(C) PLOS One [1]. This unaltered content originally appeared in journals.plosone.org.
Licensed under Creative Commons Attribution (CC BY) license.
url:https://journals.plos.org/plosone/s/licenses-and-copyright

------------



Gamma oscillations in primate primary visual cortex are severely attenuated by small stimulus discontinuities

['Vinay Shirhatti', 'Centre For Neuroscience', 'Indian Institute Of Science', 'Bengaluru', 'Iisc Mathematics Initiative', 'Poojya Ravishankar', 'Supratim Ray']

Date: 2022-06

Gamma oscillations (30 to 80 Hz) have been hypothesized to play an important role in feature binding, based on the observation that continuous long bars induce stronger gamma in the visual cortex than bars with a small gap. Recently, many studies have shown that natural images, which have discontinuities in several low-level features, do not induce strong gamma oscillations, questioning their role in feature binding. However, the effect of different discontinuities on gamma has not been well studied. To address this, we recorded spikes and local field potential from 2 monkeys while they were shown gratings with discontinuities in 4 attributes: space, orientation, phase, or contrast. We found that while these discontinuities only had a modest effect on spiking activity, gamma power drastically reduced in all cases, suggesting that gamma could be a resonant phenomenon. An excitatory–inhibitory population model with stimulus-tuned recurrent inputs showed such resonant properties. Therefore, gamma could be a signature of excitation–inhibition balance, which gets disrupted due to discontinuities.

To address these questions, we recorded spikes and local field potential (LFP) from area V1 of passively fixating alert monkeys using microelectrode arrays, while they were shown sinusoidal luminance gratings with or without discontinuities that varied along one of 4 dimensions: space, orientation, phase, and contrast. Further, the magnitude of discontinuity for each dimension was parametrically varied. We compared how gamma oscillations and firing rates changed with the magnitude of such discontinuities. Finally, we built an E-I network based on Wilson–Cowan model operating in an inhibition stabilized mode [ 14 – 16 ] and added stimulus-dependent local recurrent inputs to model discontinuities. This simple model could mimic crucial aspect of our observations.

In addition, it is unclear how gamma oscillations depend on the size of the discontinuity. Recently, Hermes and colleagues [ 7 ] proposed an image-computable model of gamma oscillations, in which the amplitude of gamma depends on the variability across orientation channels. Such a model would also predict a drop in gamma amplitude due to stimulus discontinuities since they can introduce multiple orientations, thereby activating multiple orientation channels and reducing the overall variance across them. Intuitively, reduction in gamma is expected to be graded and proportional to the size of the discontinuity, although since this image-computable model is agnostic to the underlying neuronal network structure and specific network mechanisms, the reduction in gamma with the magnitude of discontinuity could be nonlinear. Other studies have suggested that gamma could be a resonant phenomenon arising due to a tight interplay of excitatory and inhibitory (E-I) signals in a neuronal network [ 8 – 12 ]. Indeed, the V1 RF structure has an excitatory center region flanked by suppressive near-surround and far-surround regions, and involves interactions between feedforward geniculocortical signals, lateral intracortical signals from horizontal connections, and feedback signals from higher areas [ 13 ]. Stimulus discontinuities could potentially modulate the interactions between these diverse neuronal subpopulations and alter the levels of E-I in this network, which may result in a drastic reduction in gamma even with a small discontinuity.

Gamma oscillations (approximately 30 to 80 Hz) are strongly induced in the primary visual cortex (area V1) by stimuli such as gratings, bars, or colors [ 1 ]. One influential hypothesis posits that gamma oscillations play a role in visual perceptual grouping or feature binding, based on the finding that continuous bars induce stronger gamma synchronization between neurons whose receptive fields (RFs) contain parts of the bar as compared to discontinuous bars, even when the discontinuity is outside their RFs [ 2 ]. However, in the case of natural images, studies have reported disparate observations regarding the consistency of gamma oscillations [ 3 – 5 ], casting doubts on a causal role for them in feature binding in a natural setting. Because such natural stimuli might occur as discontinuities along many feature dimensions across the RF of neurons, it is important to study how different types of structural irregularities affect firing responses and gamma oscillations. A recent study explored discontinuities in chromatic content and showed that stimulus discontinuities can reduce gamma synchronization between responsive neurons [ 6 ]. However, the effect of discontinuities along other feature dimensions, such as orientation, phase, and contrast, on gamma oscillations and firing rates remains largely unknown.

Results

We implanted a microelectrode array in area V1 of 2 monkeys and estimated the RFs of the recorded sites by flashing small sinusoidal luminance gratings on locations forming a dense rectangular grid on the approximate aggregate RF for all the sites ([17]; see S1 Fig and Materials and methods for details). We have previously shown that large gratings induce 2 distinct gamma oscillations in V1, termed slow (20 to 35 Hz) and fast (35 to 70 Hz) gamma [18]. Here, we presented large static gratings (radii of 9.6° and 6.4° for the 2 monkeys) at a spatial frequency of 4 cycles per degree (cpd), 100% contrast (except in the contrast discontinuities experiment), at an orientation that induced strong fast gamma oscillations (although for Monkey 2 (M2), these induced moderately strong slow gamma as well), and introduced discontinuities of different types. Therefore, the following results are focused on the fast gamma band, and “gamma” refers to this band. Unless otherwise stated, for the discontinuous gratings, the radius of the inner grating was fixed at 0.3° and 0.2° for Monkeys 1 and 2, respectively, which was close to the average RF sizes (mean ± SEM for Monkey 1 (M1): 0.28° ± 0.009°, M2: 0.176°± 0.007°). Thus, the discontinuity across experiments occurred approximately in the visual space corresponding to a transition between the center and surround. In each session, stimuli were centered approximately on the RF center of one of the recorded sites.

Effect of orientation discontinuity To evaluate the effect of orientation discontinuity, we varied the relative orientation of the inner and outer parts of the static grating stimulus (Fig 3A). Average TF difference spectra across trials of the different stimuli, for an example site from a session in M1, show that gamma oscillations were strongest for matched orientations, and their strength reduced drastically even with the smallest mismatch of 10° on both sides (by approximately 72% for a difference of ‒10° between outer and inner orientation ((O-I)°) and by approximately 69% for (O-I)° = 10°). As this orientation difference systematically increased, there was a drastic reduction in the strength of gamma power across the population in both monkeys as evidenced in the average TF spectra (Fig 3A, rows 3 and 4) and change in power (Fig 3B). As before, a slight increase in peak frequency was also observed (Fig 3B). On the other hand, spiking activity increased as the mismatch between inner and outer orientation increased (normalized firing rates, Fig 3C). This is consistent with previous studies of cross orientation suppression where lateral inhibition from the surround has been shown to be the strongest when the center and surround orientation are matched and weakens with increase in orientation differences [22,23]. PPT PowerPoint slide

PNG larger image

TIFF original image Download: Fig 3. Gamma oscillations are reduced by orientation discontinuity. (A–E) Same format as in Fig 1. For M2, there are 2 additional steps of discontinuity on either side (‒50° to 50° in steps of 10°). Figure data are located at https://doi.org/10.5281/zenodo.6523772. M1, Monkey 1; M2, Monkey 2. https://doi.org/10.1371/journal.pbio.3001666.g003 For a subset of strongly firing units, we compared the dependence on orientation discontinuity of the normalized gamma power to normalized spiking activity (Fig 3D), similar to the analysis in Fig 1D. For the smallest orientation discontinuity that we presented, normalized gamma power reduced significantly for both sides by approximately 48% (for (O-I)° = ‒10°, z-value = ‒4.90, p = 0.96 × 10‒6, WSR test) and approximately 52% (for (O-I)° = 10°, z-value = ‒4.94, p = 0.80 × 10‒6) in M1 and approximately 12% (for (O-I)° = ‒10°, z-value = ‒5.40, p = 0.67 × 10‒7) and approximately 15% (for (O-I)° = 10°, z-value = ‒6.07, p = 0.13 × 10‒8) in M2, whereas firing rates remained mostly unchanged (Fig 3D, WSR test, z-value = 1.88, p = 0.06 and z-value = 1.06, p = 0.29 for the 2 sides in M1; similarly z-value = 0.47, p = 0.64 and z-value = ‒0.78, p = 0.43 in M2). To further compare the rate of change in gamma and firing rates due to orientation discontinuity, we computed the slope of regression of their normalized values with discontinuity on both sides over the range where mean values varied clearly ((O-I)° = 0° to ±20° in M1 and (O-I)° = 0° to ±30° in M2). Across sites, the slopes were significantly negative for gamma ((z-value = ‒4.92, p = 0.88 × 10‒6) and (‒4.94, 0.80 × 10‒6) on the 2 sides in M1 and (‒6.51, 0.75 × 10‒10) and (‒6.48, 0.89 × 10‒10) in M2, WSR test) and significantly positive for firing rates ((z-value = 3.78, p = 0.16 × 10‒4) and (4.04, 0.54 × 10‒4) in M1 (4, p = 0.64 × 10‒4) and (2.82, 0.48 × 10‒2) in M2, WSR test). However, the magnitude of the mean slope (averaged across both sides) was larger for gamma than for firing rates consistently across individual sites in both the monkeys (Fig 3E, (z-value = 4.60, p = 0.42 × 10‒5) in M1 and (5.80, 0.66 × 10‒8) in M2, WSR test). As in the previous case, the mean slopes were consistently negative for gamma across all sites for both monkeys, whereas there was more heterogeneity of effects for spiking responses (S2B Fig). Interestingly, the mean firing responses changed significantly between conditions of 10° to 20° orientation differences, after which they again remained comparable for increasing orientation differences in both the monkeys (Fig 3D). Gamma, on the other hand, was sensitive to orientation differences across a larger range, and this effect was more consistent across the recorded sites.

[END]

[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001666

(C) Plos One. "Accelerating the publication of peer-reviewed science."
Licensed under Creative Commons Attribution (CC BY 4.0)
URL: https://creativecommons.org/licenses/by/4.0/


via Magical.Fish Gopher News Feeds:
gopher://magical.fish/1/feeds/news/plosone/

You are viewing proxied material from magical.fish. The copyright of proxied material belongs to its original authors. Any comments or complaints in relation to proxied material should be directed to the original authors of the content concerned. Please see the disclaimer for more details.