Natural Movies Evoke Spike Trains with Low Spike Time Variability in Cat Primary Visual Cortex (original) (raw)

Responses of primary visual cortical neurons to natural movies in anesthetized cat

BMC Neuroscience, 2008

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Phase-of-firing coding of natural visual stimuli in primary visual cortex

We investigated the hypothesis that neurons encode rich naturalistic stimuli in terms of their spike times relative to the phase of ongoing network fluctuations rather than only in terms of their spike count. We recorded local field potentials (LFPs) and multiunit spikes from the primary visual cortex of anaesthetized macaques while binocularly presenting a color movie. We found that both the spike counts and the low-frequency LFP phase were reliably modulated by the movie and thus conveyed information about it. Moreover, movie periods eliciting higher firing rates also elicited a higher reliability of LFP phase across trials. To establish whether the LFP phase at which spikes were emitted conveyed visual information that could not be extracted by spike rates alone, we compared the Shannon information about the movie carried by spike counts to that carried by the phase of firing. We found that at low LFP frequencies, the phase of firing conveyed 54% additional information beyond that conveyed by spike counts. The extra information available in the phase of firing was crucial for the disambiguation between stimuli eliciting high spike rates of similar magnitude.

Responses of neurons in primary and inferior temporal visual cortices to natural scenes

Proceedings of the Royal Society B: Biological Sciences, 1997

The primary visual cortex (V1) is the ¢rst cortical area to receive visual input, and inferior temporal (IT) areas are among the last along the ventral visual pathway. We recorded, in area V1 of anaesthetized cats and area ITof awake macaque monkeys, responses of neurons to videos of natural scenes. Responses were analysed to test various hypotheses concerning the nature of neural coding in these two regions. A variety of spike-train statistics were measured including spike-count distributions, interspike interval distributions, coe¤cients of variation, power spectra, Fano factors and di¡erent sparseness measures. All statistics showed non-Poisson characteristics and several revealed self-similarity of the spike trains. Spike-count distributions were approximately exponential in both visual areas for eight di¡erent videos and for counting windows ranging from 50 ms to 5 seconds. The results suggest that the neurons maximize their information carrying capacity while maintaining a ¢xed long-term-average ¢ring rate, or equivalently, minimize their average ¢ring rate for a ¢xed information carrying capacity.

Responses to Natural Scenes in Cat V1

Journal of Neurophysiology, 2003

Studies on processing in primary visual areas often use artificial stimuli such as bars or gratings. As a result, little is known about the properties of activity patterns for the natural stimuli processed by the visual system on a daily basis. Furthermore, in the cat, a well-studied model system for visual processing, most results are obtained from anesthetized subjects and little is known about neuronal activations in the alert animal. Addressing these issues, we measure local field potentials (lfp) and multiunit spikes in the primary visual cortex of awake cats. We compare changes in the lfp power spectra and multiunit firing rates for natural movies, movies with modified spatio-temporal correlations as well as gratings. The activity patterns elicited by drifting gratings are qualitatively and quantitatively different from those elicited by natural stimuli and this difference arises from both spatial as well as temporal properties of the stimuli. Furthermore, both local field potentials and multiunit firing rates are most sensitive to the second-order statistics of the stimuli and not to their higher-order properties. Finally, responses to natural movies show a large variability over time because of activity fluctuations induced by rapid stimulus motion. We show that these fluctuations are not dependent on the detailed spatial properties of the stimuli but depend on their temporal jitter. These fluctuations are important characteristics of visual activity under natural conditions and impose limitations on the readout of possible differences in mean activity levels.

Stimulus-dependent oscillations in the cat visual cortex: differences between bar and grating stimuli

Brain Research, 1996

We have investigated the dependence of cortical oscillations on the type of visual stimulus. Single unit recordings were performed in areas 17 and 18 of the cat visual cortex. Among 217 cortical neurons oscillations in the frequency range of 22-102 Hz were found in 29 cells (13%). The proportion of oscillating cells was higher (16%) if both bar and grating stimuli were used to stimulate cortical neurons. It was found that gratings are more effective than bars in triggering oscillatory patterns in cortical cells. Among 21 oscillating cells which were stimulated with both bar and grating stimuli, oscillations evoked with gratings were found in 17 neurons (81%) while oscillations evoked with bar stimuli were triggered in 7 cells (33%). The distributions of oscillation frequencies were statistically different for oscillations evoked with bars and gratings. Frequencies of oscillations evoked with bars were in the lower and higher range than frequencies of oscillations evoked with gratings. In 3 cells (14%), rhythmic patterns could be evoked with both bar and grating stimuli. However, the oscillations were of different frequencies. No significant correlation was found between the strength of oscillations and firing rate of cortical neurons. Both simple and complex cells manifested the same dependence on stimulus type. However, complex cells mostly exhibited oscillations in the lower frequency range while simple cells did so when neurons were stimulated with bars. The results suggest that various classes of visual stimuli can be coded by a temporal pattern of cortical responses.

Heterogeneity in the Responses of Adjacent Neurons to Natural Stimuli in Cat Striate Cortex

Journal of Neurophysiology, 2006

Yen S-C, Baker J, Gray CM. Heterogeneity in the responses of adjacent neurons to natural stimuli in cat striate cortex. . When presented with simple stimuli like bars and gratings, adjacent neurons in striate cortex exhibit shared selectivity for multiple stimulus dimensions, such as orientation, direction, and spatial frequency. This has led to the idea that local averaging of neuronal responses provides a more reliable representation of stimulus properties. However, when stimulated with complex, time-varying natural scenes (i.e., movies), striate neurons exhibit highly sparse responses. This raises the question of how much response heterogeneity the local population exhibits when stimulated with movies, and how it varies with separation distance between cells. We investigated this question by simultaneously recording the responses of groups of neurons in cat striate cortex to the repeated presentation of movies using silicon probes in a multi-tetrode configuration. We found, first, that the responses of striate neurons to movies are brief (tens of milliseconds), decorrelated, and exhibit high population sparseness. Second, we found that adjacent neurons differed significantly in their peak firing rates even when they responded to the same frames of a movie. Third, pairs of adjacent neurons recorded on the same tetrodes exhibited as much heterogeneity in their responses as pairs recorded by different tetrodes. These findings demonstrate that complex natural scenes evoke highly heterogeneous responses within local populations, suggesting that response redundancy in a cortical column is substantially lower than previously thought.

to Natural Stimuli in Cat Striate Cortex Heterogeneity in the Responses of Adjacent Neurons

Yen S-C, Baker J, Gray CM. Heterogeneity in the responses of adjacent neurons to natural stimuli in cat striate cortex. . When presented with simple stimuli like bars and gratings, adjacent neurons in striate cortex exhibit shared selectivity for multiple stimulus dimensions, such as orientation, direction, and spatial frequency. This has led to the idea that local averaging of neuronal responses provides a more reliable representation of stimulus properties. However, when stimulated with complex, time-varying natural scenes (i.e., movies), striate neurons exhibit highly sparse responses. This raises the question of how much response heterogeneity the local population exhibits when stimulated with movies, and how it varies with separation distance between cells. We investigated this question by simultaneously recording the responses of groups of neurons in cat striate cortex to the repeated presentation of movies using silicon probes in a multi-tetrode configuration. We found, first, that the responses of striate neurons to movies are brief (tens of milliseconds), decorrelated, and exhibit high population sparseness. Second, we found that adjacent neurons differed significantly in their peak firing rates even when they responded to the same frames of a movie. Third, pairs of adjacent neurons recorded on the same tetrodes exhibited as much heterogeneity in their responses as pairs recorded by different tetrodes. These findings demonstrate that complex natural scenes evoke highly heterogeneous responses within local populations, suggesting that response redundancy in a cortical column is substantially lower than previously thought.

Functional Heterogeneity in Neighboring Neurons of Cat Primary Visual Cortex in Response to Both Artificial and Natural Stimuli

Journal of Neuroscience, 2013

Neurons in primary visual cortex of many mammals are clustered according to their preference to stimulus parameters such as orientation and spatial frequency. Nevertheless, responses to complex visual stimuli are highly heterogeneous between adjacent neurons. To investigate the relation between these observations, we recorded from pairs of neighboring neurons in area 17 of anesthetized cats in response to stimuli of differing complexity: sinusoidal drifting gratings, binary dense noise, and natural movies. Comparisons of the tuning curves revealed similar orientation and direction preferences for neighboring neurons, but large differences in preferred phase, direction selectivity, and tuning width of spatial frequency. No pair was similar across all tuning properties. The neurons' firing rates averaged across multiple stimulus repetitions (the "signal") were also compared. Binned between 10 and 200 ms, the correlation between these signals was close to zero in the median across all pairs for all stimulus classes. Signal correlations agreed poorly with differences in tuning properties, except for receptive field offset and relative modulation (i.e., the strength of phase modulation). Nonetheless, signal correlations for different stimulus classes were well correlated with each other, even for gratings and movies. Conversely, trial-to-trial fluctuations (termed "noise") were poorly correlated between neighboring neurons, suggesting low degrees of common input. In response to gratings and visual noise, signal and noise correlations were well correlated with each other, but less so for responses to movies. These findings have relevance for our understanding of the processing of natural stimuli in a functionally heterogeneous cortical network.

Entrainment to video displays in primary visual cortex of macaque and humans

The Journal of neuroscience : the official journal of the Society for Neuroscience, 2004

Cathode ray tubes (CRTs) display images refreshed at high frequency, and the temporal waveform of each pixel is a luminance impulse only a few milliseconds long. Although humans are perceptually oblivious to this flicker, we show in V1 in macaque monkeys and in humans that extracellularly recorded action potentials (spikes) and visual-evoked potentials (VEPs) align with the video impulses, particularly when high-contrast stimuli are viewed. Of 91 single units analyzed in macaque with a 60 Hz video refresh, 29 cells (32%) significantly locked their firing to a uniform luminance display, but their number increased to 75 (82%) when high-contrast stimuli were shown. Of 92 cells exposed to a 100 Hz refresh, 21 (23%) significantly phase locked to high-contrast stimuli. Phase locking occurred in both input and output layers of V1 for simple and complex cells, regardless of preferred temporal frequency. VEPs recorded in humans showed significant phase locking to the video refresh in all sev...

Feedforward Excitation and Inhibition Evoke Dual Modes of Firing in the Cat's Visual Thalamus during Naturalistic Viewing

Neuron, 2007

Thalamic relay cells transmit information from retina to cortex by firing either rapid bursts or tonic trains of spikes. Bursts occur when the membrane voltage is low, as during sleep, because they depend on channels that cannot respond to excitatory input unless they are primed by strong hyperpolarization. Cells fire tonically when depolarized, as during waking. Thus, mode of firing is usually associated with behavioral state. Growing evidence, however, suggests that sensory processing involves both burst and tonic spikes. To ask if visually evoked synaptic responses induce each type of firing, we recorded intracellular responses to natural movies from relay cells and developed methods to map the receptive fields of the excitation and inhibition that the images evoked. In addition to tonic spikes, the movies routinely elicited lasting inhibition from the center of the receptive field that permitted bursts to fire. Therefore, naturally evoked patterns of synaptic input engage dual modes of firing.