Sensory neural codes using multiplexed temporal scales

Panzeri, Stefano; Brunel, Nicolas; Logothetis, Nikos K.; Kayser, Christoph

doi:10.1016/j.tins.2009.12.001

Cited by 484 publications

(440 citation statements)

References 82 publications

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Section: Discussionsupporting

confidence: 67%

“…3b). The observation that mid-and high-gamma activity were related to the phase consistency of beta and theta activity, respectively, extends the ideas that gamma frequency variations reflect information routing 32,34,45,46 and that message-passing is indexed by specific hierarchical combinations of slow and high frequencies (low/high frequency ratio) 47 .The current data demonstrate that violating intermodal expectations changes the neural dynamics of slow (delta and theta) brain activity, and increases the coordination between local low-beta and high-gamma oscillatory activity. Our data suggest that this transition occurs in brain regions where audio-visual predictions are likely updated (STS) and new prediction errors generated (auditory and visual cortices).…”

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confidence: 67%

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Transitions in neural oscillations reflect prediction errors generated in audiovisual speech

2011

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According to the predictive coding theory, top-down predictions are conveyed by backward connections and prediction errors are propagated forward across the cortical hierarchy. Using MEG in humans, we show that violating multisensory predictions causes a fundamental and qualitative change in both the frequency and spatial distribution of cortical activity. When visual speech input correctly predicted auditory speech signals, a slow delta regime (3-4 Hz) developed in higher-order speech areas. In contrast, when auditory signals invalidated predictions inferred from vision, a low-beta (14-15 Hz) / high-gamma (60-80 Hz) coupling regime appeared locally in a multisensory area (area STS). This frequency shift in oscillatory responses scaled with the degree of audio-visual congruence and was accompanied by increased gamma activity in lower sensory regions. These findings are consistent with the notion that bottom-up prediction errors are communicated in predominantly high (gamma) frequency ranges, whereas top-down predictions are mediated by slower (beta) frequencies.© 2011 Nature America, Inc. All rights reserved.7 9 8 VOLUME 14 | NUMBER 6 | JUNE 2011 nature neurOSCIenCe a r t I C l e S converge-that is, where multisensory predictions are generatedwhereas gamma activity was seen in lower sensory cortices where prediction errors emerge and are propagated forward. RESULTSWe presented 15 subjects with stimuli in one of three conditions: videos (audio-visual: AV condition) of a speaker pronouncing the syllables /pa/, / a/, /la/, /ta/, /ga/ and /fa/ (International Phonetic Alphabet notation); an auditory track of these videos combined with a still face (auditory: A condition); or a mute visual track (visual: V condition). The videos could be either natural or a random combination of auditory and visual tracks, creating conditions in which auditory and visual tracks were congruent (AVc condition) and ones in which they were incongruent (AVi condition; see Online Methods and Supplementary Fig. 1). Incongruent combinations yielding fusion illusory percepts-that is, McGurk stimuli-were excluded 8,11 . Subjects performed an unrelated target detection task on the syllable /fa/ that was presented in A, V or AVc form in 13% of the trials (97% correct detection). These trials were subsequently excluded from the analyses. The five other syllables were chosen because they yielded graded recognition accuracy when presented visually (Fig. 1a), resulting from an increasing predictiveness 10 . The phonological prediction conveyed by mouth movements (visemes) varies in specificity depending on the pronounced syllable. Typically, syllables beginning with a consonant that is formed at the front of the mouth (/p/, /m/) convey a more specific prediction than those formed at the back (/g/, /k/, /r/, /l/) 8 . Our second experimental factor pertained to the validity of the visual prediction with respect to the auditory input. Physically, the audio-visual stimuli could be either congruent (valid prediction) or incongruent (invalid prediction), w...

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Section: Discussionsupporting

confidence: 67%

supporting

confidence: 67%

Transitions in neural oscillations reflect prediction errors generated in audiovisual speech

2011

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“…integration (Panzeri et al, 2010;van Wassenhove, 2009), while the phase of neural oscillations provides the temporal stamping operation needed to preserve the timing of operations in parallel systems. As such, the same informational content can be encoded in a multiplexed manner with (i) integration operating on those sensory attributes used in the building of an internal object (Engel and Singer, 2001;Treisman, 1996) while (ii) segregation -or temporal stampingprovides the automatic encoding of event timing.…”

Section: Neural Oscillations: Multiplex Encoding Of Informationmentioning

confidence: 99%

Encoding of event timing in the phase of neural oscillations

2014

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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.

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“…In other situations, inhibition correlates spiking across pairs of neurons (14)(15)(16)(17)(18)(19). Inhibitory inputs can change rates and correlations differentially, suggesting that some circuits may be capable of encoding stimulus information at multiple timescales (20)(21)(22)(23)(24). Thus, inhibition can influence population activity in a variety of ways according to the details of the circuitry and the patterns of population activity.…”

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confidence: 99%

Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition

Giridhar

Doiron

Urban

2011

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

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Neurons respond to sensory stimuli by altering the rate and temporal pattern of action potentials. These spike trains both encode and propagate information that guides behavior. Local inhibitory networks can affect the information encoded and propagated by neurons by altering correlations between different spike trains. Correlations introduce redundancy that can reduce encoding but also facilitate propagation of activity to downstream targets. Given this trade-off, how can networks maximize both encoding and propagation efficacy? Here, we examine this problem by measuring the effects of olfactory bulb inhibition on the pairwise statistics of mitral cell spiking. We evoked spiking activity in the olfactory bulb in vitro and measured how lateral inhibition shapes correlations across timescales. We show that inhibitory circuits simultaneously increase fast correlation (i.e., synchrony increases) and decrease slow correlation (i.e., firing rates become less similar). Further, we use computational models to show the benefits of fast correlation/slow decorrelation in the context of odor coding. Olfactory bulb inhibition enhances population-level discrimination of similar inputs, while improving propagation of mitral cell activity to cortex. Our findings represent a targeted strategy by which a network can optimize the correlation structure of its output in a dynamic, activity-dependent manner. This trade-off is not specific to the olfactory system, but rather our work highlights mechanisms by which neurons can simultaneously accomplish multiple, and sometimes competing, aspects of sensory processing.

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Sensory neural codes using multiplexed temporal scales

Cited by 484 publications

References 82 publications

Transitions in neural oscillations reflect prediction errors generated in audiovisual speech

Transitions in neural oscillations reflect prediction errors generated in audiovisual speech

Encoding of event timing in the phase of neural oscillations

Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition

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