Temporal regularity within sensory input, can be defined as a uniformly structured
and recurring stimulation. Perceiving temporal regularity is integral to effectively
perceiving the world around us, such as in speech and music perception. Indeed, natural
environments constantly present our perceptual systems with different forms of temporal
regularities and rhythms. Efficient sensitivity to temporal changes not only allows
us to maintain a coherent perception of our experiences, but importantly, also allows
us to build expectations and predict future events (Gutschalk et al., 2002; Nobre
and van Ede, 2017). Previous work investigating the underlying neural mechanisms of
temporal pattern perception have focused on neural synchronization (NS). This is defined
as the ability of neural oscillations to synchronize with temporal regularity in external
stimuli (Lakatos et al., 2008; Henry and Obleser, 2012), further suggesting that temporal
regularity boosts neural activity at the same frequency as that of the external stimulus.
This externally-synchronized neural activity can then be used to predict future auditory
activity (Nobre and van Ede, 2017). More recently, the role of sustained activity
(SA) has also been investigated in temporal regularity perception, using electroencephalography
(EEG) and magnetoencephalography (Barascud et al., 2016; Southwell and Chait, 2018).
For instance, detection of regularity in short auditory sequences is demarcated by
increased sustained low-frequency evoked magnetoencephalographic activity, which occurs
irrespective of the temporal structure (Barascud et al., 2016). The precise relationship
between NS and SA is not fully understood. One suggestion is that NS allows the recognition
of auditory patterns, while SA subsequently allows the processing of this information
in the higher order brain regions. A recently published study by Herrmann and Johnsrude
(2018) examined the relationship between NS and SA in the processing of auditory temporal
patterns using EEG.
To investigate whether NS and SA co-occur, the authors used sequences of tones arranged
in random and regular frequency patterns; in this case, coherent frequency modulation
(FM), similar to previous experiments on SA (Barascud et al., 2016; Southwell et al.,
2017). EEG recordings were performed whilst participants listened to auditory rhythms
in four conditions: one contained no temporal regularity, whereas the others contained
a temporal pattern. In order to study both neural processes concomitantly, two implementations
were made: two of the rhythms had a sinusoidal oscillatory pattern, to observe synchronization
(2.5 and 5 Hz sinusoidal FM), while high-pass filtering was omitted in studying SA,
because it is a low frequency signal (Barascud et al., 2016).
Whilst the first experiment replicated previous results of increased SA when regularity
occurs (Barascud et al., 2016; Southwell et al., 2017), the main finding was that
both SA and NS showed increased activity, indicating the first evidence of the co-occurrence
of these two processes. Herrmann and Johnsrude (2018) also showed a correlation between
the effect of regularity on SA and inter-trial phase coherence, concluding that these
signals are not independent. This assumption was made by the authors despite a significant
correlation for only one condition, with sinusoidal oscillatory patterns for the frequency
of 2.5 Hz, and no correlation for 5 Hz. Taking this difference into account, we concluded
that the interdependency between the signals could be related to the frequency of
the stimulus—an important distinction to understand the extent to which NS and SA
can be dissociated. Further experimentation replicating this experiment using a wider
range of frequencies is necessary to elucidate this relationship.
Interestingly, the finding that NS is more sensitive to regularity imposed by a coherent
frequency modulation in sounds, compared to SA, indicates an indirect relationship
between the two processes. This observation led the authors to investigate the extent
to which the attentional state of the participant affected NS and SA in detecting
temporally regular patterns. To address this, participants either attended to sounds
with and without regularity (in an auditory duration categorization task) or were
instructed to ignore the sounds and perform a visual multiple object tracking (MOT)
task. Increased SA was observed when participants performed either a MOT task or an
auditory task for sounds without temporal regularities, suggesting that attentional
demands produced an increase in the response. Sohoglu and Chait (2016) have demonstrated
that increased SA, due to regular patterns, is independent of attention. However,
in their experiments they used a visual comparison task, while in the present MOT
task the participant had to track and remember the target position. We hypothesize
that the MOT task is more attentionally and/or even more cognitively demanding (Cavanagh
and Alvarez, 2005). Furthermore, as the same participants made judgments in both the
auditory and visual tasks in alternating blocks, the cognitive demands required to
solve the MOT task could at least in part also influence the SA during the auditory
task. Whether the rise in SA is due to an increase facilitated by the attentional
state, or rather the recruitment of different cognitive processes for the task, [akin
to observations made by Southwell et al. (2017)] remains to be clarified.
Additionally, whereas regularity-related NS activity was unaffected by visual or acoustically
demanding tasks, increased SA due to regularity was only observed when participants
attended to the auditory stimuli. We hypothesize that cognitive processes, such as
working memory taking part during the MOT task, have an increased demand for computational
resources, compared with the auditory task alone and could interfere with the sensitivity
of the SA to detect regularities, compared with NS. To clarify this, we propose the
use of discrimination tasks for both modalities. Interestingly, Barascud et al. (2016)
demonstrated an interaction between the primary auditory cortex, the hippocampus and
inferior frontal gyrus during regularity detection by SA. We suggest that the participation
and activation of these areas during cognitive processes, like attention and working
memory, could help to explain increased SA as well as the difference in NS.
It is noteworthy that evidence for regularity-related SA activation was only found
when attention was applied during the auditory task and not during the visual task.
Interpretation of this finding however, is confounded by the fact that the authors
observed an important SA difference even prior to the transition to the auditory-visual
comparison. Two possible interpretations for the observed differences between the
auditory and visual decoy tasks could be that attending to a cognitively demanding
visual task, may consequently result in the suppression of regularity-based sustained
activity. Alternatively, attending to sounds could result in the enhancement of regularity-based
sustained activity. Evidence that a visual task is able to impair auditory pattern
detection could also suggest prioritization of visual information with respect to
auditory information. Although Herrmann and Johnsrude (2018) suggest modality differences
between audition and vision, this difference is only documented for SA—a process that
has already been differentiated from NS. We propose an alternative hypothesis that
NS and SA rely on different underlying mechanisms thereby explaining the modality
of differences evidenced here.
These results provide novel evidence on NS and SA in detecting temporal regularities.
Specifically, that these processes co-occur and are differentially affected by cognitive
demands. The authors suggest that NS and SA reflect neural processes at different
hierarchical levels, however these results alone do not inform us about the underlying
neural mechanisms of these processes. It may be informative to pair EEG with neuroimaging
methods, with high spatial resolution, such as functional magnetic resonance imaging,
to differentiate the brain regions that mediate temporal pattern processing. Furthermore,
whilst NS and SA are plausibly linked through their sensitivity to auditory regularity,
evaluating the differences between SA and NS in influencing temporal pattern perception,
in a behavioral sense, is also an important feat. We agree with the authors' interpretation
that NS is likely to suggest more sensory-driven and automatic responses to temporal
patterns, rather than SA, which is thought to be influenced by more cognitively-mediated
processing. Causal perturbation of sensory cortices using Transcranial Magnetic Stimulation
(TMS), or alternatively through a dual-task paradigm where one task recruits attentional
mechanisms and the second employs cognitive processing (that excludes specific attentional
processing), would clarify this interaction.
The findings of Herrmann and Johnsrude (2018) clarify at least in part the functional
dependence between two different neural responses, NS and SA, in the processing of
auditory temporal patterns. By employing coherent FM patterns and parametrically manipulating
the degree of phase coherence, it was found that both NS and SA were modulated and
co-occur. This novel result indicates that there are concurrent neural signals measuring
temporal structure in sounds. Importantly, NS demonstrated increased sensitivity to
the degree of FM phase coherence. Additionally, it was found that NS to auditory temporal
regularity still occurred, despite co-occurring visual demanding distractors. However,
SA was not sensitive to the same auditory regularity, which may reflect different
stages of regularity processing. These results suggest that while temporal patterns
induce neural activity in both responses of NS and SA, these patterns of activity
are not identical and are in fact, modulated differently by cognitive demands.
Author Contributions
AM and LGC both contributed to the conception and writing of this review. AM prepared
the draft for submission.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.