The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization

Vinck, Martin; Wingerden, Marijn van; Womelsdorf, Thilo; Fries, Pascal; Pennartz, Cyriel M. A.

doi:10.1016/j.neuroimage.2010.01.073

Cited by 427 publications

(511 citation statements)

References 25 publications

(26 reference statements)

Supporting

Mentioning

498

Contrasting

Order By: Relevance

“…We focused on the sustained period because it allows the assumption that the data are approximately stationary, and because stimuli that are stationary or smoothly moving occupy most of natural viewing time, whereas sudden stimulus onsets are rare. During the sustained period (0.25 s after stimulus onset until end of trial), we quantified spike-field locking with a metric that is not biased by the number of spikes-namely, the pairwise phase consistency (PPC) (16). Spikes were, on average, phase locked to LFP oscillations in the gamma-frequency band (Fig.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

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

117

120

View full text Add to dashboard Cite

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...

show abstract

Section: Resultsmentioning

confidence: 99%

“…Spike-LFP phase was determined by fast Fourier transforming a Hanning-tapered LFP segment around each spike. The consistency of spike-LFP phases was quantified using the PPC (16). We quantified orientation selectivity as the OSI by considering the neuronal response variation across all orientations by calculating [1 − circular variance].…”

Section: Methodsmentioning

confidence: 99%

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

117

120

View full text Add to dashboard Cite

show abstract

“…This therefore provides an appropriate point of reference to evaluate coherence estimates in experimental multivariate time series compared with the null hypothesis of random multivariate (1/f ) noise (Achard et al, 2008), while controlling for any possible estimation bias attributable to autocorrelation or amplitude changes in the observed time series. An alternative approach to the same statistical issues has been to construct an innovative estimator of pairwise phase consistency (Vinck et al, 2010) that is an analytically unbiased and consistent estimator of population parameters of oscillations, but does not address the problem of amplitude-related bias.…”

Section: Methodsmentioning

confidence: 99%

Cognitive Effort Drives Workspace Configuration of Human Brain Functional Networks

et al. 2011

View full text Add to dashboard Cite

Effortful cognitive performance is theoretically expected to depend on the formation of a global neuronal workspace. We tested specific predictions of workspace theory, using graph theoretical measures of network topology and physical distance of synchronization, in magnetoencephalographic data recorded from healthy adult volunteers (N ϭ 13) during performance of a working memory task at several levels of difficulty. We found that greater cognitive effort caused emergence of a more globally efficient, less clustered, and less modular network configuration, with more long-distance synchronization between brain regions. This pattern of task-related workspace configuration was more salient in the ␤-band (16 -32 Hz) and ␥-band (32-63 Hz) networks, compared with both lower (␣-band; 8 -16 Hz) and higher (high ␥-band; 63-125 Hz) frequency intervals. Workspace configuration of ␤-band networks was also greater in faster performing participants (with correct response latency less than the sample median) compared with slower performing participants. Processes of workspace formation and relaxation in relation to time-varying demands for cognitive effort could be visualized occurring in the course of task trials lasting Ͻ2 s. These experimental results provide support for workspace theory in terms of complex network metrics and directly demonstrate how cognitive effort breaks modularity to make human brain functional networks transiently adopt a more efficient but less economical configuration.

show abstract

“…3D by the pairwise phase consistency (PPC) between MUA (recorded on one electrode) and the LFP (combined across the other electrodes). The PPC is a recently introduced synchronization metric (18,19) that avoids any bias by trial number, spike number, or spike rate (details are provided in Methods). To avoid strong nonstationarities, the first 0.3 s after stimulus onset was excluded.…”

Section: Stimulus Repetition Leads To Increasing Mua-lfp Synchronizatmentioning

confidence: 99%

Stimulus repetition modulates gamma-band synchronization in primate visual cortex

Brunet

Bosman

Vinck

et al. 2014

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

Self Cite

123

133

View full text Add to dashboard Cite

When a sensory stimulus repeats, neuronal firing rate and functional MRI blood oxygen level-dependent responses typically decline, yet perception and behavioral performance either stay constant or improve. An additional aspect of neuronal activity is neuronal synchronization, which can enhance the impact of neurons onto their postsynaptic targets independent of neuronal firing rates. We show that stimulus repetition leads to profound changes of neuronal gamma-band (∼40-90 Hz) synchronization. Electrocorticographic recordings in two awake macaque monkeys demonstrated that repeated presentations of a visual grating stimulus resulted in a steady increase of visually induced gamma-band activity in area V1, gamma-band synchronization between areas V1 and V4, and gamma-band activity in area V4. Microelectrode recordings in area V4 of two additional monkeys under the same stimulation conditions allowed a direct comparison of firing rates and gamma-band synchronization strengths for multiunit activity (MUA), as well as for isolated single units, sorted into putative pyramidal cells and putative interneurons. MUA and putative interneurons showed repetition-related decreases in firing rate, yet increases in gamma-band synchronization. Putative pyramidal cells showed no repetition-related firing rate change, but a decrease in gamma-band synchronization for weakly stimulus-driven units and constant gamma-band synchronization for strongly driven units. We propose that the repetition-related changes in gamma-band synchronization maintain the interareal stimulus signaling and sharpen the stimulus representation by gamma-synchronized pyramidal cell spikes.adaptation | learning | oscillation | plasticity | priming S timulus repetition typically leads to reduced neuronal firing rates and reduced functional MRI blood oxygen leveldependent signals, whereas behavior that is based on stimulus processing is not affected or is enhanced (1). Different models have been proposed to reconcile these behavioral and neurophysiological findings (1). In a "fatigue model," neuronal responses are reduced in proportion to their amplitude, leaving relative response patterns unchanged; in a "sharpening model," neurons that code features irrelevant to identification of a stimulus exhibit repetition suppression, leading to a sparser and sharpened representation of the repeated stimulus; and in a "facilitation model," stimulus repetition leads to faster stimulus processing, and thereby smaller overall neuronal activity. Gotts and coworkers (2-4) suggested a "synchronization model" in which stimulus repetition leads to reduced firing rates accompanied by increased synchronization. The increased synchronization might explain how less-activated neuronal groups can maintain their impact onto postsynaptic neurons and, ultimately, behavior, while reducing metabolic costs at the same time. The synchronization model has received support from a number of studies in human subjects, using source-localized magnetoencephalography. Ghuman et al. (5) report enhanced ...

show abstract

The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization

Cited by 427 publications

References 25 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

Cognitive Effort Drives Workspace Configuration of Human Brain Functional Networks

Stimulus repetition modulates gamma-band synchronization in primate visual cortex

Contact Info

Product

Resources

About