Ординатура / Офтальмология / Английские материалы / Binocular Rivalry_Alais, Blake_2005

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neurons in areas TEO and V4, and those areas in turn receive their input from V2 and V1. Recordings in V4 revealed that only about half the neurons modulate their firing rates according to the perceptual selection of the monkey (Leopold and Logothetis, 1996). Surprisingly, only about half of those modulating neurons show a positive correlation between their firing-rate modulation and the perceptual selection. Firing rates in the other half are negatively correlated with perception (i.e., neurons respond during rivalry as if only the nonperceived stimulus were present). Finally, in area V1, only a minority of neurons show firing rate modulations with perceptual alternations, and again those can be of either sign (Leopold and Logothetis, 1996).

How, then, do neurons in V1 and V4 that represent the perceived stimulus control IT neurons despite the fact that they do not change their firing rates in a consistent way? One possibility is that the population of V1 and V4 neurons representing the perceived stimulus increases its impact through enhanced synchronization (Salinas and Sejnowski, 2001). Precise synchronization has been shown, both in vitro and in vivo, to enhance the impact of a given number of input spikes (Alonso, Usrey, and Reid, 1996; Azouz and Gray, 2000; Salinas and Sejnowski, 2000).

The Strabismic Animal as a Model for Stimulus Selection

We tested the hypothesis that perceptual selection is achieved through synchronization in primary visual cortex of awake, behaving strabismic cats. Strabismus essentially establishes permanent interocular rivalry. As during nonstrabismic rivalry, the input to the two eyes cannot be fused and the input from one of the two eyes is selected for perception. The strabismic cat model offers several advantages:

1.Most cells in early visual cortex are monocular (Hubel and Wiesel, 1965), permitting unambiguous association with the respective eye’s stimulus.

2.Strabismic subjects always experience interocular rivalry (rivalry between the eyes) and not figural rivalry (rivalry between two stimuli, parts of which can be distributed in different eyes). They experience rivalry even when both retinas receive congruent stimulation (Holopigian, Blake, and Greenwald, 1988).

3.In strabismic subjects, one eye often develops perceptual dominance (Enoksson, 1968; Von Noorden, 1990). The dominant eye stimulus benefits from a permanent competitive advantage and suppresses the

nondominant eye stimulus. This can be exploited in the present context. Eye dominance can be determined once and then used to predict the outcome of stimulus competition when stimulus selection is not directly assessed (Fries et al., 1997; Fries, Schröder, et al., 2001; Fries et al., 2002).

For these reasons, we examined neuronal correlates of stimulus selection in adult cats that had been made strabismic at 3 weeks of age. We first dichoptically presented gratings moving in opposite directions in the two eyes of the cats (temporonasally for each eye). During 60-second periods of such stimulation, the cats typically developed optokinetic nystagmus (OKN). During rivalry, OKN direction is strongly and reliably correlated with the perceived stimulus (Fox, Todd, and Bettinger, 1975; Logothetis and Schall, 1990). Monocular stimulation always resulted in OKN driven by that stimulus, while dichoptic stimulation with equal contrast for both eyes typically resulted in almost permanent selection of the dominant eye. After determining for each animal which eye was dominant, we implanted the primary visual cortex with up to 34 electrodes. Since the electrodes were implanted on the basis of gross cortical anatomy but without knowledge of the stimulus and ocular selectivities at each site, the first recordings were used to assess each site’s preferences for eye and orientation.

As expected in strabismic animals, most sites were monocularly driven by only one of the two eyes (Hubel and Wiesel, 1965). For subsequent recording sessions, we selected groups of eight electrodes (the number of available amplifiers) that preferred stimulation of the same eye and that could be coactivated by a grating of one orientation. To test the effects of perceptual selection during rivalry, we used two stimuli. One was in the preferred eye and of the preferred orientation for the recorded neurons, and was called the “activating stimulus.” The other was in the nonpreferred eye and orthogonal to the activating stimulus, and was called the “nonactivating stimulus.” Those stimuli were then presented monocularly or dichoptically in randomly interleaved trials while neuronal activity was recorded. The movement direction of the gratings was reversed every 1.5 sec, which was sufficient to avoid eye movements entirely (Fries et al., 2002). The activating and the nonactivating stimuli were turned on either simultaneously or with a relative temporal offset of 3 sec (corresponding to one cycle of the movement direction).

This design allowed us to analyze the effect of stimulus selection or suppression in several different ways. The different paradigms and the results obtained with them are described in the following sections.

Selection of an Activating Stimulus in the Dominant Eye

We recorded from neurons activated by the dominant eye and compared monocular stimulation of the dominant eye with dichoptic stimulation. Under both conditions, the stimulus in the dominant eye was the activating stimulus and the one that was perceived. Only when a competing, nonactivating stimulus was presented to the nondominant eye was there active selection of the activating stimulus in the dominant eye. Otherwise, the latter stimulus was the only one present. In figure 14.1, panels A and B show firing rates of primary visual cortex neurons obtained with this paradigm. Panel A shows the firing rate at a recording site in primary visual cortex when an optimally oriented grating stimulus is presented to the dominant eye. The response is strong and sustained throughout the stimulation period. Panel C (3–6 sec) shows the response of the same site when the nondominant eye is presented with an orthogonal but otherwise identical stimulus. There is only a short response to stimulus onset and only a slight elevation of the sustained firing rate. Panel B shows the response when both stimuli are presented simultaneously. During this rivalry condition, the stimulus in the dominant eye, which is the main activating stimulus, has to be selected actively. Despite active stimulus selection, the firing rate stays unchanged relative to monocular stimulation of the dominant eye.

Figure 14.2, panels A and B, shows an analysis of oscillatory neuronal synchronization in the same data set. Panel A shows spike-triggered averages (STAs) of local field potentials (LFPs) for the monocular (gray) and the rivalry (black) conditions. STAs were computed by averaging local field potential traces at 128 msec around the time of occurrence of spikes. Spikes and LFPs were taken from two electrodes separated by several millimeters but both activated by the stimulus in the dominant eye. The negative LFP deflection peaking just before the spike (time 0) indicates synchronization between neuronal activities at both sites, because LFP negativities reflect neuronal activation. The strong oscillatory modulation of the STAs indicates that synchronization occurs between oscillating neuronal activities. When the activating stimulus is selected during rivalry, oscillatory neuronal synchronization is strongly enhanced. The frequency and strength of oscillatory neuronal synchronization can best be studied

Figure 14.1 Examples of firing rate histograms under monocular and rivalry stimulation conditions. Further explanation is in the text.

Figure 14.2 (A) and (B) show an example of stimulus-selection-related enhancement of gamma-frequency synchronization among neurons activated by the dominant eye. (C) and (D) show an example of stimulus-suppression-related reduction in gamma-frequency synchronization among neurons activated by the nondominant eye.

by calculating spike-field coherence (SFC) spectra, as shown in panel B. The SFC spectra are the power spectra of the STAs normalized to the average power of the LFP traces used to compile the STAs. SFCs thus reflect synchronization between spikes and LFPs independent of eventual changes in firing rate or spectral content of the LFP. The SFCs show a pronounced peak between 40 and 70 Hz (in the gamma-frequency range, which is strongly enhanced by active stimulus selection).

Suppression of an Activating Stimulus in the Nondominant Eye

We also recorded from neurons activated by the nondominant eye and compared monocular stimulation of that eye with dichoptic stimulation. In this comparison, for both conditions, the stimulus in the nondominant eye was the activating stimulus. This activating stimulus was perceived under monocular stimulation but was perceptually suppressed when there was a competing nonactivating stimulus in the dominant eye. Figure 14.1, panels E and F, shows the respective firing rates of a site in primary visual cortex. Panel E shows stimulation of the nondominant eye with the optimally oriented grating, leading to a very strong response. The response indicates a slight direction selectivity of the recording site, because movement direction reversals occuring every 1.5 sec modulate the firing rate. Monocular stimulation of the dominant eye with an orthogonal grating, as shown in panel G (3–6 sec), is ineffective in activating this site. When both stimuli are combined to instigate rivalry, the activating stimulus in the nondominant eye is perceptually suppressed. Nevertheless, as shown in panel F, firing rates remain virtually unchanged. In contrast, oscillatory neuronal synchronization is strongly affected. Figure 14.2, panels C and D, shows the STAs and SFCs for the same data set from neurons activated by the nondominant eye. Panel D shows that perceptual suppression of the activating stimulus during rivalry leads to a profound reduction in gamma-frequency synchronization.

While these results establish that gamma-frequency synchronization is a correlate of the selection of an activating stimulus presented to the dominant eye of a strabismic animal, it might be argued that this is a special case and that the situation might be different when selection is due to factors other than strabismic eye dominance. For this reason, we manipulated the relative dominance of the two stimuli by manipulating their relative contrasts or onset timings.

Selection of a Newly Appearing Stimulus

When a stimulus is introduced into one eye against a stimulus that has already been presented to the other eye for some seconds, the newly appearing stimulus is reliably perceptually selected. This is known as flash suppression (Wolfe, 1984; Sheinberg and Logothetis, 1997; see chapters 11 and 12 in this volume). Thus, we could analyze the first 1.5-sec period after

the introduction of an activating stimulus against a nonactivating stimulus that had already been presented to the other eye for 3 sec. This was compared against the first 1.5 sec after simultaneous presentation of activating and nonactivating stimuli in normal rivalry trials. Since this paradigm is explicitly independent of stimulus selection due to strabismic eye dominance, data from neurons activated by either eye can be treated alike. For neurons activated by the dominant eye, figure 14.1, panels B and C, shows the respective firing rates. For neurons activated by the nondominant eye, firing rates are shown in figure 14.1, panels F and G. Overall, the selection of the newly appearing activating stimulus resulted in a slight reduction of firing rates relative to the condition with simultaneous stimulus onsets. By contrast, neuronal gamma-frequency synchronization was enhanced when the activating stimulus was selected. This is demonstrated in figure 14.3, panels A and B.

Suppression by a Newly Appearing Stimulus

When a stimulus is introduced to one eye against a preexisting stimulus in the other eye, and therefore selected, the previous stimulus is suppressed. Thus, we can analyze perceptual suppression of an activating stimulus by a temporally delayed nonactivating stimulus and compare the results against normal rivalry trials with simultaneous stimulus onset. Firing rates for those conditions are shown in figures 14.1B and 14.1D for neurons activated by the dominant eye and in figure 14.1F and 14.1H for neurons activated by the nondominant eye. The suppression of an activating stimulus due to the introduction of a novel, nonactivating stimulus led to a slight increase in firing rates. By contrast, gamma-frequency synchronization was reduced when the activating stimulus was suppressed (figures 14.3C and 14.3D).

An earlier study on interocular competition used a very similar stimulation paradigm (Sengpiel and Blakemore, 1994; and see chapter 11 in this volume), but observed firing rate reductions. The animals in Sengpiel’s study were anesthetized and paralyzed, and not examined behaviorally before the experiments. We repeated our measurements under general anesthesia in two of our animals with implanted electrodes, and recorded from the same electrodes as in the awake condition. The effects were very similar to those described by Sengpiel, suggesting anesthesia as the main reason for the discrepancy.