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Neuroscience 337 (2016) 306–314

TRACING THE NEURAL BASIS OF AUDITORY ENTRAINMENT


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

http://dx.doi.org/10.1016/j.neuroscience.2016.09.011
0306-4522/Ó 2016 IBRO. Published by Elsevier Ltd. All rights reserved.

306
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 measured the spectral amplitude of frequency bins from


105 Hz to 135 Hz (corresponding to the stimulus F0). In
omis
da da sion
da silence addition, we measured the root mean square amplitude
(RMS) for each FFR in the same time window of 5 ms
40ms 50ms 40ms 160 x SOA to 50 ms after stimulus onset. Furthermore, we measured
SOA = 90ms
trial-by-trial consistency of the responses to the sound
stimuli in the isochronous and irregular conditions by com-
B Irregular condition
puting correlation coefficients between even- and odd-
numbered trials (Hornickel and Kraus, 2013). Response
omis consistency was found to be lower in non-bilingual adults
da da sion da silence
(Krizman et al., 2014), and poor readers (Hornickel and
min.17ms mean 50ms max. 87ms 160 x SOA Kraus, 2013). It has been interpreted as increased neural
variability as shown in experimental-animal models
Fig. 1. Presentation of stimuli in isochronous and irregular (Centanni et al., 2014).
sequences. Both sequences contain /da/ syllables, infrequent syllable
Spectral amplitude measures were entered into two
omissions, and blocks of 160 silent SOAs. (A) In the isochronous
condition stimuli were presented with an SOA of 90 ms (ISI 50 ms). different repeated-measures ANOVAs with factors
(B) In the irregular condition the SOA varied between 57 and 127 ms ‘‘sequence regularity” (isochronous or irregular) and
with an average of 90 ms, and the ISI varied between 17 ms and stimulus type: the first ANOVA compared omissions and
87 ms with an average of 50 ms. silent blocks to check for effects of entrainment
(increased response amplitude within sound sequence),
and Makeig, 2004), erplab (Lopez-Calderon and Luck, the second ANOVA compared prior /da/ and post /da/
2014) and letswave (http://amouraux.webnode.com/lets- stimuli to check for effects of adaptation (increased
wave) toolboxes, as well as custom Matlab scripts. Fol- response amplitudes after omissions). The same
lowing published procedures, responses were bandpass procedure was applied to the RMS measures.
filtered into a high- or low-frequency band in order to iso- Response consistency was compared across conditions
late subcortical and cortical components of the EEG sig- in a repeated measures ANOVA with factors ‘‘sequence
nal (Musacchia et al., 2008; Skoe and Kraus, 2010a; regularity” (isochronous or irregular) and stimuli type
Lehmann et al., 2015). For the subcortical response, data (prior /da/ or post /da). Post-hoc t-tests were used to
from a Fpz were re-referenced to the seventh cervica detect significant differences at 5% alpha level.
(C7), as this montage has been shown to elicit a brain-
stem FFR with a better signal-to-noise ratio than the tradi- Cortical Event-Related potentials and steady-state-
tional montage (Cz referenced to mastoids) used for evoked potentials. To analyze cortical responses, EEG
auditory-evoked potentials (King and Sininger, 1992; signals from electrode Cz were re-referenced to the
Krishnan et al., 2005; Cousineau et al., 2015). For the cor- average signal recorded from the left and right mastoid,
tical response, recording from the vertex electrode (Cz) bandpass-filtered between 0.1 Hz and 50 Hz, and
was referenced to linked mastoids, as done for the corti- downsampled to 256 Hz.
cal components by a previous studies that simultaneously In order to compute event-related potentials, epochs
recorded cortical and subcortical activity (Musacchia spanning from -100 to 600 ms relative to the onset of
et al., 2008). omissions and relative to the onset of /da/ stimuli. We
selected /da/ stimuli that were preceded and followed by
Brainstem frequency-following responses. To analyze four other /da/ stimuli to exclude inconsistent responses
auditory brainstem responses, continuous EEG due to adjacent omissions or silent trials. Epochs
recordings from the hairline electrode (Fpz) were re- containing artifacts were rejected by visual inspection
referenced to C7, bandpass-filtered off-line between and by using EEGLAB’s automatic iterative rejection
100 Hz and 2 kHz, and split into epochs spanning from procedure with an initial threshold of five standard
20 ms to +70 ms relative to stimulus onset (Krishnan deviations (Delorme and Makeig, 2004). Individual peak
et al., 2005; Skoe and Kraus, 2010a). Epochs containing amplitudes of the most prominent negative peak and the
artifacts were rejected by visual inspection and by using most prominent positive peak were extracted from
eeglab’s automatic iterative rejection procedure with an responses to omissions in the isochronous and irregular
initial threshold of five standard deviations (Delorme and conditions and the peak-to-peak amplitude differences
Makeig, 2004). FFRs were obtained by averaging epochs were computed and compared between conditions with
separately for each condition and trial type: responses to / a t-test.
da/ stimuli preceding an omission (‘‘prior /da/”), those just We also computed steady-state-evoked potentials
after an omission (‘‘post /da/”), the omissions themselves (SSEPs) to capture neural entrainment to the
(‘‘omission”), and silent trials excluding the first 50 trials of presentation rate of the stimuli (11.1 Hz). For each
each silent block (‘‘silence”). participant, 15 epochs of 33-s time-locked to the onset
Because the sustained period of the FFR reflects of a /da/ stimulus were extracted from the isochronous
phase-locking to characteristics of the stimulus and irregular conditions such that no epoch contained
waveform (Song et al., 2008; Skoe and Kraus, 2010a), silent trials. Those epochs were averaged and
we computed a fast Fourier transform (FFT) of each transformed into the frequency domain using a FFT.
FFR between 5 ms and 50 ms after stimulus onset and The signal-to-noise ratio of the frequency-domain signal
A. Lehmann et al. / Neuroscience 337 (2016) 306–314 309

was increased by subtracting, for each frequency bin, the Cortical SSEP. In the cortex, we found a clear peak in
average amplitude measured at three neighboring the spectral amplitude at the repetition rate of the stimuli
frequency bins (Nozaradan et al., 2011). The spectral in the isochronous sequence, but not in the irregular
amplitude at the presentation rate was compared sequence (t13 = 4.261, p = <.05; see Fig. 3C).
between isochronous and irregular conditions using a
two-tailed paired-sample t-test. 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
RESULTS
higher spectral amplitude at the fundamental frequency
Cortex but not brainstem responds to omitted of the stimuli (F1,13 = 12.202, p = <.05, isochronous
sounds sequence: t13 = 3.160, p = <.05, irregular sequence:
t13 = 2.284, p = <.05) and higher RMS amplitude
In the cortex, we found a clear evoked response to
(F1,13 = 59.039, p = <.05, isochronous sequence:
omitted stimuli in both regular and jitter sequences
t13 = 4.123, p = <.05, irregular sequence:
(Fig. 2A). Negative-to-positive peak-to-peak amplitude
t13 = 7.863, p = <.05).
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 DISCUSSION
to omissions in either condition, and brainstem activity in To trace entrainment-related processes along the
omission trials did not differ from activity in the silent auditory pathway, we simultaneously recorded cortical
intervals (Repeated measures ANOVA, interaction effect and subcortical responses to isochronous and irregular
of condition* stimuli type, F1,13 = 1.395, p > .05, sequences of sounds containing sporadic omissions.
Fig. 3B). Sounds flanking omissions evoked clear We asked whether early brainstem centers respond to
responses in both conditions (Fig. 2B). Note that here infrequent sound omissions and whether presentation
the term ‘‘omission” is used generally to address cortical regularity modulates the auditory brainstem response.
and brainstem activity obtained from the presentation of We observed responses evoked by omissions in the
an omitted stimulus, and therefore should not be auditory cortex, but not in the brainstem. However,
confused with the terms omission N1 or omission MMN brainstem responses showed higher inter-trial
obtained from other protocols (Yabe et al., 1997; consistency when stimuli were presented in an
SanMiguel et al., 2013), because cortical omission isochronous sequence than in an irregular sequence.
responses may indicate several high-level mechanisms, We also observed a steady-state-evoked response at
such as predictive coding (see introduction), but brain- the average presentation rate in the cortex during
stem omission responses, if they exist, may indicate isochronous, but not jittered presentation. Lastly we
other, perhaps lower-level, mechanisms. found stronger adaptation in the cortex and brainstem of
responses to stimuli that preceded omissions than those
that followed omissions.
Enhanced brainstem and cortical encoding of
isochronous sound sequence Cortex, but not brainstem responds to omitted
sounds
Despite the lack of evoked responses to omissions in the
brainstem, we found effects of stimulus sequence We did not observe responses evoked by omissions in
regularity. The intertrial consistency of brainstem the brainstem, even though auditory cortex responded
responses to sounds presented in the isochronous strongly to these omissions (Busse and Woldorff, 2003;
sequence was higher than that in the irregular sequence Zanto et al., 2006; Honing et al., 2012). Cortical omission
(repeated measures ANOVA, main effect of condition, responses showed the expected latency and morphology
F1,13 = 40.504, p < .05, Fig. 3A). In order to test (Bendixen et al., 2012), and were larger in the isochro-
whether this effect could simply be explained by the nous than in the irregular sequence, likely because
length of the prior silent interval, we compared the entrainment and the build-up of temporal expectancy
consistency obtained in the irregular condition to a increases with sequence regularity (Schwartze et al.,
worst-case scenario where each of the two bins used to 2011).
compute consistency were composed of the larger and Similar findings were reported by Oceák and
smaller SOA trials respectively. This worst-case colleagues, who found that the amplitude of standard
scenario consistency measure did not differ significantly minus omission responses was significantly higher for
from the originally computed one (t26 = 0.1013, isochronous SOA compared to random SOA (Oceák
p = 0.92). et al., 2006). Although the interpretation of omission
Additionally, sound stimuli following omissions (‘post / responses is still under debate (Predictive coding:
da/’) showed higher consistency than stimuli preceding Cornella et al., 2015; regularity violation: Näätänen et al.,
omissions (‘prior /da/’) (main effect of stimulus type, 2007; sound offset rebound: Horváth et al., 2010; loudness
F1,13 = 42.942, p = <.05, isochronous sequence: changes: Oceák et al., 2006; Fishman, 2014;), there is
t13 = 6.187, p = <.05, irregular sequence: mounting evidence for predictive coding in the auditory
t13 = 3.802, p = <.05). 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) 306–314 311

brainstem nuclei (Giraud et al., 2000), it is possible that beta oscillations (Iversen et al., 2009; Fujioka and
omissions in faster stimulus sequences would have trig- Trainor, 2012), and gamma oscillations (Snyder and
gered brainstem omission responses. Large, 2005; Zanto et al., 2006). Our study clearly shows
a difference in cortical SSEPs between isochronous and
Consistency of brainstem responses depends on irregular conditions, but the relationship between sus-
sequence regularity tained cortical oscillation and parametric variations of tim-
ing variability remains to be investigated.
Even if cognitive activity changes brainstem processing in
the short term, such a modulation is likely mediated by Differential adaptation mechanisms in cortex and
efferent projections (Tzounopoulos and Kraus, 2009) brainstem
which modulate ongoing subcortical activity, but may not
generate activity, and would thus be insufficient to pro- The observed larger responses to stimuli after an
duce overt responses to omissions. Our finding of higher omission in both the cortical and subcortical recordings
consistency of the brainstem response to sounds pre- may be due to adaptation (Thompson and Spencer,
sented in an isochronous sequence indicates that, while 1966; Ulanovsky et al., 2003). Neural adaptation at the
no overt omission response was present, the responses brainstem level has been observed in the transient audi-
to sound stimuli were modulated by sequence regularity. tory brainstem response to clicks (Lasky, 1997; Hood,
To rule out that the lower consistency in the irregular con- 1998) but for the first time it is reported here in the FFR.
dition is due to bottom-up adaptation effects, we used a This is not trivial since the FFR is not predictable from
worst-case scenario computation of consistency, and the response to click and tones and may involve distinct
showed that this entrainment effect cannot be explained neural generators (Galbraith et al., 1998; Palmer and
solely by the variability in SOA across trials. Shamma, 2004; Johnson et al., 2008; Skoe and Kraus,
Higher response consistency has been associated 2010a).
with more robust processing of sounds and increased
temporal precision of encoding (Schatteman et al., Subcortical involvement in beat processing
2008; Anderson et al., 2012). Studies in animals suggest
that thalamic neurons entrain to repetitive sound stimula- The aforementioned mechanisms – response to omitted
tion at low repetitions rates (Gao et al., 2009). It may thus stimuli, modulation by sequence regularity and
be that a lower rate would have resulted in measurable adaptation – differentially observed in cortical and
omission responses. Recording brainstem responses to brainstem responses, underlie the capacity to extract
sequences with long SOA is difficult due to the large num- and process beat/rhythm, and therefore point to a
ber of repetitions required for sufficient signal quality. It selective involvement of the brainstem (Zanto et al.,
has been demonstrated that cortical responses to an 2006). However the protocol used in the current study
unexpected offset of regular sequences are faster when does not allow us to elaborate on such processes
the sequence is attended than during passive listening because our SOA (90 ms period) was below the range
(Yamashiro et al., 2009; Andreou et al., 2015), however, of human tempo perception (200 ms/300 BPM –
this was not the case for isochronous sequences. We 1000 ms/60 BPM: Drake and Botte, 1993).
thus think that attending to the sequences would likely In sum, our results suggest that stimulus omissions in
not have increased the likelihood of measuring an overt fast sound sequences do not trigger measurable omission
omission response. responses in the human ABR. The human auditory
brainstem response selectively exhibits relevant
properties related to beat extraction (sequence
Cortical responses are modulated by sequence regularity modulation, adaptation).
regularity
Cortical event-related responses are modulated by the Acknowledgments—This work was funded by the National
temporal structure of sound sequences (Luck, 2005; Science and Engineering Council of Canada. We thank Dr. Nina
Lakatos et al., 2008; Schwartze et al., 2011). Here we Kraus for providing the /da/ stimulus. MS was supported by a
career grant from the Fonds de Recherche du Quebec – Sante.
found cortical steady-state-evoked potentials (SSEPs)
DJA was supported by an undergraduate research stipend from
with clear spectral amplitude at the average rate of the National Science and Engineering Council of Canada.
stimulation in the isochronous sequence but not in the
irregular sequence. Such sustained activity in response
to isochronous sequences may have contributed to the
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(Accepted 8 September 2016)


(Available online 22 September 2016)