Gamma-band synchronization in visual cortex predicts speed of change detection

Womelsdorf, Thilo; Fries, Pascal; Mitra, Partha P.; Desimone, Robert

doi:10.1038/nature04258

Cited by 690 publications

(668 citation statements)

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“…Our finding of reduced noise correlation around the mean gamma phase and with generally enhanced gamma power is consistent with several recent studies relating either gammaband synchronization or noise correlation to attention. When attention is directed to a behaviorally relevant stimulus, neurons in area V4 that are driven by this stimulus show enhanced gamma-band synchronization (7,8,10,19,44,(45)(46)(47). We demonstrate here that enhanced gamma-band synchronization co-occurs with reduced noise correlation.…”

Section: Discussionmentioning

confidence: 70%

Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle

Womelsdorf

Lima²,

Vinck³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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115

120

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Gamma-band synchronization adjusts the timing of excitatory and inhibitory inputs to a neuron. Neurons in the visual cortex are selective for stimulus orientation because of dynamic interactions between excitatory and inhibitory inputs. We hypothesized that these interactions and hence also orientation selectivity vary during the gamma cycle. We determined for each spike its phase relative to the gamma cycle. As a function of gamma phase, we then determined spike rates and their orientation selectivity. Orientation selectivity was modulated by gamma phase. The firing rate of spiking activity that occurred close to a neuron's mean gamma phase of firing was most orientation selective. This stimulus-selective signal could best be conveyed to postsynaptic neurons if it were not corrupted by noise correlations. Noise correlations between firing rates were modulated by gamma phase such that they were not statistically detectable for the spiking activity occurring close to a neuron's mean gamma phase of firing. Thus, gamma-band synchronization produces spiking activity that carries maximal stimulus selectivity and minimal noise correlation in its firing rate, and at the same time synchronizes this spiking activity for maximal impact on postsynaptic targets. oscillation | primary visual cortex | neuronal coding | neuronal tuning | information theory R hythmic neuronal synchronization has been described in numerous brain systems, species, and under many different conditions. A prominent proposal is that rhythmically synchronized spikes have an enhanced impact on target neurons. This consequence of synchronization might stem from direct feedforward triggering of coincidence detection mechanisms, from the entrainment of target neurons, or from both mechanisms in conjunction (1-4). This proposal has been detailed in several computational studies (5, 6) and has received substantial experimental support (7-11).Here, we ask a complementary, yet central question: Does the rhythmically synchronized spiking activity, besides its enhanced impact, also carry an enhanced representation of, e.g., a sensory stimulus in its firing rate? One of the best-studied cases of neuronal stimulus selectivity is the orientation selectivity of neurons in primary visual cortex. We recorded from several sites in awake monkey primary visual cortex while it was stimulated with patches of drifting grating that varied in orientation. Those stimuli induced strong gamma-band synchronization. We sorted spikes based on the phase in the gamma cycle at which they occurred, and we tested whether orientation selectivity varied as a function of phase in the gamma cycle.Stimulus-selective neuronal responses signal a stimulus to postsynaptic target neurons most effectively when they are not corrupted by so-called correlated noise. The term "noise" is often used to denote variance in neuronal activity that is not explained by variance in the sensory stimulus. This so-called noise might well be fully determined, just by brain processes that are not determined by the...

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Section: Discussionmentioning

confidence: 70%

Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle

Womelsdorf

Lima²,

Vinck³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

115

120

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“…Experimental studies in visual cortex (Treue and Maunsell 1996;Luck et al 1997;Reynolds et al 1999;Reynolds and Desimone 2003) have shown that the output of a neuron may reflect either input, depending on whether attention is directed to one or the other stimulus. This biasing of competition in favour of the attended stimulus is correlated with the appearance of enhanced gamma band (30-80 Hz) synchronization (Fries et al 2001(Fries et al , 2007Fries 2009;Gruber et al 1999;Taylor et al 2005;Womelsdorf et al 2005). This observation suggests that the responses of a neuron to multiple input signals not only depend on the properties of the neuron, but also on the neuronal encoding of information in oscillatory, synchronized firing of the spike input.…”

Section: Introductionmentioning

confidence: 95%

“…Recordings of EEG and MEG (see, e.g. Schoffelen et al 2005) and local field potentials (see Womelsdorf et al 2005) have shown that a realistic gamma signal has a band-pass frequency spectrum and look very similar to band-pass filtered Gaussian White noise (see Womelsdorf et al 2005, Fig. 1).…”

Section: Introductionmentioning

confidence: 99%

Gamma oscillations as a mechanism for selective information transmission

2010

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In the past decades, many studies have focussed on the relation between the input and output of neurons with the aim to understand information processing by neurons. A particular aspect of neuronal information, which has not received much attention so far, concerns the problem of information transfer when a neuron or a population of neurons receives input from two or more (populations of) neurons, in particular when these (populations of) neurons carry different types of information. The aim of the present study is to investigate the responses of neurons to multiple inputs modulated in the gamma frequency range. By a combination of theoretical approaches and computer simulations, we test the hypothesis that enhanced modulation of synchronized excitatory neuronal activity in the gamma frequency range provides an advantage over a less synchronized input for various types of neurons. The results of this study show that the spike output of various types of neurons [i.e. the leaky integrate and fire neuron, the quadratic integrate and fire neuron and the Hodgkin-Huxley (HH) neuron] and that of excitatory-inhibitory coupled pairs of neurons, like the Pyramidal Interneuronal Network Gamma (PING) model, is highly phase-locked to the larger of two gamma-modulated input signals. This implies that the neuron selectively responds to the input with the larger gamma modulation if the amplitude of the gamma modulation exceeds that of the other signals by a certain amount. In that case, the output of the neuron is entrained by one of multiple inputs and that other inputs are not represented in the output. This mechanism for selective information transmission is enhanced for short membrane time constants of the neuron.

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“…For instance, gamma-band synchronization among neurons in the visual cortex predicts the speed of change detection [55] ; the temporal structure of neuronal activity in macaque parietal cortex during a working memory task predicts the time of a planned movement [56] ; anticipatory activity in primate motor cortex codes memorized movement sequences [57] ; anticipatory rate changes in rat mPFC neurons predict different rewards in special working memory; and nucleus accumbens neurons in rats encode predicted and ongoing reward costs [38] . our data showed that mPFC cells exhibited anticipatory activity in correct trials of the working memory task, but 701 not in incorrect trials.…”

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confidence: 99%

Anticipatory activity in rat medial prefrontal cortex during a working memory task

Bai

Liu

et al. 2012

Neurosci. Bull.

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Objective Working memory is a key cognitive function in which the prefrontal cortex plays a crucial role.This study aimed to show the firing patterns of a neuronal population in the prefrontal cortex of the rat in a working memory task and to explore how a neuronal ensemble encodes a working memory event. Methods Sprague-Dawley rats were trained in a Y-maze until they reached an 80% correct rate in a working memory task. Then a 16-channel microelectrode array was implanted in the prefrontal cortex. After recovery, neuronal population activity was recorded during the task, using the Cerebus data-acquisition system. Spatio-temporal trains of action potentials were obtained from the original neuronal population signals. Results During the Y-maze working memory task, some neurons showed significantly increased firing rates and evident neuronal ensemble activity. Moreover, the anticipatory activity was associated with the delayed alternate choice of the upcoming movement. In correct trials, the averaged pre-event firing rate (10.86 ± 1.82 spikes/ bin) was higher than the post-event rate (8.17 ± 1.15 spikes/bin) (P <0.05). However, in incorrect trials, the rates did not differ. Conclusion The results indicate that the anticipatory activity of a neuronal ensemble in the prefrontal cortex may play a role in encoding working memory events.

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Gamma-band synchronization in visual cortex predicts speed of change detection

Cited by 690 publications

References 27 publications

Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle

Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle

Gamma oscillations as a mechanism for selective information transmission

Anticipatory activity in rat medial prefrontal cortex during a working memory task

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