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A Precluding Role of Low-Frequency Oscillations for Auditory Perception in a Continuous Processing Mode

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A Precluding Role of Low-Frequency Oscillations for Auditory Perception in a Continuous Processing Mode The Journal of Neuroscience, December 5, 2012 • 32(49):17525–17527 • 17525 Journal Club Editor’s Note: These short, critical reviews of recent papers in the Journal, written exclusively by graduate students or postdoctoral fellows, are intended to summarize the important findings of the paper and provide additional insight and commentary. For more information on the format and purpose of the Journal Club, please see http://www.jneurosci.org/misc/ifa_features.shtml. A Precluding Role of Low-Frequency Oscillations for Auditory Perception in a Continuous Processing Mode Molly J. Henry* and Bjo¨rn Herrmann* Max Planck Research Group “Auditory Cognition,” Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany Review of Ng et al. Neural oscillatory activity is suggested more quickly and elicited larger evoked Consistent results were observed to play an important role in human per- brain responses. across measures, with significant differ- ception and cognition (Buzsa´ki and A recent report in The Journal of Neu- ences observed between hits and misses Draguhn, 2004). For example, recent roscience was the first to show neural in pre-target time intervals for power, evidence, largely derived from experi- phase effects on the detection of near- ITPC, and the bifurcation index. Cru- ments conducted in the visual domain, threshold auditory stimuli (Ng et al., cial to the authors’ main argument, pre- suggests that near-threshold target stimuli 2012a). Electroencephalograms (EEGs) target power and phase consistency are better detected when target presenta- were recorded while human participants across trials (i.e., ITPC) were both larger tion coincides with the preferred phase in monitored for a near-threshold target for misses than for hits. Similarly, the the ongoing neural oscillation. Phase ef- sound embedded in an ongoing stimulus. bifurcation index was significantly nega- fects on detection performance have been Specifically, Ng et al. (2012a) created 4-s- tive, indicating a more concentrated observed in the theta and alpha frequency long stimuli by overlapping and adding 80 phase distribution for misses than for hits bands (for review, see VanRullen et al., different natural sound segments, each just before target occurrence. These find- 2011). 1.4–2 s in length. A brief target sound (a ings were flanked by an analysis of the in- The relation of neural oscillatory phase camera shutter) was presented on each stantaneous neural phase at a pre-target to auditory perception has been investi- trial at one of six time points distributed time point (Ϫ200 ms), which revealed gated using mostly supra-threshold stim- across the middle 1 s section of the stimu- stronger modulation of performance by uli (Lakatos et al., 2005; Stefanics et al., lus (Ng et al., 2012a; Fig. 1). Participants pre-stimulus phase for trials in which par- 2010). Endogenous oscillations in the indicated detection via button press. Be- ticipants failed to detect the target sound delta band were entrained by (i.e., phase havioral performance showed that partic- than for trials in which the target was locked to) external rhythmic stimulation, ipants perceived targets in approximately detected. leading to precise time locking of the op- half of the trials. Trials were thus split into Thus, this is the first study to demon- timal neural delta phase to the onset time hits and misses for the EEG analysis. strate a specific modulation of miss rates, of a predictable target. In turn, targets fall- The EEG analyses focused on oscilla- but not hit rates, for near-threshold stim- ing into the preferred or “best” phase of tory activity in the 2–6 Hz frequency uli as a function of the phase of ongoing the delta oscillation were responded to band. The authors reported results in neural oscillations. On this basis, the au- terms of pre-target power, intertrial phase thors conclude that the role of a low- coherence (ITPC), and a bifurcation in- frequency (2–6 Hz) oscillatory phase in Received Sept. 19, 2012; revised Oct. 4, 2012; accepted Oct. 8, 2012. dex. Power reflects the overall magnitude audition is a “precluding” rather than an M.J.H. and B.H. are supported by the Max Planck Society (Max Planck of oscillatory brain activity, and ITPC in- “ensuring” one. Put differently, they sug- Research Group Grant to Jonas Obleser). We are grateful to Benedict Ng for dexes the concentration of the neural gest that oscillatory phase serves a protec- providing us with an example stimulus from the original study. *M.J.H. and B.H. contributed equally to this work. phase or “phase consistency” across trials. tive or gating role—keeping out sensory CorrespondenceshouldbeaddressedtoeitherBjo¨rnHerrmannorMolly For the bifurcation index, negative values information that coincides with the sub- J. Henry, Max Planck Research Group Auditory Cognition, Max Planck Insti- indicate stronger phase concentration in optimal phase of the oscillation rather tute for Human Cognitive and Brain Sciences, Stephanstraße 1A, 04103 one condition (i.e., hits vs misses), while than selecting sensory information that Leipzig, Germany. E-mail: [email protected] or henry@cbs. mpg.de. positive values indicate phase consistency coincides with the optimal phase of the DOI:10.1523/JNEUROSCI.4456-12.2012 for both hits and misses, but with different oscillation. This finding contrasts with a Copyright © 2012 the authors 0270-6474/12/3217525-03$15.00/0 preferred phase angles. number of previous studies that report 17526 • J. Neurosci., December 5, 2012 • 32(49):17525–17527 Henry and Herrmann • Journal Club Figure 1._Waveform (top), amplitude envelope (red line), and spectrum (bottom) are shown separately for an example stimulus from the original study (left, courtesy of Benedict Ng), and also a spokenGermansentenceforcomparison(right,“DerMinisterhatwa¨hrendderSitzunginderHauptstadtdenSprechergetroffenunddasErgebnisberichtet.”).Incontrasttothetemporalregularity contained in the sentence material, the example stimulus possesses no temporal regularity by which neural oscillations could be entrained. (a.u., arbitrary units). both a “best” and a “worst” phase within segments was lost as a result of overlap- sponds to a “worst,” or in the terms of Ng et al. the cycle of a low-frequency oscillation ping and adding 80 sound tokens. In this (2012a), “precluding” phase. (Lakatos et al., 2005; Mathewson et al., regard, it is important to note that the re- As opposed to the rhythmic processing 2009). ported ITPC data suggesting entrained mode, listeners are likely to enter a continu- We suggest that the reason for this discrep- neural responses (Ng et al., 2012a, their ous processing mode when stimuli are tem- ancy is the likely use of a continuous (rather Fig. 2A) were taken from a previous study porally unstructured as in Ng et al., 2012a. than rhythmic) processing mode by listeners by the same group (Ng et al., 2012b) that During continuous processing, low-fre- in the study of Ng et al. (2012a). The authors critically involved a different stimulus in quency modulations are suppressed and examined brain responses in the 2–6 Hz fre- which temporal structure might have sup- long periods of low excitability are mini- quency range because ITPC in low frequency ported neural phase locking. In the cur- mized (Schroeder and Lakatos, 2009). That Ͻ bands ( 8 Hz) was reported to be greater than rent study, however, there is insufficient is, the low-frequency oscillation spends rel- Ͼ in higher frequency bands ( 8 Hz; see Ng et evidence to conclude that the stimulation atively more time in the high-excitability al., 2012a, their Fig. 2A). In particular, this in- elicited consistent brain responses that phase—since the onset time of a future creased ITPC was interpreted as evidence of could be taken as entrained. stimulus is unpredictable, it is advantageous neural entrainment. In the context of the We therefore suggest that the absence of to be ready at all times. Thus, a “best” phase brain–environment relation, entrainment in- any “ensuring” effect of a low-frequency oscil- for target detection is not necessarily ex- volves coupling of ongoing neural oscillations pected. However, a “worst” (i.e., “preclud- latory phase might lie directly in the failure of to rhythmic (i.e., oscillatory) external stimula- ing”) phase for detection is likely to be the stimulation to entrain ongoing brain oscil- tion such that the two systems have, on aver- observed during inevitable lapses in the lations. This point is critical in light of the age, equivalent periods and their phase maintenance of high excitability. We sug- recently proposed distinction between “rhyth- relationship is stable. By this definition, both gest that it is exactly these lapses into the mic” versus “continuous” processing modes oscillatory systems must possess temporal reg- low-excitability phase of the low-frequency ularity (Roenneberg et al., 2005). Even by a (Schroeder and Lakatos, 2009). Stimuli con- oscillation that Ng et al. (2012a) observed more loose definition of entrainment as in- taining temporal regularities at different time and that correspond to the peak in the dis- volving a neural response that tracks a quasi- scales are preferably processed in a “rhythmic” tribution of misses. periodic signal such as speech over time (Peelle mode. This mode supports predictions about In conclusion, our interpretation of the and Davis, 2012), the signal must possess some the time of occurrence of an upcoming (and data of Ng and colleagues is not at all incon- modulation by which the brain can be possibly important) event. An advantageous sistent with the existence of both an optimal entrained. and energy-efficient consequence of entrain- (excitatory) and a suboptimal (inhibitory) In contrast, stimuli presented in the ment to a temporally predictable sequence is phase of low-frequency oscillations—that study by Ng et al. (2012a) lacked temporal that the high-excitability phase of the en- is, an “ensuring” and a “precluding” role for regularity and thus could not entrain on- trained oscillation aligns with event onsets, low-frequency oscillatory phase.
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