Tuning of the Human Neocortex to the Temporal Dynamics of Attended Events

Besle, Julien; Schevon, Catherine A.; Mehta, Ashesh D.; Lakatos, Péter L.; Goodman, Robert; McKhann, Guy M.; Emerson, Ronald G.; Schroeder, Charles E.

doi:10.1523/jneurosci.4518-10.2011

Cited by 245 publications

(244 citation statements)

References 33 publications

Supporting

Mentioning

210

Contrasting

Order By: Relevance

“…Auditory studies have similarly investigated the impact of pre-target oscillatory state but did so mostly in paradigms in which oscillations were driven by discrete and periodic stimuli. These auditory studies found effects mostly at lower frequencies, such as the delta and theta bands (Luo and Poeppel, 2007;Lakatos et al, 2009;Schroeder and Lakatos, 2009;Stefanics et al, 2010;Besle et al, 2011;Ding and Simon, 2012). Our results reiterate this importance of theta-band over alpha-band oscillations in auditory cortex for stimulus detection.…”

Section: Role Of Oscillatory State For Perceptionsupporting

confidence: 84%

“…For example, psychophysical perceptual performance correlates with specific states of spontaneous prestimulus oscillations, as shown by correlations between alpha-band power and visual detection rates (Romei et al, 2008;van Dijk et al, 2008) and dependencies of detection rates on the phase of ongoing oscillations (Busch et al, 2009;Mathewson et al, 2009;Busch and VanRullen, 2010). Such effects of prestimulus oscillatory state on perception can be further enhanced by expectation or attention Schroeder and Lakatos, 2009;Stefanics et al, 2010;Besle et al, 2011) and also manifest in occulomotor responses . These findings promote speculations about a periodic processing mode of sensation Giraud and Poeppel, 2012;Jensen et al, 2012), whereby discrete windows of opportunity control the entry of stimuli to cognition.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

A Precluding But Not Ensuring Role of Entrained Low-Frequency Oscillations for Auditory Perception

2012

View full text Add to dashboard Cite

Oscillatory activity in sensory cortices reflects changes in local excitation-inhibition balance, and recent work suggests that phase signatures of ongoing oscillations predict the perceptual detection of subsequent stimuli. Low-frequency oscillations are also entrained by dynamic natural scenes, suggesting that the chance of detecting a brief target depends on the relative timing of this to the entrained rhythm. We tested this hypothesis in humans by implementing a cocktail-party-like scenario requiring subjects to detect a target embedded in a cacophony of background sounds. Using EEG to measure auditory cortical oscillations, we find that the chance of target detection systematically depends on both power and phase of theta-band (2-6 Hz) but not alpha-band (8 -12 Hz) oscillations before target. Detection rates were higher and responses faster when oscillatory power was low and both detection rate and response speed were modulated by phase. Intriguingly, the phase dependency was stronger for miss than for hit trials, suggesting that phase has a inhibiting but not ensuring role for detection. Entrainment of theta range oscillations prominently occurs during the processing of attended complex stimuli, such as vocalizations and speech. Our results demonstrate that this entrainment to attended sensory environments may have negative effects on the detection of individual tokens within the environment, and they support the notion that specific phase ranges of cortical oscillations act as gatekeepers for perception.

show abstract

Section: Role Of Oscillatory State For Perceptionsupporting

confidence: 84%

Section: Introductionmentioning

confidence: 99%

A Precluding But Not Ensuring Role of Entrained Low-Frequency Oscillations for Auditory Perception

2012

View full text Add to dashboard Cite

show abstract

“…Recordings from macaque auditory cortex (3,9,10), human auditory cortex (11), and human electroencephalography (EEG) recordings (12)(13)(14) confirm that delta phase reorganizes in response to rhythmic auditory stimulation and that optimal phase aligns to expected times of event onsets. The results are amplified event-related potentials (ERPs) and increased firing in response to stimulus onsets (3,15).…”

mentioning

confidence: 87%

Frequency modulation entrains slow neural oscillations and optimizes human listening behavior

Henry

Obleser

2012

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

392

393

View full text Add to dashboard Cite

The human ability to continuously track dynamic environmental stimuli, in particular speech, is proposed to profit from "entrainment" of endogenous neural oscillations, which involves phase reorganization such that "optimal" phase comes into line with temporally expected critical events, resulting in improved processing. The current experiment goes beyond previous work in this domain by addressing two thus far unanswered questions. First, how general is neural entrainment to environmental rhythms: Can neural oscillations be entrained by temporal dynamics of ongoing rhythmic stimuli without abrupt onsets? Second, does neural entrainment optimize performance of the perceptual system: Does human auditory perception benefit from neural phase reorganization? In a human electroencephalography study, listeners detected short gaps distributed uniformly with respect to the phase angle of a 3-Hz frequency-modulated stimulus. Listeners' ability to detect gaps in the frequency-modulated sound was not uniformly distributed in time, but clustered in certain preferred phases of the modulation. Moreover, the optimal stimulus phase was individually determined by the neural delta oscillation entrained by the stimulus. Finally, delta phase predicted behavior better than stimulus phase or the event-related potential after the gap. This study demonstrates behavioral benefits of phase realignment in response to frequency-modulated auditory stimuli, overall suggesting that frequency fluctuations in natural environmental input provide a pacing signal for endogenous neural oscillations, thereby influencing perceptual processing.pre-stimulus phase | auditory processing | EEG | FM N eural oscillations are associated with rhythmic fluctuations in the excitation-inhibition cycle of local neuronal populations (1-3). That is, a single neuron is not equally likely to discharge in response to stimulation at all points in time. Instead, its likelihood of responding is influenced by local extracellular and membrane potentials that, in turn, are reflected in neural oscillations. Critically, these neural oscillations can be entrained by external rhythmic sensory stimulation (3, 4) or, less naturally, by rhythmic neural stimulation using transcranial magnetic stimulation (TMS) or transcranial alternating current stimulation (TACS; refs. 5 and 6). As a result, neurons are more likely to fire at temporally expected points in time. Restated, the time of peak neural sensitivity predicts the point in time at which an upcoming stimulus will occur within a framework of continued temporal regularity. Such a rhythmic neural processing mode is adaptive given the abundance of behaviorally relevant environmental auditory stimuli that are inherently rhythmic in nature and, thus, could provide a pacing signal for neural oscillations across a range of frequency bands.Entrainment of low-frequency oscillations involves a reorganization of phase so that the optimal, in this case most excitable, phase comes into line with temporally expected critical events in the ong...

show abstract

“…gamma range, N 40 Hz) provide a reliable index of feature binding within and across sensory modalities (Arnal et al, 2011;Engel et al, 1991;Roelfsema et al, 1997;Senkowski et al, 2008;Tallon-Baudry and Bertrand, 1999). In multisensory integration, low-frequency neural oscillations (delta, 1-2 Hz) play a crucial role in the temporal selection (Besle et al, 2011;Fiebelkorn et al, 2013;Gomez-Ramirez et al, 2011;Lakatos et al, 2008;Schroeder and Lakatos, 2009) and in the integration of AV information (Fiebelkorn et al, 2011;Kösem and van Wassenhove, 2012;Luo et al, 2010).…”

Section: Neural Oscillations: Multiplex Encoding Of Informationmentioning

confidence: 99%

“…Here, we hypothesize that the brain could use oscillatory entrainment to establish a temporal reference frame and we thus ask whether the phase of entrained neural oscillations actually encodes the "when" of perception. Specifically, the preferred phase of oscillatory entrainment is known to be context-dependent (Besle et al, 2011;Gomez-Ramirez et al, 2011;Lakatos et al, 2008;Rees et al, 1986), suggesting that neural entrainment may not be a passive neural response. Additionally, preferential phases of entrained neural oscillations are subject-specific (Besle et al, 2011), making this neural index particularly well-suited for investigating the highly subjective and variable nature of time perception.…”

Section: Introductionmentioning

confidence: 99%

Encoding of event timing in the phase of neural oscillations

2014

View full text Add to dashboard Cite

a b s t r a c t a r t i c l e i n f oTime perception is a critical component of conscious experience. To be in synchrony with the environment, the brain must deal not only with differences in the speed of light and sound but also with its computational and neural transmission delays. Here, we asked whether the brain could actively compensate for temporal delays by changing its processing time. Specifically, can changes in neural timing or in the phase of neural oscillation index perceived timing? For this, a lag-adaptation paradigm was used to manipulate participants' perceived audiovisual (AV) simultaneity of events while they were recorded with magnetoencephalography (MEG). Desynchronized AV stimuli were presented rhythmically to elicit a robust 1 Hz frequency-tagging of auditory and visual cortical responses. As participants' perception of AV simultaneity shifted, systematic changes in the phase of entrained neural oscillations were observed. This suggests that neural entrainment is not a passive response and that the entrained neural oscillation shifts in time. Crucially, our results indicate that shifts in neural timing in auditory cortices linearly map participants' perceived AV simultaneity. To our knowledge, these results provide the first mechanistic evidence for active neural compensation in the encoding of sensory event timing in support of the emergence of time awareness.

show abstract

Tuning of the Human Neocortex to the Temporal Dynamics of Attended Events

Cited by 245 publications

References 33 publications

A Precluding But Not Ensuring Role of Entrained Low-Frequency Oscillations for Auditory Perception

A Precluding But Not Ensuring Role of Entrained Low-Frequency Oscillations for Auditory Perception

Frequency modulation entrains slow neural oscillations and optimizes human listening behavior

Encoding of event timing in the phase of neural oscillations

Contact Info

Product

Resources

About