The Involvement of Endogenous Neural Oscillations in the Processing of Rhythmic Input: More Than a Regular Repetition of Evoked Neural Responses

Abstract

It is undisputed that presenting a rhythmic stimulus leads to a measurable brain response that follows the rhythmic structure of this stimulus. What is still debated, however, is the question whether this brain response exclusively reflects a regular repetition of evoked responses, or whether it also includes entrained oscillatory activity. Here we systematically present evidence in favor of an involvement of entrained neural oscillations in the processing of rhythmic input while critically pointing out which questions still need to be addressed before this evidence could be considered conclusive. In this context, we also explicitly discuss the potential functional role of such entrained oscillations, suggesting that these stimulus-aligned oscillations reflect, and serve as, predictive processes, an idea often only implicitly assumed in the literature.

Keywords: ERP; endogenous; entrainment; evoked response; oscillation; phase; power.

Figure 1

It has often been reported that neural oscillations can align to a rhythmic stimulus (shown schematically in A, bottom). The spectrum of this stimulus-aligned signal will reflect the dominant frequency of the stimulus (B, gray). However, each of the individual stimulus presentations will also evoke a neural response which, if repeated regularly, can also resemble an oscillation (shown schematically in A, top) and show a spectrum that reproduces the periodicity of the stimulus (B, black). Note that the additional peaks in the spectrum produced by the regular repetition of evoked responses reflect the imperfect sinusoidal shape of the signal which can introduce harmonic peaks in the spectrum. However, oscillations as measured with electrophysiological methods are often far from perfect sinusoids (Cole and Voytek, 2017), potentially increasing the similarity between aligned oscillations and regularly occurring evoked neural responses, and excluding harmonics in the spectrum of the signal as a criterion to distinguish the two.

Figure 2

Overview of selected studies that show endogenous oscillatory activity in the absence of measurable evoked responses. (A) Ding et al. (2016) constructed speech sentences in which not only words (4 Hz) but also phrases (2 Hz) and sentences (1 Hz) fluctuated rhythmically (top). The spectrum of these stimuli only reflected the word rate, but not the rhythm of phrases or sentences (middle). Apart from brain responses at the frequency of words, the authors also observed neural activity fluctuating at phrase and sentence rates, even though these were not present in the stimulus spectrum (bottom). Asterisks mark frequency bins with significantly higher power than neighboring bins (see Ding et al., , for details). Reproduced with permission from Ding et al. (2016). (B) In the study by Zoefel and Heil (2013), only detected but not undetected auditory stimuli produced a noticeable evoked neural response (left; no stimuli were presented during catch trials). Nevertheless, brain activity averaged across instances of three subsequently missed stimuli revealed an oscillatory pattern at stimulation frequency (right; S denotes the timing of stimulus presentation). Reproduced with permission from Zoefel and Heil (2013). (C) Lakatos et al. (2013) recorded neural activity in monkey auditory cortex during and after the presentation of rhythmic auditory stimuli. They found that, even after the offset of the rhythmic stimulus sequence, the neural phase at the time of expected stimulus occurrence (shown by vertical lines) is strongly biased toward a particular phase (see insets for a phase distribution across trials). This phenomenon was visible both in tonotopical regions tuned to the sound frequency of the stimulus (shown) and in those who are not (not shown). Reproduced with permission from Lakatos et al. (2013).

Figure 3

Overview of selected studies providing evidence from signal properties and cognitive effects that are expected to differ between endogenous oscillatory activity and regular evoked responses. (A) ten Oever et al. (2017) reported higher inter-trial coherence (ITC) for rhythmic (Rh) compared random (Ra) auditory subthreshold stimuli stream (sub-threshold trials are denoted “pre”; supra-threshold trials are denoted “post”). The higher ITC was paralleled with lower power values for the rhythmic compared to the random subthreshold sounds. Asterisks indicate a significant difference (p < 0.05) between rhythmic and random conditions. (B) The intensity required for a rhythmic stimulus to “entrain” an endogenous oscillation depends on the distance between the stimulus frequency and the natural frequency of the oscillator. This relationship results in a triangular shape representing the dependence of entrainment strength on frequency and intensity of the entraining stimulus, the so-called Arnold Tongue. Notbohm et al. (2016) reported that the EEG signal in response to a rhythmic visual stimulus follows the characteristics of an Arnold Tongue, if it is analyzed based on participants' individual alpha frequency (IAF). Reproduced with permission from Notbohm et al. (2016). (C) Mathewson et al. (2012) measured the probability of detecting a visual target at different time lags after the offset of a rhythmic visual stimulus (~12 Hz). They found a periodic modulation of perception (i.e., target detection); these aftereffects were also present when a certain jitter was introduced in the rhythm, but not after the presentation of two visual stimuli separated by a certain time interval (576 ms) but without any rhythmic component (control). Reproduced with permission from Mathewson et al. (2012).