A model of the dynamics of retinal activity during natural visual fixation

2007 ◽  
Vol 24 (2) ◽  
pp. 217-230 ◽  
Author(s):  
GAËLLE DESBORDES ◽  
MICHELE RUCCI

During visual fixation, small eye movements keep the retinal image continuously in motion. It is known that neurons in the visual system are sensitive to the spatiotemporal modulations of luminance resulting from this motion. In this study, we examined the influence of fixational eye movements on the statistics of neural activity in the macaque's retina during the brief intersaccadic periods of natural visual fixation. The responses of parvocellular (P) and magnocellular (M) ganglion cells in different regions of the visual field were modeled while their receptive fields scanned natural images following recorded traces of eye movements. Immediately after the onset of fixation, wide ensembles of coactive ganglion cells extended over several degrees of visual angle, both in the central and peripheral regions of the visual field. Following this initial pattern of activity, the covariance between the responses of pairs of P and M cells and the correlation between the responses of pairs of M cells dropped drastically during the course of fixation. Cell responses were completely uncorrelated by the end of a typical 300-ms fixation. This dynamic spatial decorrelation of retinal activity is a robust phenomenon independent of the specifics of the model. We show that it originates from the interaction of three factors: the statistics of natural scenes, the small amplitudes of fixational eye movements, and the temporal sensitivities of ganglion cells. These results support the hypothesis that fixational eye movements, by shaping the statistics of retinal activity, are an integral component of early visual representations.

2015 ◽  
Vol 112 (10) ◽  
pp. 3110-3115 ◽  
Author(s):  
Irina Yonit Segal ◽  
Chen Giladi ◽  
Michael Gedalin ◽  
Michele Rucci ◽  
Mor Ben-Tov ◽  
...  

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.


2004 ◽  
Vol 21 (5) ◽  
pp. 725-738 ◽  
Author(s):  
MICHELE RUCCI ◽  
ANTONINO CASILE

Early in life, visual experience appears to influence the refinement and maintenance of the orientation-selective responses of neurons in the primary visual cortex. After eye opening, the statistical structure of visually driven neural responses depends not only on the stimulus, but also on how the stimulus is scanned during behavior. Modulations of neural activity due to behavior may thus play a role in the experience-dependent refinement of cell response characteristics. To investigate the possible influences of eye movements on the maturation of thalamocortical connectivity, we have simulated the responses of neuronal populations in the lateral geniculate nucleus (LGN) and V1 of the cat while images of natural scenes were scanned in a way that replicated the cat's oculomotor activity. In the model, fixational eye movements were essential to attenuate neural sensitivity to the broad correlational structure of natural visual input, decorrelate neural responses, and establish a regime of neural activity that was compatible with a Hebbian segregation of geniculate afferents to the cortex. We show that this result is highly robust and does not depend on the precise characteristics of the model.


2007 ◽  
Vol 97 (5) ◽  
pp. 3439-3448 ◽  
Author(s):  
Yamei Tang ◽  
Alan Saul ◽  
Moshe Gur ◽  
Stephanie Goei ◽  
Elsie Wong ◽  
...  

Studies of visual function in behaving subjects require that stimuli be positioned reliably on the retina in the presence of eye movements. Fixational eye movements scatter stimuli about the retina, inflating estimates of receptive field dimensions, reducing estimates of peak responses, and blurring maps of receptive field subregions. Scleral search coils are frequently used to measure eye position, but their utility for correcting the effects of fixational eye movements on receptive field maps has been questioned. Using eye coils sutured to the sclera and preamplifiers configured to minimize cable artifacts, we reexamined this issue in two rhesus monkeys. During repeated fixation trials, the eye position signal was used to adjust the stimulus position, compensating for eye movements and correcting the stimulus position to place it at the desired location on the retina. Estimates of response magnitudes and receptive field characteristics in V1 and in LGN were obtained in both compensated and uncompensated conditions. Receptive fields were narrower, with steeper borders, and response amplitudes were higher when eye movement compensation was used. In sum, compensating for eye movements facilitated more precise definition of the receptive field. We also monitored horizontal vergence over long sequences of fixation trials and found the variability to be low, as expected for this precise behavior. Our results imply that eye coil signals can be highly accurate and useful for optimizing visual physiology when rigorous precautions are observed.


2007 ◽  
Vol 98 (3) ◽  
pp. 1380-1391 ◽  
Author(s):  
Ronen Segev ◽  
Elad Schneidman ◽  
Joe Goodhouse ◽  
Michael J. Berry

The concerted action of saccades and fixational eye movements are crucial for seeing stationary objects in the visual world. We studied how these eye movements contribute to retinal coding of visual information using the archer fish as a model system. We quantified the animal's ability to distinguish among objects of different sizes and measured its eye movements. We recorded from populations of retinal ganglion cells with a multielectrode array, while presenting visual stimuli matched to the behavioral task. We found that the beginning of fixation, namely the time immediately after the saccade, provided the most visual information about object size, with fixational eye movements, which consist of tremor and drift in the archer fish, yielding only a minor contribution. A simple decoder that combined information from ≤15 ganglion cells could account for the behavior. Our results support the view that saccades impose not just difficulties for the visual system, but also an opportunity for the retina to encode high quality “snapshots” of the environment.


2018 ◽  
Author(s):  
Ricardo Kienitz ◽  
Joscha T. Schmiedt ◽  
Katharine A. Shapcott ◽  
Kleopatra Kouroupaki ◽  
Richard C. Saunders ◽  
...  

SummaryGrowing evidence suggests that distributed spatial attention may invoke theta (3-9 Hz) rhythmic sampling processes. The neuronal basis of such attentional sampling is however not fully understood. Here we show using array recordings in visual cortical area V4 of two awake macaques that presenting separate visual stimuli to the excitatory center and suppressive surround of neuronal receptive fields elicits rhythmic multi-unit activity (MUA) at 3-6 Hz. This neuronal rhythm did not depend on small fixational eye movements. In the context of a distributed spatial attention task, during which the monkeys detected a spatially and temporally uncertain target, reaction times (RT) exhibited similar rhythmic fluctuations. RTs were fast or slow depending on the target occurrence during high or low MUA, resulting in rhythmic MUA-RT cross-correlations at at theta frequencies. These findings suggest that theta-rhythmic neuronal activity arises from competitive receptive field interactions and that this rhythm may subserve attentional sampling.HighlightsCenter-surround interactions induce theta-rhythmic MUA of visual cortex neuronsThe MUA rhythm does not depend on small fixational eye movementsReaction time fluctuations lock to the neuronal rhythm under distributed attention


2010 ◽  
Vol 8 (6) ◽  
pp. 348-348
Author(s):  
M. Rucci ◽  
G. Desbordes ◽  
A. Casile

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