Neuroscience 337 (2016) 306–314
TRACING THE NEURAL BASIS OF AUDITORY ENTRAINMENT
ALEXANDRE LEHMANN, b,c,d,ey
DIANA JIMENA ARIAS a,b*y AND
MARC SCHÖNWIESNER b,c,d
a
University of Quebec at Montreal, Montreal, QC, Canada
b
International Laboratory for Brain, Music and Sound
Research (BRAMS), Montreal, QC, Canada
c
Center for Research on Brain, Language and Music (CRBLM),
Montreal, QC, Canada
d
Department of Psychology, University of Montreal, Montreal,
QC, Canada
e
Department of Otolaryngology Head & Neck Surgery,
McGill University, Montreal, QC, Canada
Abstract—Neurons in the auditory cortex synchronize their
responses to temporal regularities in sound input. This cou-
pling or ‘‘entrainment” is thought to facilitate beat extraction
and rhythm perception in temporally structured sounds,
such as music. As a consequence of such entrainment,
the auditory cortex responds to an omitted (silent) sound
in a regular sequence. Although previous studies suggest
that the auditory brainstem frequency-following response
(FFR) exhibits some of the beat-related effects found in the
cortex, it is unknown whether omissions of sounds evoke
a brainstem response. We simultaneously recorded cortical
and brainstem responses to isochronous and irregular
sequences of consonant–vowel syllable /da/ that contained
sporadic omissions. The auditory cortex responded
strongly to omissions, but we found no evidence of evoked
responses to omitted stimuli from the auditory brainstem.
However, auditory brainstem responses in the isochronous
sound sequence were more consistent across trials than in
the irregular sequence. These results indicate that the audi-
tory brainstem faithfully encodes short-term acoustic prop-
erties of a stimulus and is sensitive to sequence
regularity, but does not entrain to isochronous sequences
sufficiently to generate overt omission responses, even for
sequences that evoke such responses in the cortex. These
findings add to our understanding of the processing of
sound regularities, which is an important aspect of human
cognitive abilities like rhythm, music and speech percep-
tion. Ó 2016 IBRO. Published by Elsevier Ltd. All rights
reserved.
*Correspondence to: A. Lehmann, Department of Otolaryngology
Head & Neck Surgery, McGill University, Montreal, QC, Canada.
E-mail address: dianajiab@gmail.com (D. J. Arias).
y
Shared first authorship: these authors contributed equally to this
work.
Abbreviations: FFR, frequency-following response; FFT, Fourier
transform; Fpz, fronto-central electrode; RMS, root mean square
amplitude; SOA, stimulus onset asynchrony.
http://dx.doi.org/10.1016/j.neuroscience.2016.09.011
0306-4522/Ó 2016 IBRO. Published by Elsevier Ltd. All rights reserved.
306
Key words: rhythmic entrainment, human brainstem, audi-
tory cortex, electro-encephalography, temporal regularity,
stimulus omissions.
INTRODUCTION
Neurons in the auditory cortex can synchronize their
activity to a regular stimulation (Nozaradan et al., 2011,
2012). Such neurons may underlie a pattern-forming
dynamical system or a bank of oscillators that couple to
external rhythms and thus enable entrainment to different
rates of the auditory input. Entrainment to stimulus regu-
larities may underlie cognitive functions such as the per-
ception of beat in music (Jones, 1974; Large and Kolen,
1994; Gasser and Eck, 1996; Eck, 1999; Large and
Jones, 1999; van Noorden and Moelants, 1999; Large
and Grondin, 2008) and the ability to synchronize move-
ments with predictable, periodic sounds (Deutsch, 1983;
Peper et al., 1995; Jones and Pfordresher, 1997; Jones
and Yee, 1997; Scheirer, 1998; Pressing, 1999; Repp,
1999; van Noorden and Moelants, 1999; Snyder and
Krumhansl, 2001). Several models have been proposed
for the extraction of temporal structure, such as the afore-
mentioned bank of oscillators (Large et al., 2015), but also
models based on note duration (Longuet-Higgins and
Lee, 1982), autocorrelation (Brown, 1993; Vos et al.,
1994), pulse saliency (Parncutt, 1994), comb filtering
(Scheirer, 1998), neural networks (Gasser et al., 1999),
rule-based systems (Desain and Honing, 1999; Eck,
2001), and information theory (Casagrande and Eck,
2005). None of these models is tied to specific neural pro-
cessing stages, perhaps because the neural basis of beat
induction and rhythm perception is complex and involves
many auditory and non-auditory brain regions (Schubotz
and Cramon, 2001; Grahn and Brett, 2007; Chen et al.,
2008, 2009; Grahn, 2009; Teki et al., 2011; Konoike
et al., 2012; Grahn and Rowe, 2013).
In particular, it is unclear at the moment to what extent
auditory brainstem structures contribute to beat
extraction. Auditory brainstem responses exhibit some
of the beat-related effects found in the cortex. Brainstem
responses to sound onsets falling on a beat are larger
than responses to off-beat onsets (Tierney and Kraus,
2013). Individuals who are able to tap in synchrony with
a simple beat also have less variable timing and greater
between-trial phase-locking of the auditory brainstem
response than those less able to tap in synchrony
(Tierney and Kraus, 2013). Auditory brainstem responses
are also modulated by musical expertise in general (Wong
et al., 2007) and respond to other features of music, such
as intervals (Lee et al., 2009; Lerud et al., 2014).
 A. Lehmann et al. / Neuroscience 337 (2016) 306–314 307

Here we asked whether the human auditory brainstem Procedure

responds to infrequent sound omissions and whether
The experiment was conducted in a sound-attenuated
regularity in the presented sequence of sounds
and electromagnetically shielded room. Participants
modulates this response. Responses evoked when a
were comfortably seated and watched a silent subtitled
sound is omitted from a regular sequence are thought to
movie while auditory-evoked responses were recorded.
indicate that neural populations have become entrained
They were instructed to remain immobile during the
to the temporal structure of the sequence (Snyder and
recording periods to minimize muscle artefacts. The
Large, 2005; Zanto et al., 2006). Perhaps the most basic
experiment started with a 2-min recording of click-
form of an omission response occurs when sounds are
evoked ABR to verify the integrity of the peripheral and
infrequently omitted from an isochronous sequence of
brainstem auditory processing. The test consisted of a
identical sounds. Such events evoke a cortical mismatch
series of 2500 clicks of 100-ls duration presented
response (Näätänen, 1975; Tervaniemi et al., 1994; Yabe
binaurally at 75-dB SPL at a presentation rate of 20 Hz
et al., 1997; Näätänen et al., 2007).
through insert earphones (ER2, Etymotic Research,
We measured auditory-evoked responses to
www.etymotic.com).
isochronous and temporally jittered sequences of a
Participants then completed two experimental
consonant–vowel syllable, simultaneously at the
conditions of 54 min each, in which /da/ stimuli were
auditory brainstem and cortical level. Stimuli were
presented binaurally via insert earphones at 72.5-dB
pseudo-randomly omitted and we compared responses
SPL and at an average presentation rate of 11.1 Hz.
to stimuli and omissions between brainstem and cortex
Stimulus presentation was controlled by custom Matlab
and between temporally regular and irregular
scripts (The MathWorks, www.mathworks.com) and
sequences. If portions of the auditory brainstem track
stimuli were generated and played digitally by a
temporal regularity in sound sequences and contribute
dedicated signal processor (RX6, Tucker-Davis
to beat extraction, then they should respond to omitted
Technologies, www.tdt.com) at a 50-kHz sampling rate.
sounds during isochronous but not irregular sequences.
Within conditions, stimuli were presented in either an
An absence of such responses to omitted stimuli in both
isochronous or a temporally jittered (irregular) sequence
conditions would imply that the brainstem does not
(Fig 1). In the isochronous condition, all sounds were
contribute to these brain mechanisms, or that the
presented with a stimulus onset asynchrony (SOA) of
contribution does not result in an evoked response. If
90 ms (inter-stimulus interval of 50 ms), whereas in the
brainstem structures entrain to repetitive sound
irregular condition the SOA was randomly selected from
sequences, we would also expect a more robust
a uniform distribution ranging from 57 ms to 127 ms in
frequency encoding of these responses during
each trial (inter-stimulus intervals between 17–87 ms).
isochronous than irregular sequences, as well as higher
The average onset asynchrony was 90 ms in both
neural consistency. In the cortex, we expected to
conditions. Stimuli were infrequently (8%) omitted from
replicate previous findings in the form of a typical tri-
each sequence. Omissions were always separated by 8
phasic response evoked by omissions.
to 18 /da/ stimuli. Five silent blocks of 160 trials without
stimulus presentation were inserted at pseudorandom
EXPERIMENTAL PROCEDURES times during both conditions.
Each condition consisted of 31250 /da/ trials, 2500
Participants omission trials and 2560 silent trials.
Fifteen healthy normal-hearing participants (3 males)
between the ages of 22 and 41 years were recruited to
EEG recordings
take part in the experiment. Participants gave informed
consent and received a financial compensation for their EEG signals were recorded from five active sintered Ag-
time. One participant was excluded due to a noisy EEG AgCl electrodes placed at the hairline fronto-central
signal. The experimental procedure conformed to the electrode (Fpz), the vertex (Cz), the seventh cervical
World Medical Association’s Declaration of Helsinki and (C7), and the mastoids (M1 and M2). Active electrodes
was approved by the Research Ethics Committee of contain the first amplifier stage within the electrode
the Faculty of Arts and Sciences of the University of cover and provide impedance transformation on the
Montreal. electrode to prevent interference currents from
generating significant impedance-dependent nuisance
voltages. We therefore did not control electrode
Stimuli
impedances but rather kept direct-current offset close to
A synthetic consonant–vowel syllable, /da/, was used to zero during electrode placement. Reference-free
evoke brainstem and cortical responses. Evoked and electrode signals were amplified, sampled at 16384 Hz
frequency-following responses (FFRs) to this stimulus (ActiveTwo amplifier, BioSemi, www.biosemi.com), and
have been studied extensively (Russo et al., 2004; Skoe stored for offline analysis.
and Kraus, 2010a). In a pilot experiment, this stimulus
evoked larger-amplitude responses than other simple
Data analysis
and complex tones and syllables. The stimulus is 40-ms
long and its fundamental frequency varies slightly Data analysis was performed in Matlab (The Mathworks,
between 117 and 121 Hz over this duration. www.mathworks.com/matlab) using eeglab (Delorme
308 A. Lehmann et al. / Neuroscience 337 (2016) 306–314
A Isochronous condition
omis
da da sion
da silence
40ms 50ms 40ms 160 x SOA
SOA = 90ms
B Irregular condition
omis
da da sion da silence
min.17ms mean 50ms max. 87ms 160 x SOA
Fig. 1. Presentation of stimuli in isochronous and irregular
sequences. Both sequences contain /da/ syllables, infrequent syllable
omissions, and blocks of 160 silent SOAs. (A) In the isochronous
condition stimuli were presented with an SOA of 90 ms (ISI 50 ms).
(B) In the irregular condition the SOA varied between 57 and 127 ms
with an average of 90 ms, and the ISI varied between 17 ms and
87 ms with an average of 50 ms.
and Makeig, 2004), erplab (Lopez-Calderon and Luck,
2014) and letswave (http://amouraux.webnode.com/lets-
wave) toolboxes, as well as custom Matlab scripts. Fol-
lowing published procedures, responses were bandpass
filtered into a high- or low-frequency band in order to iso-
late subcortical and cortical components of the EEG sig-
nal (Musacchia et al., 2008; Skoe and Kraus, 2010a;
Lehmann et al., 2015). For the subcortical response, data
from a Fpz were re-referenced to the seventh cervica
(C7), as this montage has been shown to elicit a brain-
stem FFR with a better signal-to-noise ratio than the tradi-
tional montage (Cz referenced to mastoids) used for
auditory-evoked potentials (King and Sininger, 1992;
Krishnan et al., 2005; Cousineau et al., 2015). For the cor-
tical response, recording from the vertex electrode (Cz)
was referenced to linked mastoids, as done for the corti-
cal components by a previous studies that simultaneously
recorded cortical and subcortical activity (Musacchia
et al., 2008).
Brainstem frequency-following responses. To analyze
auditory brainstem responses, continuous EEG
recordings from the hairline electrode (Fpz) were re-
referenced to C7, bandpass-filtered off-line between
100 Hz and 2 kHz, and split into epochs spanning from
20 ms to +70 ms relative to stimulus onset (Krishnan
et al., 2005; Skoe and Kraus, 2010a). Epochs containing
artifacts were rejected by visual inspection and by using
eeglab’s automatic iterative rejection procedure with an
initial threshold of five standard deviations (Delorme and
Makeig, 2004). FFRs were obtained by averaging epochs
separately for each condition and trial type: responses to /
da/ stimuli preceding an omission (‘‘prior /da/”), those just
after an omission (‘‘post /da/”), the omissions themselves
(‘‘omission”), and silent trials excluding the first 50 trials of
each silent block (‘‘silence”).
Because the sustained period of the FFR reflects
phase-locking to characteristics of the stimulus
waveform (Song et al., 2008; Skoe and Kraus, 2010a),
we computed a fast Fourier transform (FFT) of each
FFR between 5 ms and 50 ms after stimulus onset and
measured the spectral amplitude of frequency bins from
105 Hz to 135 Hz (corresponding to the stimulus F0). In
addition, we measured the root mean square amplitude
(RMS) for each FFR in the same time window of 5 ms
to 50 ms after stimulus onset. Furthermore, we measured
trial-by-trial consistency of the responses to the sound
stimuli in the isochronous and irregular conditions by com-
puting correlation coefficients between even- and odd-
numbered trials (Hornickel and Kraus, 2013). Response
consistency was found to be lower in non-bilingual adults
(Krizman et al., 2014), and poor readers (Hornickel and
Kraus, 2013). It has been interpreted as increased neural
variability as shown in experimental-animal models
(Centanni et al., 2014).
Spectral amplitude measures were entered into two
different repeated-measures ANOVAs with factors
‘‘sequence regularity” (isochronous or irregular) and
stimulus type: the first ANOVA compared omissions and
silent blocks to check for effects of entrainment
(increased response amplitude within sound sequence),
the second ANOVA compared prior /da/ and post /da/
stimuli to check for effects of adaptation (increased
response amplitudes after omissions). The same
procedure was applied to the RMS measures.
Response consistency was compared across conditions
in a repeated measures ANOVA with factors ‘‘sequence
regularity” (isochronous or irregular) and stimuli type
(prior /da/ or post /da). Post-hoc t-tests were used to
detect significant differences at 5% alpha level.
Cortical Event-Related potentials and steady-state-
evoked potentials. To analyze cortical responses, EEG
signals from electrode Cz were re-referenced to the
average signal recorded from the left and right mastoid,
bandpass-filtered between 0.1 Hz and 50 Hz, and
downsampled to 256 Hz.
In order to compute event-related potentials, epochs
spanning from -100 to 600 ms relative to the onset of
omissions and relative to the onset of /da/ stimuli. We
selected /da/ stimuli that were preceded and followed by
four other /da/ stimuli to exclude inconsistent responses
due to adjacent omissions or silent trials. Epochs
containing artifacts were rejected by visual inspection
and by using EEGLAB’s automatic iterative rejection
procedure with an initial threshold of five standard
deviations (Delorme and Makeig, 2004). Individual peak
amplitudes of the most prominent negative peak and the
most prominent positive peak were extracted from
responses to omissions in the isochronous and irregular
conditions and the peak-to-peak amplitude differences
were computed and compared between conditions with
a t-test.
We also computed steady-state-evoked potentials
(SSEPs) to capture neural entrainment to the
presentation rate of the stimuli (11.1 Hz). For each
participant, 15 epochs of 33-s time-locked to the onset
of a /da/ stimulus were extracted from the isochronous
and irregular conditions such that no epoch contained
silent trials. Those epochs were averaged and
transformed into the frequency domain using a FFT.
The signal-to-noise ratio of the frequency-domain signal
 A. Lehmann et al. / Neuroscience 337 (2016) 306–314
was increased by subtracting, for each frequency bin, the
average amplitude measured at three neighboring
frequency bins (Nozaradan et al., 2011). The spectral
amplitude at the presentation rate was compared
between isochronous and irregular conditions using a
two-tailed paired-sample t-test.
RESULTS
Cortex but not brainstem responds to omitted
sounds
In the cortex, we found a clear evoked response to
omitted stimuli in both regular and jitter sequences
(Fig. 2A). Negative-to-positive peak-to-peak amplitude
was larger for omissions occurring in the isochronous
compared to the irregular sequence (t13 = 6,200,
p = <.05). In the brainstem, no response was apparent
to omissions in either condition, and brainstem activity in
omission trials did not differ from activity in the silent
intervals (Repeated measures ANOVA, interaction effect
of condition* stimuli type, F1,13 = 1.395, p > .05,
Fig. 3B). Sounds flanking omissions evoked clear
responses in both conditions (Fig. 2B). Note that here
the term ‘‘omission” is used generally to address cortical
and brainstem activity obtained from the presentation of
an omitted stimulus, and therefore should not be
confused with the terms omission N1 or omission MMN
obtained from other protocols (Yabe et al., 1997;
SanMiguel et al., 2013), because cortical omission
responses may indicate several high-level mechanisms,
such as predictive coding (see introduction), but brain-
stem omission responses, if they exist, may indicate
other, perhaps lower-level, mechanisms.
Enhanced brainstem and cortical encoding of
isochronous sound sequence
Despite the lack of evoked responses to omissions in the
brainstem, we found effects of stimulus sequence
regularity. The intertrial consistency of brainstem
responses to sounds presented in the isochronous
sequence was higher than that in the irregular sequence
(repeated measures ANOVA, main effect of condition,
F1,13 = 40.504, p < .05, Fig. 3A). In order to test
whether this effect could simply be explained by the
length of the prior silent interval, we compared the
consistency obtained in the irregular condition to a
worst-case scenario where each of the two bins used to
compute consistency were composed of the larger and
smaller SOA trials respectively. This worst-case
scenario consistency measure did not differ significantly
from the originally computed one (t26 = 0.1013,
p = 0.92).
Additionally, sound stimuli following omissions (‘post /
da/’) showed higher consistency than stimuli preceding
omissions (‘prior /da/’) (main effect of stimulus type,
F1,13 = 42.942, p = <.05, isochronous sequence:
t13 = 6.187, p = <.05, irregular sequence:
t13 = 3.802, p = <.05).
309
Cortical SSEP. In the cortex, we found a clear peak in
the spectral amplitude at the repetition rate of the stimuli
in the isochronous sequence, but not in the irregular
sequence (t13 = 4.261, p = <.05; see Fig. 3C).
Pre vs post. In addition, the FFR analysis showed
enhanced responses to stimuli presented directly after
an omission compared to those presented before an
omission in both conditions (Fig. 3B), in the form of
higher spectral amplitude at the fundamental frequency
of the stimuli (F1,13 = 12.202, p = <.05, isochronous
sequence: t13 = 3.160, p = <.05, irregular sequence:
t13 = 2.284, p = <.05) and higher RMS amplitude
(F1,13 = 59.039, p = <.05, isochronous sequence:
t13 = 4.123, p = <.05, irregular sequence:
t13 = 7.863, p = <.05).
DISCUSSION
To trace entrainment-related processes along the
auditory pathway, we simultaneously recorded cortical
and subcortical responses to isochronous and irregular
sequences of sounds containing sporadic omissions.
We asked whether early brainstem centers respond to
infrequent sound omissions and whether presentation
regularity modulates the auditory brainstem response.
We observed responses evoked by omissions in the
auditory cortex, but not in the brainstem. However,
brainstem responses showed higher inter-trial
consistency when stimuli were presented in an
isochronous sequence than in an irregular sequence.
We also observed a steady-state-evoked response at
the average presentation rate in the cortex during
isochronous, but not jittered presentation. Lastly we
found stronger adaptation in the cortex and brainstem of
responses to stimuli that preceded omissions than those
that followed omissions.
Cortex, but not brainstem responds to omitted
sounds
We did not observe responses evoked by omissions in
the brainstem, even though auditory cortex responded
strongly to these omissions (Busse and Woldorff, 2003;
Zanto et al., 2006; Honing et al., 2012). Cortical omission
responses showed the expected latency and morphology
(Bendixen et al., 2012), and were larger in the isochro-
nous than in the irregular sequence, likely because
entrainment and the build-up of temporal expectancy
increases with sequence regularity (Schwartze et al.,
2011).
Similar findings were reported by Oceák and
colleagues, who found that the amplitude of standard
minus omission responses was significantly higher for
isochronous SOA compared to random SOA (Oceák
et al., 2006). Although the interpretation of omission
responses is still under debate (Predictive coding:
Cornella et al., 2015; regularity violation: Näätänen et al.,
2007; sound offset rebound: Horváth et al., 2010; loudness
changes: Oceák et al., 2006; Fishman, 2014;), there is
mounting evidence for predictive coding in the auditory
system (Bendixen et al., 2012) and computational models
310 A. Lehmann et al. / Neuroscience 337 (2016) 306–314

A Isochronous B Isochronous
4 Irregular 4
Irregular

Amplitude[ µV]

Amplitude [µV]
2 2

0 0

-2 -2

-100 0 100 200 300 400 500 -100 0 100 200 300 4 00 500
Time (ms) Time (ms)

C Isochronous Prior /da/ D Irregular Prior /da/

0.6 Post /da/ 0.6 Post /da/
0.5 Omission 0.5 Omission
0.4 0.4
Amplitude [µV]

Amplitude [µV]
0.3 0.3
0.2 0.2
0.1 0.1
0 0
-0.1 -0.1
-0.2 -0.2
-0.3 -0.3
-0.4 -0.4
-10 0 10 20 30 40 50 60 -10 0 10 20 30 40 50 60
Time (ms) Time (ms)

Fig. 2. Grand average of cortical and brainstem potentials measured in the different stimulus conditions. Cortical responses to omissions (A) and to
/da/ stimuli (B) in the isochronous (black line) and the irregular condition (gray dashed line). Responses to the ongoing sound sequence have been
subtracted to omissions. Brainstem responses to /da/ stimuli just before an omission (pale gray dashed line), to /da/ stimuli right after an omission
(black line) and to the omission (dark gray line) in the isochronous (C) and irregular conditions (D). No omission-evoked response was apparent.

Fig. 3. (A) Consistency index of /da/ events in brainstem. It corresponds to the coefficient of correlation between odd and even trials within each
condition. Isochronous sequences (gray bars) elicited responses of higher inter-trial consistency than irregular sequences (white bars). The highest
consistency was observed for stimuli directly following an omission (Post). (B) Spectral FFR amplitudes at stimulus F0 (120 Hz) for different
stimulus conditions in isochronous (gray bars) and irregular sequences (white bars). Responses to stimuli directly following an omission (Post) were
larger than those preceding omissions (Prior). No amplitude differences were found between omissions and silent periods. (C) Spectral SSEP
amplitudes at average stimulus presentation rate in the cortex. Values were extracted from epochs containing stimuli and omissions but excluding
silent blocks. No response was observed in the irregular condition. All panels show mean values ± SEM. Asterisks highlight significant differences
at p < .05.

of such mechanisms account for omission responses changes in wave V (thought to arise from the inferior col-
(Wacongne et al., 2012; Schröger et al., 2014). The lack liculus) or earlier potentials (Slabu et al., 2010; Grimm
of omission responses in the auditory brainstem in either et al., 2011). There is conflicting evidence for the larger
sequence presentations conditions supports the notion question whether brainstem processing is affected by
that the auditory brainstem faithfully encodes short-term cognitive and task demands such as attentional focus
acoustic properties of a stimulus (Galbraith et al., 1995; and listening context (Chandrasekaran et al., 2009; Skoe
Skoe and Kraus, 2010a), but does not contribute and Kraus, 2010b; Lehmann and Schönwiesner, 2014)
significantly to extracting regularities in sound input and or not (Varghese et al., 2015).
to predicting future input based on such regularities. This In the present paper, omission duration and frequency
hypothesis is supported by previous results. Two previous was suitable to elicit cortical omission responses.
studies examined ABRs in a predictive coding paradigm However, because auditory cortex tends to respond
and found no evidence for responses evoked by sound better to slower amplitude modulations than auditory
 A. Lehmann et al. / Neuroscience 337 (2016) 306–314
brainstem nuclei (Giraud et al., 2000), it is possible that
omissions in faster stimulus sequences would have trig-
gered brainstem omission responses.
Consistency of brainstem responses depends on
sequence regularity
Even if cognitive activity changes brainstem processing in
the short term, such a modulation is likely mediated by
efferent projections (Tzounopoulos and Kraus, 2009)
which modulate ongoing subcortical activity, but may not
generate activity, and would thus be insufficient to pro-
duce overt responses to omissions. Our finding of higher
consistency of the brainstem response to sounds pre-
sented in an isochronous sequence indicates that, while
no overt omission response was present, the responses
to sound stimuli were modulated by sequence regularity.
To rule out that the lower consistency in the irregular con-
dition is due to bottom-up adaptation effects, we used a
worst-case scenario computation of consistency, and
showed that this entrainment effect cannot be explained
solely by the variability in SOA across trials.
Higher response consistency has been associated
with more robust processing of sounds and increased
temporal precision of encoding (Schatteman et al.,
2008; Anderson et al., 2012). Studies in animals suggest
that thalamic neurons entrain to repetitive sound stimula-
tion at low repetitions rates (Gao et al., 2009). It may thus
be that a lower rate would have resulted in measurable
omission responses. Recording brainstem responses to
sequences with long SOA is difficult due to the large num-
ber of repetitions required for sufficient signal quality. It
has been demonstrated that cortical responses to an
unexpected offset of regular sequences are faster when
the sequence is attended than during passive listening
(Yamashiro et al., 2009; Andreou et al., 2015), however,
this was not the case for isochronous sequences. We
thus think that attending to the sequences would likely
not have increased the likelihood of measuring an overt
omission response.
Cortical responses are modulated by sequence
regularity
Cortical event-related responses are modulated by the
temporal structure of sound sequences (Luck, 2005;
Lakatos et al., 2008; Schwartze et al., 2011). Here we
found cortical steady-state-evoked potentials (SSEPs)
with clear spectral amplitude at the average rate of the
stimulation in the isochronous sequence but not in the
irregular sequence. Such sustained activity in response
to isochronous sequences may have contributed to the
observed increased intertrial consistency in brainstem
response, potentially through corticofugal connections
(Tzounopoulos and Kraus, 2009). A sustained cortical
oscillation at the beat frequency may underlie several pre-
vious results (Arnal and Giraud, 2012; Merchant et al.,
2015), including that sounds falling on a beat of a rhythmic
tone sequence evoke higher-amplitude event-related
potentials (Brochard et al., 2003; Abecasis et al., 2009;
Potter et al., 2009; Winkler et al., 2009; Schaefer et al.,
2011; Tierney and Kraus, 2014), evoked and induced
311
beta oscillations (Iversen et al., 2009; Fujioka and
Trainor, 2012), and gamma oscillations (Snyder and
Large, 2005; Zanto et al., 2006). Our study clearly shows
a difference in cortical SSEPs between isochronous and
irregular conditions, but the relationship between sus-
tained cortical oscillation and parametric variations of tim-
ing variability remains to be investigated.
Differential adaptation mechanisms in cortex and
brainstem
The observed larger responses to stimuli after an
omission in both the cortical and subcortical recordings
may be due to adaptation (Thompson and Spencer,
1966; Ulanovsky et al., 2003). Neural adaptation at the
brainstem level has been observed in the transient audi-
tory brainstem response to clicks (Lasky, 1997; Hood,
1998) but for the first time it is reported here in the FFR.
This is not trivial since the FFR is not predictable from
the response to click and tones and may involve distinct
neural generators (Galbraith et al., 1998; Palmer and
Shamma, 2004; Johnson et al., 2008; Skoe and Kraus,
2010a).
Subcortical involvement in beat processing
The aforementioned mechanisms – response to omitted
stimuli, modulation by sequence regularity and
adaptation – differentially observed in cortical and
brainstem responses, underlie the capacity to extract
and process beat/rhythm, and therefore point to a
selective involvement of the brainstem (Zanto et al.,
2006). However the protocol used in the current study
does not allow us to elaborate on such processes
because our SOA (90 ms period) was below the range
of human tempo perception (200 ms/300 BPM –
1000 ms/60 BPM: Drake and Botte, 1993).
In sum, our results suggest that stimulus omissions in
fast sound sequences do not trigger measurable omission
responses in the human ABR. The human auditory
brainstem response selectively exhibits relevant
properties related to beat extraction (sequence
regularity modulation, adaptation).
Acknowledgments—This work was funded by the National
Science and Engineering Council of Canada. We thank Dr. Nina
Kraus for providing the /da/ stimulus. MS was supported by a
career grant from the Fonds de Recherche du Quebec – Sante.
DJA was supported by an undergraduate research stipend from
National Science and Engineering Council of Canada.
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