Gamma Oscillation Maintains Stimulus Structure-Dependent Synchronization in Cat Visual Cortex

Neuronal responses in primary visual cortex have been found to be highly variable. This has led to the widespread notion that neuronal responses have to be averaged over large numbers of neurons to obtain suitably invariant responses that can be used to reliably encode or represent external stimuli. However, it is possible that the high variability of neuronal responses may result from the use of simple, artificial stimuli and that the visual cortex may respond differently to dynamic, naturalistic images. To investigate this question, we recorded the responses of primary visual cortical neurons in the anesthetized cat under stimulation with time-varying natural movies. We found that cortical neurons on the whole exhibited a high degree of spike count variability, but a surprisingly low degree of spike time variability. The spike count variability was further reduced when all but the first spike in a burst were removed. We also found that responses exhibiting low spike time variability exhibited low spike count variability, suggesting that rate coding and temporal coding might be more compatible than previously thought. In addition, we found the spike time variability to be significantly lower when stimulated by natural movies as compared with stimulation using drifting gratings. Our results indicate that response variability in primary visual cortex is stimulus dependent and significantly lower than previous measurements have indicated.

Section: Interspike Interval Distributionssupporting

confidence: 91%

Natural Movies Evoke Spike Trains with Low Spike Time Variability in Cat Primary Visual Cortex

Herikstad¹,

Baker²,

Lachaux³

et al. 2011

“…Snider et al (1998) found that monosynaptic connections (CCGs with peaks offset from zero) between neurons in cat V1 were more sensitive to stimulus orientation than contrast. Samonds and Bonds (2004) showed that common-input CCGs are larger for effectively oriented stimuli. Llampl et al (1999) showed that membrane potential fluctuations between pairs of V1 neurons are correlated and stimulus dependent, also consistent with our data.…”

Section: Comparison With Previous Studiesmentioning

confidence: 99%

“…However, most studies investigating synchrony between single V1 cortical neurons have focused either on the effect of altering the "gestalt" characteristics of the stimulus (Livingstone, 1996) or have used indirect measurements such as the synchrony of multiunit activity (MUA) (Lamme and Spekreijse, 1998) or the strength of oscillations in single-unit activity, MUA, or the local field potential (LFP) (Gray et al, 1989; synchrony, this is because different stimuli might recruit different subpopulations of neurons in the recorded signal. For measures of oscillatory firing, this is because the stimulus dependence of oscillations is controversial (Ghose and Freeman, 1992;Young et al, 1992) and because some studies have failed to find a strong relationship between oscillatory firing and synchronous firing of single neurons (Samonds and Bonds, 2004) (but see Maldonado et al, 2000). To compare the sensitivity of spike count and spike timing correlation between single V1 neurons, we therefore investigated the orientation dependence of synchrony in our population of pairs.…”

Section: Orientation Dependence Of Spike Timing Correlationmentioning

confidence: 99%

Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque

Kohn¹,

Ma²

2005

506

584

Nearby cortical neurons often have correlated trial-to-trial response variability, and a significant fraction of their spikes occur synchronously. These two forms of correlation are both believed to arise from common synaptic input, but the origin of this input is unclear. We investigated the source of correlated responsivity by recording from pairs of single neurons in primary visual cortex of anesthetized macaque monkeys and comparing correlated variability and synchrony for spontaneous activity and activity evoked by stimuli of different orientations and contrasts. These two stimulus manipulations would be expected to have different effects on the cortical pool providing input to the recorded pair: changing stimulus orientation should recruit different populations of cells, whereas changing stimulus contrast affects primarily the relative strength of sensory drive and ongoing cortical activity. Consistent with this predicted difference, we found that correlation was affected by these stimulus manipulations in different ways. Synchrony was significantly stronger for orientations that drove both neurons well than for those that did not, but correlation on longer time scales was orientation independent. Reducing stimulus contrast resulted in a decrease in the temporal precision of synchronous firing and an enhancement of correlated response variability on longer time scales. Our results thus suggest that correlated responsivity arises from mechanisms operating at two distinct timescales: one that is orientation tuned and that determines the strength of temporally precise synchrony, and a second that is contrast sensitive, of low temporal frequency, and present in ongoing cortical activity.

“…Recordings in monkey have also shown that visual gamma oscillations are modulated by orientation (Friedman-Hill et al, 2000) and show sharper orientation tuning than lower frequency oscillations (Frien et al, 2000). Given that behavioral orientation discrimination thresholds are better than might be predicted from individual neuronal receptive fields, it has been proposed that visual gamma oscillations may also provide a mechanism for synchronizing neurons into a cooperative neural assembly that then enhances orientation discrimination performance (Samonds et al, 2004;Samonds and Bonds, 2005).…”

Section: Introductionmentioning

confidence: 99%

Orientation Discrimination Performance Is Predicted by GABA Concentration and Gamma Oscillation Frequency in Human Primary Visual Cortex

Edden¹,

Muthukumaraswamy²,

Freeman³

et al. 2009

317

306

Neuronal orientation selectivity has been shown in animal models to require corticocortical network cooperation and to be dependent on the presence of GABAergic inhibition. However, it is not known whether variability in these fundamental neurophysiological parameters leads to variability in behavioral performance. Here, using a combination of magnetic resonance spectroscopy, magnetoencephalography, and visual psychophysics, we show that individual performance on a visual orientation discrimination task is correlated with both the resting concentration of GABA and the frequency of stimulus-induced gamma oscillations in human visual cortex. Behaviorally, a strong oblique effect was found, with the mean angular threshold for oblique discrimination being five times higher than that for vertically oriented stimuli. Similarly, we found an oblique effect for the dependency of performance on neurophysiological parameters. Orientation detection thresholds were significantly negatively correlated with visual cortex GABA concentration for obliquely oriented patterns (r ϭ Ϫ0.65, p Ͻ 0.015) but did not reach significance for vertically oriented stimuli (r ϭ Ϫ0.39, p ϭ 0.2). Similarly, thresholds for obliquely oriented stimuli were negatively correlated with gamma oscillation frequency (r ϭ Ϫ0.65, p Ͻ 0.017), but thresholds for vertical orientations were not (r ϭ Ϫ0.02, p ϭ 0.9). Gamma oscillation frequency was positively correlated with GABA concentration in primary visual cortex (r ϭ 0.67, p Ͻ 0.013). These results confirm the importance of GABAergic inhibition in orientation selectivity and demonstrate, for the first time, that interindividual performance on a simple visual task is linked to neurotransmitter concentration. The results also suggest a key role for GABAergic gamma oscillations in visual discrimination tasks.