1989:323-337. Experimental Brain Research Series 17
26.
Graf W, Simpson JI, Leonard CS. Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells.  J Neurophysiol. 1988;60(6):2091-2121PubMed
27.
Van der Steen J, Simpson JI, Tan J. Representation of three-dimensional eye movements in the cerebellar flocculus of the rabbit. In: Schmid R, Zambarbieri D, eds. Oculomotor Control and Cognitive Processes. Amsterdam, the Netherlands: Elsevier; 1991:63-77
28.
Tan HS, van der Steen J, Simpson JI, Collewijn H. Three-dimensional organization of optokinetic responses in the rabbit.  J Neurophysiol. 1993;69(2):303-317PubMed
29.
Simpson JI, Van der Steen J, Tan J, Graf W, Leonard CS. Representations of ocular rotations in the cerebellar flocculus of the rabbit.  Prog Brain Res. 1989;80:213-223
30.
Ito M, Nisimaru N, Yamamoto M. Specific patterns of neuronal connexions involved in the control of the rabbit's vestibulo-ocular reflexes by the cerebellar flocculus.  J Physiol. 1977;265(3):833-854PubMed
31.
Grasse KL, Cynader MS. Response properties of single units in the accessory optic system of the dark-reared cat.  Brain Res. 1986;392(1-2):199-210PubMed
32.
Grasse KL, Cynader MS. The accessory optic system of the monocularly deprived cat.  Brain Res. 1987;428(2):229-241PubMed
33.
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