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Article ; Online: Nonhuman Primate Studies to Advance Vision Science and Prevent Blindness.

Mustari, Michael J

2017 Volume 58, Issue 2, Page(s) 216–225

Abstract: Most primate behavior is dependent on high acuity vision. Optimal visual performance in primates depends heavily upon frontally placed eyes, retinal specializations, and binocular vision. To see an object clearly its image must be placed on or near the ... ...

Abstract	Most primate behavior is dependent on high acuity vision. Optimal visual performance in primates depends heavily upon frontally placed eyes, retinal specializations, and binocular vision. To see an object clearly its image must be placed on or near the fovea of each eye. The oculomotor system is responsible for maintaining precise eye alignment during fixation and generating eye movements to track moving targets. The visual system of nonhuman primates has a similar anatomical organization and functional capability to that of humans. This allows results obtained in nonhuman primates to be applied to humans. The visual and oculomotor systems of primates are immature at birth and sensitive to the quality of binocular visual and eye movement experience during the first months of life. Disruption of postnatal experience can lead to problems in eye alignment (strabismus), amblyopia, unsteady gaze (nystagmus), and defective eye movements. Recent studies in nonhuman primates have begun to discover the neural mechanisms associated with these conditions. In addition, genetic defects that target the retina can lead to blindness. A variety of approaches including gene therapy, stem cell treatment, neuroprosthetics, and optogenetics are currently being used to restore function associated with retinal diseases. Nonhuman primates often provide the best animal model for advancing fundamental knowledge and developing new treatments and cures for blinding diseases.
MeSH term(s)	Animals ; Blindness/prevention & control ; Eye Movements/physiology ; Genetic Therapy ; Optogenetics/methods ; Primates ; Strabismus/pathology ; Vision, Binocular/physiology
Language	English
Publishing date	2017-06-02
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2192062-X
ISSN	1930-6180 ; 1084-2020
ISSN (online)	1930-6180
ISSN	1084-2020
DOI	10.1093/ilar/ilx009
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Article ; Online: Response properties of MST parafoveal neurons during smooth pursuit adaptation.

Ono, Seiji / Mustari, Michael J

Journal of neurophysiology

2016 Volume 116, Issue 1, Page(s) 210–217

Abstract: Visual motion neurons in the posterior parietal cortex play a critical role in the guidance of smooth pursuit eye movements. Initial pursuit (open-loop period) is driven, in part, by visual motion signals from cortical areas, such as the medial superior ... ...

Abstract	Visual motion neurons in the posterior parietal cortex play a critical role in the guidance of smooth pursuit eye movements. Initial pursuit (open-loop period) is driven, in part, by visual motion signals from cortical areas, such as the medial superior temporal area (MST). The purpose of this study was to determine whether adaptation of initial pursuit gain arises because of altered visual sensitivity of neurons at the cortical level. It is well known that the visual motion response in MST is suppressed after exposure to a large-field visual motion stimulus, showing visual motion adaptation. One hypothesis is that foveal motion responses in MST are associated with smooth pursuit adaptation using a small target spot. We used a step-ramp tracking task with two steps of target velocity (double-step paradigm), which induces gain-down or gain-up adaptation. We found that after gain-down adaptation 58% of our MST visual neurons showed a significant decrease in firing rate. This was the case even though visual motion input (before the pursuit onset) from target motion was constant. Therefore, repetitive visual stimulation during the gain-down paradigm could lead to adaptive changes in the visual response. However, the time course of adaptation did not show a correlation between the visual response and pursuit behavior. These results indicate that the visual response in MST may not directly contribute to the adaptive change in pursuit initiation.
MeSH term(s)	Adaptation, Physiological/physiology ; Adaptation, Psychological/physiology ; Animals ; Macaca mulatta ; Microelectrodes ; Motion Perception/physiology ; Neurons/physiology ; Photic Stimulation ; Pursuit, Smooth/physiology ; Temporal Lobe/physiology
Language	English
Publishing date	2016--01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00203.2016
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Article ; Online: Childhood Onset Strabismus: A Neurotrophic Factor Hypothesis.

Rudell, Jolene C / Fleuriet, Jérome / Mustari, Michael J / McLoon, Linda K

Journal of binocular vision and ocular motility

2021 Volume 71, Issue 2, Page(s) 35–40

Abstract: Strabismus is a genetically heterogeneous disorder with complex molecular and neurophysiological causes. Evidence in the literature suggests a strong role for motor innervation in the etiology of strabismus, which connects central neural processes to the ...

Abstract	Strabismus is a genetically heterogeneous disorder with complex molecular and neurophysiological causes. Evidence in the literature suggests a strong role for motor innervation in the etiology of strabismus, which connects central neural processes to the peripheral extraocular muscles. Current treatments of strabismus through surgery show that an inherent sensorimotor plasticity in the ocular motor system decreases the effectiveness of treatment, often driving eye alignment back toward its misaligned pre-surgical state by altering extraocular muscle tonus. There is recent interest in capitalizing on existing biological processes in extraocular muscles to overcome these compensatory mechanisms. Neurotrophins are trophic factors that regulate survival and development in neurons and muscle, including extraocular muscles. Local administration of neurotrophins to extraocular muscles partially reversed strabismus in an animal model of strabismus. The hypothesis is that sustained release of neurotrophins gives more time for the ocular motor system to adapt to a slow change in alignment in the desired direction. The effect of neurotrophins on extraocular muscles is complex, as different neurotrophic factors have diverse effects on extraocular muscle contraction profiles, patterns of innervation, and density of extraocular muscle precursor cells. Neurotrophic factors show promise as a therapeutic option for strabismus, which may help to improve treatment outcomes and offset devastating amblyopia and psychosocial effects of disease in strabismus patients.
MeSH term(s)	Adaptation, Physiological ; Amblyopia ; Animals ; Child ; Humans ; Nerve Growth Factors ; Oculomotor Muscles/surgery ; Strabismus/surgery
Chemical Substances	Nerve Growth Factors
Language	English
Publishing date	2021-04-19
Publishing country	United States
Document type	Journal Article
ISSN	2576-1218
ISSN (online)	2576-1218
DOI	10.1080/2576117X.2021.1893585
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Article ; Online: Eye alignment changes caused by sustained GDNF treatment of an extraocular muscle in infant non-human primates.

Fleuriet, Jérome / Willoughby, Christy L / Kueppers, Rachel B / Mustari, Michael J / McLoon, Linda K

Scientific reports

2020 Volume 10, Issue 1, Page(s) 11927

Abstract: The ability of sustained treatment of a single extraocular muscle with glial cell line-derived neurotrophic factor (GDNF) to produce a strabismus in infant non-human primates was tested. Six infant non-human primates received a pellet containing GDNF, ... ...

Abstract	The ability of sustained treatment of a single extraocular muscle with glial cell line-derived neurotrophic factor (GDNF) to produce a strabismus in infant non-human primates was tested. Six infant non-human primates received a pellet containing GDNF, releasing 2 µg/day for 90 days, on one medial rectus muscle. Eye alignment was assessed up to 6 months. Five of the six animals showed a slow decrease in eye misalignment from the significant exotropia present at birth, ending with approximately 10° of exotropia. Controls became orthotropic. Misalignment averaged 8° three months after treatment ended. After sustained GDNF treatment, few changes were seen in mean myofiber cross-sectional areas compared to age-matched naïve controls. Neuromuscular junction number was unaltered in the medial rectus muscles, but were significantly reduced in the untreated lateral recti. Neuromuscular junctions on slow fibers became multiply innervated after this sustained GDNF treatment. Pitx2-positive cells significantly decreased in treated and contralateral medial rectus muscles. Our study suggests that balanced GDNF signaling plays a role in normal development and maintenance of orthotropia. Sustained GDNF treatment of one medial rectus muscle resulted in a measurable misalignment largely maintained 3 months after treatment ended. Structural changes suggest mechanisms for producing an imbalance in muscle function.
MeSH term(s)	Animals ; Eye/drug effects ; Female ; Glial Cell Line-Derived Neurotrophic Factor/pharmacology ; Haplorhini ; Male ; Muscle Development/drug effects ; Neuromuscular Junction/drug effects ; Oculomotor Muscles/innervation ; Oculomotor Muscles/physiology ; Stem Cells/drug effects ; Stem Cells/metabolism ; Time Factors
Chemical Substances	Glial Cell Line-Derived Neurotrophic Factor
Language	English
Publishing date	2020-07-17
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-020-68743-3
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Article ; Online: FEFsem neuronal response during combined volitional and reflexive pursuit.

Bakst, Leah / Fleuriet, Jérome / Mustari, Michael J

Journal of vision

2017 Volume 17, Issue 5, Page(s) 13

Abstract: Although much is known about volitional and reflexive smooth eye movements individually, much less is known about how they are coordinated. It is hypothesized that separate cortico-ponto-cerebellar loops subserve these different types of smooth eye ... ...

Abstract	Although much is known about volitional and reflexive smooth eye movements individually, much less is known about how they are coordinated. It is hypothesized that separate cortico-ponto-cerebellar loops subserve these different types of smooth eye movements. Specifically, the MT-MST-DLPN pathway is thought to be critical for ocular following eye movements, whereas the FEF-NRTP pathway is understood to be vital for volitional smooth pursuit. However, the role that these loops play in combined volitional and reflexive behavior is unknown. We used a large, textured background moving in conjunction with a small target spot to investigate the eye movements evoked by a combined volitional and reflexive pursuit task. We also assessed the activity of neurons in the smooth eye movement subregion of the frontal eye field (FEFsem). We hypothesized that the pursuit system would show less contribution from the volitional pathway in this task, owing to the increased involvement of the reflexive pathway. In accordance with this hypothesis, a majority of FEFsem neurons (63%) were less active during pursuit maintenance in a combined volitional and reflexive pursuit task than during purely volitional pursuit. Interestingly and surprisingly, the neuronal response to the addition of the large-field motion was highly correlated with the neuronal response to a target blink. This suggests that FEFsem neuronal responses to these different perturbations-whether the addition or subtraction of retinal input-may be related. We conjecture that these findings are due to changing weights of both the volitional and reflexive pathways, as well as retinal and extraretinal signals.
MeSH term(s)	Animals ; Macaca mulatta ; Models, Animal ; Neurons/physiology ; Photic Stimulation ; Pursuit, Smooth/physiology ; Visual Perception/physiology ; Volition/physiology
Language	English
Publishing date	2017-05-01
Publishing country	United States
Document type	Journal Article
ZDB-ID	2106064-2
ISSN	1534-7362 ; 1534-7362
ISSN (online)	1534-7362
ISSN	1534-7362
DOI	10.1167/17.5.13
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Article ; Online: Comparison of three models of saccade disconjugacy in strabismus.

Walton, Mark M G / Mustari, Michael J

Journal of neurophysiology

2017 Volume 118, Issue 6, Page(s) 3175–3193

Abstract: In pattern strabismus the horizontal and vertical misalignments vary with eye position along the orthogonal axis. The disorder is typically described in terms of overaction or underaction of oblique muscles. Recent behavioral studies in humans and ... ...

Abstract	In pattern strabismus the horizontal and vertical misalignments vary with eye position along the orthogonal axis. The disorder is typically described in terms of overaction or underaction of oblique muscles. Recent behavioral studies in humans and monkeys, however, have reported that such actions are insufficient to fully explain the patterns of directional and amplitude disconjugacy of saccades. There is mounting evidence that the oculomotor abnormalities associated with strabismus are at least partially attributable to neurophysiological abnormalities. A number of control systems models have been developed to simulate the kinematic characteristics of saccades in normal primates. In the present study we sought to determine whether these models could simulate the abnormalities of saccades in strabismus by making two assumptions:
MeSH term(s)	Animals ; Evoked Potentials, Visual ; Macaca mulatta ; Models, Neurological ; Saccades ; Strabismus/physiopathology
Language	English
Publishing date	2017-12-01
Publishing country	United States
Document type	Comparative Study ; Journal Article
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00983.2016
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Article ; Online: Temporal dynamics of retinal and extraretinal signals in the FEFsem during smooth pursuit eye movements.

Bakst, Leah / Fleuriet, Jérome / Mustari, Michael J

Journal of neurophysiology

2017 Volume 117, Issue 5, Page(s) 1987–2003

Abstract: Neurons in the smooth eye movement subregion of the frontal eye field (FEFsem) are known to play an important role in voluntary smooth pursuit eye movements. Underlying this function are projections to parietal and prefrontal visual association areas and ...

Abstract	Neurons in the smooth eye movement subregion of the frontal eye field (FEFsem) are known to play an important role in voluntary smooth pursuit eye movements. Underlying this function are projections to parietal and prefrontal visual association areas and subcortical structures, all known to play vital but differing roles in the execution of smooth pursuit. Additionally, the FEFsem has been shown to carry a diverse array of signals (e.g., eye velocity, acceleration, gain control). We hypothesized that distinct subpopulations of FEFsem neurons subserve these diverse functions and projections, and that the relative weights of retinal and extraretinal signals could form the basis for categorization of units. To investigate this, we used a step-ramp tracking task with a target blink to determine the relative contributions of retinal and extraretinal signals in individual FEFsem neurons throughout pursuit. We found that the contributions of retinal and extraretinal signals to neuronal activity and behavior change throughout the time course of pursuit. A clustering algorithm revealed three distinct neuronal subpopulations:
MeSH term(s)	Animals ; Macaca mulatta ; Neurons/physiology ; Prefrontal Cortex/cytology ; Prefrontal Cortex/physiology ; Pursuit, Smooth ; Retina/physiology ; Visual Fields ; Visual Perception
Language	English
Publishing date	2017-02-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00786.2016
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Article ; Online: Response of supraoculomotor area neurons during combined saccade-vergence movements.

Pallus, Adam C / Walton, Mark M G / Mustari, Michael J

Journal of neurophysiology

2017 Volume 119, Issue 2, Page(s) 585–596

Abstract: Combined saccade-vergence movements allow humans and other primates to align their eyes with objects of interest in three-dimensions. In the absence of saccades, vergence movements are typically slow, symmetrical movements of the two eyes in opposite ... ...

Abstract	Combined saccade-vergence movements allow humans and other primates to align their eyes with objects of interest in three-dimensions. In the absence of saccades, vergence movements are typically slow, symmetrical movements of the two eyes in opposite directions. However, combined saccade-vergence movements produce vergence velocities that exceed values observed during vergence alone. This phenomenon is often called "vergence enhancement", or "saccade-facilitated vergence," though it is important to consider that rapid vergence changes, known as "vergence transients," are also observed during conjugate saccades. We developed a visual target array that allows monkeys to make saccades in all directions between targets spaced at distances that correspond to ~1° intervals of vergence angle relative to the monkey. We recorded the activity of vergence-sensitive neurons in the supra-oculomotor area (SOA), located dorsal and lateral to the oculomotor nucleus while monkeys made saccades with vergence amplitudes ranging from 0 to 10°. The primary focus of this study was to test the hypothesis that neurons in the SOA fire a high frequency burst of spikes during saccades that could generate the enhanced vergence. We found that individual neurons encode vergence velocity during both saccadic and non-saccadic vergence, yet firing rates were insufficient to produce the observed enhancement of vergence velocity. Our results are consistent with the hypothesis that slow vergence changes are encoded by the SOA while fast vergence movements require an additional contribution from the saccadic system. NEW & NOTEWORTHY Research into combined saccade-vergence movements has so far focused on exploring the saccadic neural circuitry, leading to diverging hypotheses regarding the role of the vergence system in this behavior. In this study, we report the first quantitative analysis of the discharge of individual neurons that encode vergence velocity in the monkey brain stem during combined saccade-vergence movements.
MeSH term(s)	Animals ; Female ; Macaca mulatta ; Neurons/physiology ; Oculomotor Nuclear Complex/physiology ; Saccades
Language	English
Publishing date	2017-11-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00193.2017
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Article ; Online: Abnormal tuning of saccade-related cells in pontine reticular formation of strabismic monkeys.

Walton, Mark M G / Mustari, Michael J

Journal of neurophysiology

2015 Volume 114, Issue 2, Page(s) 857–868

Abstract: Strabismus is a common disorder, characterized by a chronic misalignment of the eyes and numerous visual and oculomotor abnormalities. For example, saccades are often highly disconjugate. For humans with pattern strabismus, the horizontal and vertical ... ...

Abstract	Strabismus is a common disorder, characterized by a chronic misalignment of the eyes and numerous visual and oculomotor abnormalities. For example, saccades are often highly disconjugate. For humans with pattern strabismus, the horizontal and vertical disconjugacies vary with eye position. In monkeys, manipulations that disturb binocular vision during the first several weeks of life result in a chronic strabismus with characteristics that closely match those in human patients. Early onset strabismus is associated with altered binocular sensitivity of neurons in visual cortex. Here we test the hypothesis that brain stem circuits specific to saccadic eye movements are abnormal. We targeted the pontine paramedian reticular formation, a structure that directly projects to the ipsilateral abducens nucleus. In normal animals, neurons in this structure are characterized by a high-frequency burst of spikes associated with ipsiversive saccades. We recorded single-unit activity from 84 neurons from four monkeys (two normal, one exotrope, and one esotrope), while they made saccades to a visual target on a tangent screen. All 24 neurons recorded from the normal animals had preferred directions within 30° of pure horizontal. For the strabismic animals, the distribution of preferred directions was normal on one side of the brain, but highly variable on the other. In fact, 12/60 neurons recorded from the strabismic animals preferred vertical saccades. Many also had unusually weak or strong bursts. These data suggest that the loss of corresponding binocular vision during infancy impairs the development of normal tuning characteristics for saccade-related neurons in brain stem.
MeSH term(s)	Action Potentials ; Animals ; Disease Models, Animal ; Electric Stimulation ; Female ; Functional Laterality ; Lenses ; Macaca mulatta ; Microelectrodes ; Motor Activity/physiology ; Neural Pathways/physiopathology ; Neurons/physiology ; Photic Stimulation ; Pontine Tegmentum/physiopathology ; Regression Analysis ; Saccades/physiology ; Strabismus/physiopathology ; Visual Perception/physiology
Language	English
Publishing date	2015-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00238.2015
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Article ; Online: Role of MSTd extraretinal signals in smooth pursuit adaptation.

Ono, Seiji / Mustari, Michael J

Cerebral cortex (New York, N.Y. : 1991)

2011 Volume 22, Issue 5, Page(s) 1139–1147

Abstract: The smooth pursuit (SP) system is able to adapt to challenges associated with development or system drift to maintain pursuit accuracy. Short-term adaptation of SP can be produced experimentally using a step-ramp tracking paradigm with 2 steps of ... ...

Abstract	The smooth pursuit (SP) system is able to adapt to challenges associated with development or system drift to maintain pursuit accuracy. Short-term adaptation of SP can be produced experimentally using a step-ramp tracking paradigm with 2 steps of velocity (double-step paradigm). Previous studies have demonstrated that the macaque cerebellum plays an essential role in SP adaptation. However, it remains uncertain whether neuronal activity in afferent structures to the cerebellum shows changes associated with SP adaptation. Therefore, we focused on the dorsal-medial part of medial superior temporal cortex (MSTd), which is part of the cortico-ponto-cerebellar pathway thought to provide extraretinal signals needed for maintaining SP. We found that 54% of the SP-related neurons showed significant changes in the first 100 ms of response correlated with adaptive changes of initial pursuit. Our results indicate that some cortical neurons in MSTd could be inside the circuit involved in SP adaptation. Furthermore, our sample of MSTd neurons started their discharge on average 103 ms after SP onset. Therefore, we suggest that extraretinal signals carried in MSTd might be due to efference copy of pursuit eye velocity signals, which reflect plastic changes in the downstream motor output pathways (e.g., the cerebellum).
MeSH term(s)	Adaptation, Physiological/physiology ; Animals ; Electrophysiology ; Macaca mulatta ; Motion Perception/physiology ; Neural Pathways/physiology ; Neurons/physiology ; Photic Stimulation ; Pursuit, Smooth/physiology ; Temporal Lobe/physiology
Language	English
Publishing date	2011-07-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1077450-6
ISSN	1460-2199 ; 1047-3211
ISSN (online)	1460-2199
ISSN	1047-3211
DOI	10.1093/cercor/bhr188
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