Sustained and transient discharges of retinal ganglion cells during spontaneous eye movements of cat

During animal locomotion or position adjustments, the visual system uses image stabilization reflexes to compensate for global shifts in the visual scene. These reflexes elicit compensatory head movements (optomotor response, OMR) in unrestrained animals or compensatory eye movements (optokinetic response, OKR) in head-fixed or unrestrained animals exposed to globally rotating striped patterns. In mice, OMR are relatively easy to observe and find broad use in the rapid evaluation of visual function. OKR determinations are more involved experimentally but yield more stereotypical, easily quantifiable results. The relative contributions of head and eye movements to image stabilization in mice have not been investigated. We are using newly developed software and apparatus to accurately quantitate mouse head movements during OMR, quantitate eye movements during OKR, and determine eye movements in freely behaving mice. We provide the first direct comparison of OMR and OKR gains (head or eye velocity/stimulus velocity) and find that the two reflexes have comparable dependencies on stimulus luminance, contrast, spatial frequency, and velocity. OMR and OKR are similarly affected in genetically modified mice with defects in retinal ganglion cells (RGC) compared with wild-type, suggesting they are driven by the same sensory input (RGC type). OKR eye movements have much higher gains than the OMR head movements, but neither can fully compensate global visual shifts. However, combined eye and head movements can be detected in unrestrained mice performing OMR, suggesting they can cooperate to achieve image stabilization, as previously described for other species. NEW & NOTEWORTHY We provide the first quantitation of head gain during optomotor response in mice and show that optomotor and optokinetic responses have similar psychometric curves. Head gains are far smaller than eye gains. Unrestrained mice combine head and eye movements to respond to visual stimuli, and both monocular and binocular fields are used during optokinetic responses. Mouse OMR and OKR movements are heterogeneous under optimal and suboptimal stimulation and are affected in mice lacking ON direction-selective retinal ganglion cells.

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Analysis of vertebrate eye movements following intravitreal drug injections. I. Blockade of retinal ON-cells by 2-amino-4-phosphonobutyrate eliminates optokinetic nystagmus

Journal of Neurophysiology ◽

10.1152/jn.1988.60.3.1010 ◽

1988 ◽

Vol 60 (3) ◽

pp. 1010-1021 ◽

Cited By ~ 16

Author(s):

A. G. Knapp ◽

M. Ariel ◽

F. R. Robinson

Keyword(s):

Visual Cortex ◽

Eye Movements ◽

Retinal Ganglion Cells ◽

Optokinetic Nystagmus ◽

Ganglion Cells ◽

Directional Asymmetry ◽

Retinal Ganglion ◽

Binocular Stimulation ◽

Vertebrate Eye ◽

Stimulation Of

1. Horizontal optokinetic nystagmus (OKN) was examined in alert rabbits and cats following intravitreal injection of 2-amino-4-phosphonobutyrate (APB), an agent which selectively blocks the light-responsiveness of retinal ON-cells while having little effect on OFF-cells. The retinal actions of APB were assessed independently by electroretinography. 2. In five rabbits, doses of APB sufficient to eliminate the b-wave of the electroretinogram reduced drastically the ability of the injected eye to drive OKN at all stimulus speeds tested (1-96 degrees/s). Impairment of OKN was apparent within minutes of the injection, remained maximal for several hours, and recovered completely in 1-7 days. OKN in response to stimulation of the uninjected eye alone remained qualitatively and quantitatively normal. 3. Following administration of APB, OKN in response to binocular stimulation displayed a directional asymmetry. Stimuli moving in the preferred (temporal-to-nasal) direction for the uninjected eye became more effective than stimuli moving in the opposite direction, indicating that the injected eye could no longer contribute to binocular OKN. 4. When rabbits viewed stationary stimuli through the APB-treated eye alone, episodes of slow (less than 1 degrees/s) ocular drift were observed, similar to the positional instability seen when rabbits are placed in darkness or when the retinal image is stablized artifically (12). 5. APB had little effect on OKN in normal cats. In two cats that had previously received large lesions of the visual cortex, however, APB eliminated the ability of the injected eye to drive monocular OKN. The extent of the impairment was similar to that seen in rabbits. Because the cortex is thought to contribute more to OKN in cats than in rabbits, this result suggests that the optokinetic pathways disrupted by APB project subcortically. 6. This study demonstrates that the integrity of retinal ON-cells is required to sustain normal OKN. The results are consistent with additional anatomic and physiological evidence suggesting that a particular subclass of retinal ganglion cells, the ON-direction-selective cells, may provide a crucial source of visual input to central optokinetic pathways.

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Decorrelation of retinal response to natural scenes by fixational eye movements

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1412059112 ◽

2015 ◽

Vol 112 (10) ◽

pp. 3110-3115 ◽

Cited By ~ 13

Author(s):

Irina Yonit Segal ◽

Chen Giladi ◽

Michael Gedalin ◽

Michele Rucci ◽

Mor Ben-Tov ◽

...

Keyword(s):

Eye Movements ◽

Retinal Ganglion Cells ◽

Visual Information ◽

Ganglion Cells ◽

Natural World ◽

Natural Scenes ◽

Retinal Ganglion ◽

Spatial Correlations ◽

Fixational Eye Movements ◽

Spatiotemporal Signal

Under natural viewing conditions the input to the retina is a complex spatiotemporal signal that depends on both the scene and the way the observer moves. It is commonly assumed that the retina processes this input signal efficiently by taking into account the statistics of the natural world. It has recently been argued that incessant microscopic eye movements contribute to this process by decorrelating the input to the retina. Here we tested this theory by measuring the responses of the salamander retina to stimuli replicating the natural input signals experienced by the retina in the presence and absence of fixational eye movements. Contrary to the predictions of classic theories of efficient encoding that do not take behavior into account, we show that the response characteristics of retinal ganglion cells are not sufficient in themselves to disrupt the broad correlations of natural scenes. Specifically, retinal ganglion cells exhibited strong and extensive spatial correlations in the absence of fixational eye movements. However, the levels of correlation in the neural responses dropped in the presence of fixational eye movements, resulting in effective decorrelation of the channels streaming information to the brain. These observations confirm the predictions that microscopic eye movements act to reduce correlations in retinal responses and contribute to visual information processing.

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