Three-Dimensional Kinematics at the Level of the Oculomotor Plant

Klier, Eliana M.; Hui, Meng; Angelaki, Dora E.

doi:10.1523/jneurosci.3610-05.2006

Cited by 55 publications

(69 citation statements)

References 46 publications

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“…3D eye movements (833.33 Hz) were calibrated daily while fixating vertically and horizontally eccentric targets (Klier et al, 2005). Electrode penetrations were made into the nucleus prepositus hypoglossi, the medial and superior vestibular nuclei [same neurons as in the studies by Green et al (2007), Meng et al (2005), and Meng and Angelaki (2006)], and the interstitial nucleus of Cajal, as well as cells scattered between the abducens and oculomotor nuclei [locations identified in the studies by Ghasia and Angelaki (2005) and Klier et al (2006)]. …”

Section: Methodsmentioning

confidence: 99%

“…In contrast, motoneurons show no evidence for coding this eye position dependence of eye velocity (Ghasia and Angelaki, 2005). Instead, the half-angle rule appears to be implemented by the mechanical properties of the eyeball: likely, orbital pulleys make the pulling directions of extraocular muscles eye position dependent (Miller, 1989;Demer et al, 2000;Kono et al, 2002;Klier et al, 2006).…”

Section: The Half-angle Rule and 3d Ocular Kinematicsmentioning

confidence: 99%

“…In particular, visually guided eye movements initiated from eccentric positions have rotation axes that do not remain confined to Listing's plane (zero torsion) but tilt torsionally in the same direction as gaze by approximately half as much (known as the half-angle rule) (Tweed and Vilis, 1990;Crawford and Vilis, 1991). This property appears to be generated by the mechanical characteristics of the eyeball, likely an eye position dependence of the extraocular muscle pulling directions brought about by orbital "pulleys" (Miller, 1989;Demer et al, 2000;Kono et al, 2002;Klier et al, 2006). Therefore, unlike the evoked eye movement, motoneurons do not encode the half-angle rule (Ghasia and Angelaki, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics

Ghasia¹,

Hui²,

Angelaki³

2008

J. Neurosci.

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Inverse and forward dynamic models have been conceptually important in computational motor control. In particular, inverse models are thought to convert desired action into appropriate motor commands. In parallel, forward models predict the consequences of the motor command on behavior by constructing an efference copy of the actual movement. Despite theoretical appeal, their neural representation has remained elusive. Here, we provide evidence supporting the notion that a group of premotor neurons called burst-tonic (BT) cells represent the output of the inverse model for eye movements. We show that BT neurons, like extraocular motoneurons but different from the evoked eye movement, do not carry signals appropriate for the half-angle rule of ocular kinematics during smoothpursuit eye movements from eccentric positions. Along with findings of identical response dynamics as motoneurons, these results strongly suggest that BT cells carry a replica of the motor command. In contrast, eye-head (EH) neurons, a premotor cell type that is the target of Purkinje cell inhibition from the cerebellar flocculus/ventral paraflocculus, exhibit properties that could be consistent with the half-angle rule. Therefore, EH cells may be functionally related to the output of a forward internal model thought to construct an efference copy of the actual eye movement.

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Section: Methodsmentioning

confidence: 99%

Section: The Half-angle Rule and 3d Ocular Kinematicsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics

Ghasia¹,

Hui²,

Angelaki³

2008

J. Neurosci.

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“…5 A formerly attractive belief that the brain explicitly commands LL torsion via the vertical rectus and oblique EOMs 6 was rendered untenable by findings that cyclovertical motor neurons of monkeys do not encode LL torsion during pursuit, 7 and that abducens nerve stimulation in monkeys evokes eye movements conforming to LL. 8 Rather, as systematic changes in rectus EOM pulling directions generate LL torsion, 3 activation of any whole rectus EOM must evoke an eye movement conforming to LL. However, this mechanical constraint engendered a conundrum; while the vestibulo-ocular reflex violates LL so that its velocity axis changes by one-fourth eye position, not half as for LL, 9 motor neurons controlling cyclovertical EOMs do not command the violation.…”

Section: Mysteries Of Ocular Motor Effectorsmentioning

confidence: 99%

Compartmentalization of extraocular muscle function

Demer

2014

Eye

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Ocular motor diversity exceeds capabilities of only six extraocular muscles (EOMs), but this deficiency is overcome by the plethora of fibers within individual EOMs surpassing requirements of homogeneous actuators. This paper reviews emerging evidence that regions of individual EOMs can be differentially innervated to exert independent oculorotary torques, broadening the oculomotor repertoire, and potentially explaining diverse strabismus pathophysiology. Parallel structure characterizes EOM and tendon fibers, with little transverse coupling of experimentally imposed or actively generated tension. This arrangement enables arbitrary groupings of tendon and muscle fibers to act relatively independently. Coordinated force generation among EOM fibers occurs only upon potentially mutable coordination of innervational commands, whose central basis is suggested by preliminary findings of apparent compartmental segregation of abducens motor neuron pools. Humans, monkeys, and other mammals demonstrate separate, nonoverlapping intramuscular nerve arborizations in the superior vs inferior compartments of the medial rectus (MR) and lateral rectus (LR) EOMs that could apply force at the superior vs inferior portions of scleral insertions, and in the medial vs lateral compartments of the superior oblique that act at the equatorial vs posterior scleral insertions that might preferentially implement incycloduction vs infraduction. Magnetic resonance imaging of the MR during several physiological ocular motor behaviors indicates differential compartmental function. Differential compartmental pathology can influence clinical strabismus. Partial abducens palsy commonly affects the superior LR compartment more than the inferior, inducing vertical strabismus that might erroneously be attributed to cyclovertical EOM pathology. Surgery may selectively manipulate EOM compartments.

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“…With the head stationary, Listing's Law (LL) constrains ocular torsion to that specified by rotation from a primary position about a single axis lying in Listing's plane (Tweed and Vilis, 1987). This torsion is not encoded in the discharges of motor neurons innervating cyclovertical EOMs (Ghasia and Angelaki, 2005), yet even for abduction evoked by artificial abducens nerve stimulation, torsion conforms to LL (Klier et al, 2006). The ability of EOMs and orbital connective tissues to implement LL is explained by the active pulley hypothesis, which states that pulling directions of rectus EOMs are constrained by connective tissue pulleys that constitute their functional origins (Demer et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

Functional anatomy of the extraocular muscles during vergence

Demer¹,

Clark²,

Crane³

et al. 2008

Progress in Brain Research

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Magnetic resonance imaging (MRI) now enables precise visualization of the mechanical state of the living human orbit, enabling inferences about the effects of mechanical factors on ocular kinematics. We used 3-dimensional magnetic search coil recordings and MRI to investigate the mechanical state of the orbit during vergence in humans. Horizontal convergence of 23° from a remote to a near target aligned on one eye was geometrically ideal, and was associated with lens thickening and extorsion of the rectus pulley array of the aligned eye with superior oblique muscle relaxation and inferior oblique muscle contraction. There was no rectus muscle cocontraction. Subjective fusion through a 1° vertical prism caused a clockwise (CW) torsion in both eyes, as well as variable vertical and horizontal vergences that seldom corresponded to prism amount or direction. MRI under these conditions did not show consistent torsion of the rectus pulley array, but a complex pattern of changes in rectus extraocular muscle (EOM) crossections, consistent with co-contraction. Binocular fusion during vergence is accomplished by complex, 3D eye rotations seldom achieving binocular retinal correspondence. Vergence eye movements are sometimes associated with changes in rectus EOM pulling directions, and may sometimes be associated with co-contraction. Thus, extraretinal information about eye position would appear necessary to interpret binocular correspondence, and to avoid diplopia.

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Three-Dimensional Kinematics at the Level of the Oculomotor Plant

Cited by 55 publications

References 46 publications

Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics

Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics

Compartmentalization of extraocular muscle function

Functional anatomy of the extraocular muscles during vergence

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