The effect of attentive fixation on eye movements evoked by electrical stimulation of the frontal eye fields

The frontal eye field (FEF), an area in the primate frontal lobe, has long been considered important for the production of eye movements. Past studies have evoked saccade-like movements from the FEF using electrical stimulation in animals that were not allowed to move their heads. Using electrical stimulation in two monkeys that were free to move their heads, we have found that the FEF produces gaze shifts that are composed of both eye and head movements. Repeated stimulation at a site evoked gaze shifts of roughly constant amplitude. However, that gaze shift could be accomplished with varied amounts of head and eye movements, depending on their (head and eye) respective starting positions. This evidence suggests that the FEF controls visually orienting movements using both eye and head rotations rather than just shifting the eyes as previously thought.

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Doing Without Learning: Stimulation of the Frontal Eye Fields and Floccular Complex Does Not Instruct Motor Learning in Smooth Pursuit Eye Movements

Journal of Neurophysiology ◽

10.1152/jn.90492.2008 ◽

2008 ◽

Vol 100 (3) ◽

pp. 1320-1331 ◽

Cited By ~ 2

Author(s):

Hilary W. Heuer ◽

Stefanie Tokiyama ◽

Stephen G. Lisberger

Keyword(s):

Electrical Stimulation ◽

Eye Movements ◽

Motor Learning ◽

Visual Image ◽

Image Motion ◽

Frontal Eye Fields ◽

Electrical Microstimulation ◽

Pursuit Eye Movements ◽

Time Period ◽

Fixed Times

Under natural conditions, motor learning is instructed by sensory feedback. We have asked whether sensory signals that indicate motor errors are necessary to instruct learning or if the motor signals related to movements normally driven by sensory error signals would be sufficient. We measured eye movements in trained rhesus monkeys while employing electrical microstimulation of the floccular complex of the cerebellum and the smooth eye movement region of the frontal eye fields to alter ongoing pursuit eye movements. Repeated electrical stimulation at fixed times after the onset of target motion and pursuit failed to cause any learning that was retained beyond the time period used to instruct learning. Learning was not uncovered when the target was stabilized with respect to the moving eye to prevent competition between instructive signals created by electrical stimulation and visual image motion signals evoked when stimulation drove the eye away from the tracking target. We suggest that signals emanating from motor-related structures in the pursuit circuit do not instruct learning. Instead, instructive sensory error signals seem to be necessary.

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New Mechanism That Accounts for Position Sensitivity of Saccades Evoked in Response to Stimulation of Superior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.1998.80.6.3373 ◽

1998 ◽

Vol 80 (6) ◽

pp. 3373-3379 ◽

Cited By ~ 15

Author(s):

A. K. Moschovakis ◽

Y. Dalezios ◽

J. Petit ◽

A. A. Grantyn

Keyword(s):

Electrical Stimulation ◽

Eye Movements ◽

Superior Colliculus ◽

Short Duration ◽

High Frequency ◽

Initial Position ◽

Characteristic Vector ◽

Extraocular Motoneurons ◽

Position Sensitivity ◽

Stimulation Of

Moschovakis, A. K., Y. Dalezios, J. Petit, and A. A. Grantyn. New mechanism that accounts for position sensitivity of saccades evoked in response to stimulation of superior colliculus. J. Neurophysiol. 80: 3373–3379, 1998. Electrical stimulation of the feline superior colliculus (SC) is known to evoke saccades whose size depends on the site stimulated (the “characteristic vector” of evoked saccades) and the initial position of the eyes. Similar stimuli were recently shown to produce slow drifts that are presumably caused by relatively direct projections of the SC onto extraocular motoneurons. Both slow and fast evoked eye movements are similarly affected by the initial position of the eyes, despite their dissimilar metrics, kinematics, and anatomic substrates. We tested the hypothesis that the position sensitivity of evoked saccades is due to the superposition of largely position-invariant saccades and position-dependent slow drifts. We show that such a mechanism can account for the fact that the position sensitivity of evoked saccades increases together with the size of their characteristic vector. Consistent with it, the position sensitivity of saccades drops considerably when the contribution of slow drifts is minimal as, for example, when there is no overlap between evoked saccades and short-duration trains of high-frequency stimuli.

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Vestibular implantation and longitudinal electrical stimulation of the semicircular canal afferents in human subjects

Journal of Neurophysiology ◽

10.1152/jn.00171.2013 ◽

2015 ◽

Vol 113 (10) ◽

pp. 3866-3892 ◽

Cited By ~ 35

Author(s):

James O. Phillips ◽

Leo Ling ◽

Kaibao Nie ◽

Elyse Jameyson ◽

Christopher M. Phillips ◽

...

Keyword(s):

Electrical Stimulation ◽

Eye Movements ◽

Human Subjects ◽

Vestibular Function ◽

Slow Phase ◽

Vestibular Loss ◽

Stimulation Current ◽

Eye Velocity ◽

Over Time ◽

Stimulation Of

Animal experiments and limited data in humans suggest that electrical stimulation of the vestibular end organs could be used to treat loss of vestibular function. In this paper we demonstrate that canal-specific two-dimensionally (2D) measured eye velocities are elicited from intermittent brief 2 s biphasic pulse electrical stimulation in four human subjects implanted with a vestibular prosthesis. The 2D measured direction of the slow phase eye movements changed with the canal stimulated. Increasing pulse current over a 0–400 μA range typically produced a monotonic increase in slow phase eye velocity. The responses decremented or in some cases fluctuated over time in most implanted canals but could be partially restored by changing the return path of the stimulation current. Implantation of the device in Meniere's patients produced hearing and vestibular loss in the implanted ear. Electrical stimulation was well tolerated, producing no sensation of pain, nausea, or auditory percept with stimulation that elicited robust eye movements. There were changes in slow phase eye velocity with current and over time, and changes in electrically evoked compound action potentials produced by stimulation and recorded with the implanted device. Perceived rotation in subjects was consistent with the slow phase eye movements in direction and scaled with stimulation current in magnitude. These results suggest that electrical stimulation of the vestibular end organ in human subjects provided controlled vestibular inputs over time, but in Meniere's patients this apparently came at the cost of hearing and vestibular function in the implanted ear.

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Localization of human frontal eye fields: anatomical and functional findings of functional magnetic resonance imaging and intracerebral electrical stimulation

Journal of Neurosurgery ◽

10.3171/jns.2001.95.5.0804 ◽

2001 ◽

Vol 95 (5) ◽

pp. 804-815 ◽

Cited By ~ 61

Author(s):

Elie Lobel ◽

Philippe Kahane ◽

Ute Leonards ◽

Marie-Hélène Grosbras ◽

Stéphane Lehéricy ◽

...

Keyword(s):

Electrical Stimulation ◽

Eye Movements ◽

Magnetic Resonance ◽

3 Tesla ◽

Frontal Eye Fields ◽

Precentral Gyrus ◽

Functional Magnetic Resonance ◽

Content Type ◽

Cortical Areas ◽

Fine Print

Object. The goal of this study was to investigate the anatomical localization and functional role of human frontal eye fields (FEFs) by comparing findings from two independently conducted studies. Methods. In the first study, 3-tesla functional magnetic resonance (fMR) imaging was performed in 14 healthy volunteers divided into two groups: the first group executed self-paced voluntary saccades in complete darkness and the second group repeated newly learned or familiar sequences of saccades. In the second study, intracerebral electrical stimulation (IES) was performed in 38 patients with epilepsy prior to surgery, and frontal regions where stimulation induced versive eye movements were identified. These studies showed that two distinct oculomotor areas (OMAs) could be individualized in the region classically corresponding to the FEFs. One OMA was consistently located at the intersection of the superior frontal sulcus with the fundus of the superior portion of the precentral sulcus, and was the OMA in which saccadic eye movements could be the most easily elicited by electrical stimulation. The second OMA was located more laterally, close to the surface of the precentral gyrus. The fMR imaging study and the IES study demonstrated anatomical and stereotactic agreement in the identification of these cortical areas. Conclusions. These findings indicate that infracentimetric localization of cortical areas can be achieved by measuring the vascular signal with the aid of 3-tesla fMR imaging and that neuroimaging and electrophysiological recording can be used together to obtain a better understanding of the human cortical functional anatomy.

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Spatial and temporal properties of eye movements produced by electrical stimulation of semicircular canal afferents

Journal of Neurophysiology ◽

10.1152/jn.01029.2011 ◽

2012 ◽

Vol 108 (5) ◽

pp. 1511-1520 ◽

Cited By ~ 6

Author(s):

Richard F. Lewis ◽

Csilla Haburcakova ◽

Wangsong Gong ◽

Faisal Karmali ◽

Daniel M. Merfeld

Keyword(s):

Electrical Stimulation ◽

Eye Movements ◽

Semicircular Canal ◽

Low Frequency ◽

Velocity Storage ◽

Rotational Axis ◽

Temporal Properties ◽

Normal Manner ◽

Semicircular Canal Afferents ◽

Stimulation Of

To investigate the characteristics of eye movements produced by electrical stimulation of semicircular canal afferents, we studied the spatial and temporal features of eye movements elicited by short-term lateral canal stimulation in two squirrel monkeys with plugged lateral canals, with the head upright or statically tilted in the roll plane. The electrically induced vestibuloocular reflex (eVOR) evoked with the head upright decayed more quickly than the stimulation signal provided by the electrode, demonstrating an absence of the classic velocity storage effect that improves the dynamics of the low-frequency VOR. When stimulation was provided with the head tilted in roll, however, the eVOR decayed more rapidly than when the head was upright, and a cross-coupled vertical response developed that shifted the eye's rotational axis toward alignment with gravity. These results demonstrate that rotational information provided by electrical stimulation of canal afferents interacts with otolith inputs (or other graviceptive cues) in a qualitatively normal manner, a process that is thought to be mediated by the velocity storage network. The observed interaction between the eVOR and graviceptive cues is of critical importance for the development of a functionally useful vestibular prosthesis. Furthermore, the presence of gravity-dependent effects (dumping, spatial orientation) despite an absence of low-frequency augmentation of the eVOR has not been previously described in any experimental preparation.

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Central nystagmus. III. Functional correlations of mesodiencephalic nystagmogenic center

American Journal of Physiology-Legacy Content ◽

10.1152/ajplegacy.1959.197.2.454 ◽

1959 ◽

Vol 197 (2) ◽

pp. 454-460 ◽

Cited By ~ 27

Author(s):

F. Bergmann ◽

J. Lachmann ◽

M. Monnier ◽

P. Krupp

Keyword(s):

Electrical Stimulation ◽

Eye Movements ◽

Vestibular Nuclei ◽

Rabbit Brain ◽

Vestibular Nystagmus ◽

Posterior Commissure ◽

Common Substrate ◽

The Common ◽

Stimulation Of

Transverse cuts at various levels of the rabbit brain stem have different effects on vestibular nystagmus and on central nystagmus elicited by electrical stimulation of the mesodiencephalic nystagmogenic area. While transections rostral to the sensitive region enhance both, probably by elimination of inhibitory influences from cortex or retina, transections caudal to this region, but rostral to the colliculi, abolish central nystagmus only. Transections at the level of the inferior colliculus abolish vestibular nystagmus only, while intermediate cuts may eliminate either response. When central nystagmus alone survives, its character is changed in a specific way indicating the important role of the vestibular nuclei in normal central nystagmus. These observations lead to an approximate localization of the common substrate for conjugate eye movements involved both in central and vestibular nystagmus. Longitudinal cuts through the posterior commissure provoke a temporary disconjugated nystagmus not described hitherto.

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