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The Accessory Optic System the Fugitive Visual Control System in Infantile Strabismus

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The Accessory Optic System the Fugitive Visual Control System in Infantile Strabismus SPECIAL ARTICLE The Accessory Optic System The Fugitive Visual Control System in Infantile Strabismus Michael C. Brodsky, MD nfantile strabismus inaugurates a constellation of dissociated eye movements that corre- spond to visuovestibular reflexes in lateral-eyed animals. These visual reflexes are gener- ated by subcortical visual pathways that use binocular visual input to modulate central ves- tibular tone. In this article, I present evidence that the accessory optic system is uniquely Isuited to provide an innervational substrate for visuovestibular eye movements in humans with infantile strabismus. Arch Ophthalmol. 2012;130(8):1055-1059 Infantile strabismus is characterized by dis- subcortical visual motion detection sys- sociated binocular vision, which is the nor- tem, could generate the dissociated and non- mal condition in lateral-eyed animals.1,2 dissociated torsional eye movements that ac- Early binocular misalignment gives rise to company human infantile strabismus. dissociated eye movements (changes in eye position evoked by unequal visual input WHAT IS THE AOS? to the 2 eyes).3 These include latent nys- tagmus, dissociated vertical divergence, The AOS consists of 3 nuclei at the me- and dissociated horizontal deviation,1-3 all sodiencephalic border that receive direct of which have a prominent torsional com- retinal input from the accessory optic tract ponent. Primary oblique muscle overac- (AOT)6-9 (Figure 1). The AOT com- tion, which accompanies infantile strabis- prises an inferior and a superior fascicu- mus but is not dissociated in nature, is also lus, with its superior fasciculus divided characterized by a torsional misalign- into a posterior branch, a middle branch, ment of the eyes.4 and an anterior branch that is identical to the original transpeduncular tract (trac- tus peduncularis transversus) discovered For editorial comment in 1870 by Gudden.10,11 The number of see page 1060 accessory optic fibers is small.7 In almost all mammalian species, most optic fibers reach the accessory optic nuclei via the These binocular deviations all corre- transpeduncular tract, which is visible as spond to normal visuovestibular reflexes it courses over the brachium of the supe- that are operative in lateral-eyed ani- rior colliculus.12 1-4 mals. Evolutionarily, these visual re- In most mammalian species, the AOS flexes antedate development of the visual is composed of 3 paired terminal nuclei, cortex, which does not generate torsional namely, the dorsoterminal nucleus (DTN), 5 eye movements in humans. Therefore, any the lateroterminal nucleus (LTN), and the attempt to anatomize infantile strabismus medioterminal nucleus (MTN), which re- must explain the reemergence of these ata- ceive innervation from primary optic fi- vistic reflexes, as well as their prominent tor- bers.7-9 Input to these 3 accessory optic ter- sional components. I propose that the ac- minal nuclei is predominantly from the cessory optic system (AOS), an atavistic contralateral eye.7-9,11,12 Along with the nucleus of the optic tract (NOT), these 3 Author Affiliation: Departments of Ophthalmology and Neurology, Mayo Clinic terminal nuclei project differentially to the and Mayo Foundation, Rochester, Minnesota. dorsal cap of the inferior olive,13-16 which ARCH OPHTHALMOL / VOL 130 (NO. 8), AUG 2012 WWW.ARCHOPHTHALMOL.COM 1055 ©2012 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 Corrected on August 21, 2012 rective eye movements to stabilize 7-9 Rostral the retinal image. As an analyzer NOT of self-motion, the AOS subserves vi- sual proprioception in the afoveate CP animal.7-9 DTN The AOS is a visual system that ML RN is organized in vestibular coordi- D EW 7-9 VTRZ LTN nates. According to results of ex- INC MTN 3n MTN perimental studies by Simpson and PAGm 4n colleagues, visual and vestibular sig- inSFp nals that produce compensatory eye movements are organized about a DMNm common set of axes derived from the orientation of the semicircular ca- MLF nals (Figure 2).7,9,12,16,17 Because the rpo AOS is directionally sensitive to low- velocity movements while the ves- PVG rpc tibular system typically responds to pdl pm movements of higher velocity, the pv AOS and vestibular labyrinths form vs 2 complementary systems to detect 6n vl self-motion and promote image sta- vm bilization so that objects in the vi- vsp sual world can be quickly and ac- curately analyzed.7,8,12,13 The AOS exists in all vertebrate DC,VLO classes,6,7,18,19 including humans,20 β but it has been studied most exten- Contralateral Ipsilateral sively in the rabbit. The 3 preferred IOp MAO directions for cells in the accessory optic terminal nuclei define 3 direc- Caudal tions in visual space, namely, hori- zontally from posterior to anterior Figure 1. Neuroanatomical connections of the accessory optic system. The brainstem is depicted from for the DTN, vertically up and down the front (with the left-hand side of the animal on the right-hand side of the drawing). Accessory terminal for the MTN, and vertically down for nuclei include the dorsoterminal nucleus (DTN), which lies adjacent to the nucleus of the optic tract the LTN.7-9,11-14,21 Its 3 pretectal ac- (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), cessory optic nuclei are closely re- which send ipsilateral projections to the left dorsal cap (DC) of the inferior olive and then back to the right lated to the NOT and receive input flocculus (not shown), resulting in a double decussation of motion pathways from each eye. Adapted with predominantly from the contralat- 12 permission from Simpson et al. CP indicates posterior commissure; D, nucleus of Darkschewitsch; 7-9,12,13 DMNm, deep mesencephalic nucleus, pars medialis; EW, nucleus of Edinger-Westphal; INC, interstitial eral eye. Direction-sensitive nucleus of Cajal; inSFp, intersitial nucleus of the superior fasciculus, posterior fibers; MAO, medial ON–type retinal ganglion cells en- accessory nucleus, inferior olivary complex; ML, medial lemniscus; MLF, medial longitudinal fasciculus; code retinal image slip22,23 and trans- PAGm, periaqueductal gray, medial part; pdl, dorsolateral division, basal pontine complex; pm, medial mit this information to the AOS, in- division, basal pontine complex; pv, ventral division, basal pontine complex; PVG, periventricular gray; 24 RN, red nucleus; rpc, pontine reticular nucleus, pars caudalis; rpo, pontine reticular nucleus, pars oralis; ferior olive floccular climbing vl, lateral vestibular nucleus; VLO, ventrolateral outgrowth, inferior olivary complex; vm, medial vestibular fibers,25 and floccular Purkinje nucleus; vs, superior vestibular nucleus; vsp, spinal vestibular nucleus; VTRZ, visual tegmental relay cells.26 These 3 pairs of channels re- zone; ␤, nucleus ␤ of the inferior olive; 3n, oculomotor nerve; 4n, trochlear nerve; and 6n, abducens nerve. main anatomically distinguishable within the AOS, inferior olive, and floccular zones, which (when stimu- provides the only source of climb- type direction-sensitive ganglion lated) elicit eye movements orga- ing fibers to the flocculonodular lobe cells. The AOS neurons have large nized in a canal-like coordinate sys- of the cerebellum.7-9,13-17 In this way, receptive fields (averaging about tem.18,27-29 Each pair conveys signals cells of the AOS converge with those 40° vertically and 60° horizon- about flow of the visual surround of the vestibular system in the ves- tally), are direction selective, and about 1 of 3 rotation axes, which are tibulocerebellum.7-9 have a preference for slow-moving approximately collinear with the Despite its name, the AOS is a pri- stimuli.7-9,12,13 The AOS processes in- best-response axes of the semicir- mary visual system receiving direct formation about the speed and di- cular canals and the rotation axes of visual information from the retina rection of movement of large tex- the extraocular muscles.28 via 1 or more AOTs13 that are re- tured parts of the visual world.7-9 The The rabbit flocculus ipsilateral to sponsible for visuovestibular inter- AOS signals self-motion as a func- the seeing eye is optimally sensi- action in afoveate animals.7,16,17 Its tion of slip of the visual world over tive to optokinetic stimulation about retinal input is derived from ON– the retinal surface and generates cor- a 135° axis, while the flocculus con- ARCH OPHTHALMOL / VOL 130 (NO. 8), AUG 2012 WWW.ARCHOPHTHALMOL.COM 1056 ©2012 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 Corrected on August 21, 2012 tralateral to the seeing eye is opti- mally sensitive to optokinetic stimu- Rotation Axes Visual Climbing Fibers lation around a horizontal 45° axis (Left Flocculus of Dominant Eye) (Figure 3).26-29 For horizontal VA stimulation, the DTN and its adja- cent NOT are selectively sensitive to Paired vertical recti nasally directed optokinetic stimu- 148° lation presented to the contralat- 7,8,12,13 Paired eral eye. Conversely, electri- obliques cal microstimulation in the alert 43° ∗ ∗ rabbit’s flocculus produces abduc- ∗ 143° tion of the ipsilateral eye27,29,30 or dis- sociated torsional and vertical rota- 47° 90° tions of the 2 eyes, corresponding to 0° Paired 45° Paired the plane of 1 semicircular ca- vertical canals vertical canals nal.26-30 Because floccular motion de- 41° 139° tection for each eye is not fully rep- resented on its own side of the body, monocular optokinetic responses must be derived from the synthesis of bilateral floccular representa- 28 tions. Therefore, the flocculus pro- Figure 2. Spatial orientation of preferred axes of 3-dimensional rotation for dorsal cap neurons in the vides a subcortical binocular visual right inferior olive recorded during optokinetic stimulation in a spherical enclosure.
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