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Index
I.
II.
III.
IV.
Conclusions
V.
References
I.
Alpha oscillatory activity was the firstly discovered (Millet, 2001) and is the most prominent
neural rhythm recorded in the human brain (Klimesch et al, 1999). Despite his remarkably antique
origin, the number and extent of its competencies is object of a lively and vigorous discussion, and the
study of alpha oscillatory activity has gained great popularity over the last decade (Payne and
Sekuler, 2013).
As it is widely known, alpha oscillations were initially thought to reflect cortical idling (Adrian
and Matthews, 1934). However, this view was later began to be questioned (Pfurtscheller et al, 1996),
and some authors reported the appearance of alpha activity during internal processing which were
supposed to not to require attention from the environment (Ray and Cole, 1985), reflecting the first
observations of alpha activity over disengaged areas. Posterior research by Pfurtscheller (2001),
Klimesch (1996) and many others described in more detail the appearance of alpha rhythm eventrelated desynchronization (ERD) in occipital areas during visual information processing, whereas
event-related synchronization (ERS) appears in inactive areas.
The current stage in literature was in part established by a second series of articles which
started to talk about these relations in a generalized way, and which benefited from the accumulated
evidence (e.g Jensen et al, 2002; Sauseng et al 2005) in support of alpha oscillatory activity as a
mechanism to engage and disengage areas from activity (Klimesch et al, 2007; Jensen and Mazaheri,
2010). In particular, the landmark study by Klimesch et al (2007) pointed out that upper-alpha band
frequency power disappearance is particularly coupled with active cognitive processing. Additionally,
both articles stressed that alpha activity can be modulated in a top-down fashion, representing
functional inhibition.
This alpha inhibitory framework has posteriorly gained substantial empirical support which
has increased over the last years (Hanslmayr et al., 2007; van Dijk et al., 2008; Sauseng et al, 2009;
Handel et al 2011; Haegens et al 2011 & 2012; Roux et al, 2012; Klimesch et al, 2012). Many of these
studies used working memory paradigms (Jensen and Mazaheri, 2010), showing how alpha activity
disappeared in engaged areas and reinforced in pertinent ones, or suddenly reappeared when taskirrelevant stimuli appeared.
However, although evidence appears to be extensive, literature regarding alpha oscillations
has been in occasions chaotic and unclear in the range of processes in which alpha inhibition takes
place. It is frequent to find a lack of agreement in to what extent this phenomenon is present in
working memory or attentional tasks (Palva and Palva, 2007). This may be in part caused by the lack
of replicability in some aspects of the framework described by Klimesch (2007), perhaps due to a
certain tendency in finding new contexts and applications instead of securing the grounds.
In the following sections we will try to present a coherent and fluid view of the alpha inhibitory
role in a WM environment. WM tasks normally follow a structured set of processes; the information
needs to be adequately perceived and encoded, then the internal copy of the items presented needs
to be maintained and finally these items will be used for a comparison or perhaps a manipulation task
(Haenschel and Linden, 2011). The relatively developed stage of WM theory (Baddeley,2003) and its
position as binding point between perceptual and cognitive domains makes of WM an excellent
framework to make the most of EEG and MEG measurements, and current electrophysiological
models of WM are being developed (Roux and Uhlhaas, 2014).
II.
Once this general inhibitory character of alpha activity has been established, its significance
can vary in function of when these oscillations appear along the timeline (see graph below) and in
which localizations, as these sites may be differently relevant for the WM task (Klimesh et al, 2007).
Hence, alpha power modulations might reflect enabling/disabling of processing at the beginning of a
task as a product of cueing (pre-stimulus, Klimesch et al, 2007 or Payne and Sekuler, 2013), selective
suppression of processing in situations in which irrelevant and relevant information appear together
(dynamic encoding, e.g Freunberger, 2009 or Horschig et al, 2014) or perhaps protection of the held
items against distractors in the maintenance phase (rejection of intruders or distractors, Bonnefond
and Jensen, 2012).
Figure 1: The below graph provides an overview of the following sections. Image (left) from Payne and Sekuler
(2013), which provides some examples of pre-stimulus alpha power modulation in somatosensory, ortographic, auditory or
visual tasks. Image (right) from Freunberger et al, (2009) will be discussed in the following. Flow graph created by author.
CUEING
Encoding
Retention
Readiness
Selective
Processing
Rejecting
intruders
Freunberger et al
2009
Pre-encoding
Stimulus
onset
Enabling/disabling
Klimesch et al 2007
Timeline
So far, the vast majority of up to date literature has considered alpha power or alpha
amplitude as default elements (Palva and Palva, 2007) and we will do so as well. Therefore, unless
specified we will be always referring to alpha activity as amplitude modulation, although in the closing
sections we will pay attention to other components such as phase coupling or locking.
Enhancement of alpha activity over task-relevant areas may appear at the beginning of a task
when the appearance of an irrelevant item is announced by cueing (Rohenkohl and Nobre,2012;
Payne and Sekuler, 2013 for a good review) and it is not required to be processed, normally known as
suppression of processing by alpha ERS. Conversely, alpha power can drop as a result of cued
relevant items appearance, therefore enabling processing through alpha ERD in relevant places for
the task (Klimesch et al, 2007).
This modulatory role extends from pre-encoding to encoding phases, as it can happen either
in the middle of a task or at the beginning of a task when explicit cueing is provided. More importantly,
this process reflects the control of the subject upon its attentional resources (Wilsch et al, 2014) and
can be understood as an electrophysiological correlate of attentional top-down management
(Klimesch, 2012). Impairments in this process would entail deficiencies in WM tasks as suppression is
a key skill in working memory functioning (BelanVogel et al 2005). Clear evidence of this role can be
found at Haegens et al (2011) where a correlation between pre-stimulus alpha suppression and
performance in a somatosensory discriminatory were found in the somatosensory cortex for the
attended side, in which stimuli appearance was expected. As Payne and Sekuler (2013) state, correct
discrimination increases as pre-stimulus alpha decreases, and accuracy in the task and speed of
response were both correlated with the alpha degree. Additionally, alpha presence varied when the
reliability of the cueing was modified, suggesting a strong top-down modulation.
More sophisticated evidence of cueings and temporal expectations relevance can be found at
the study by Wilsch et al (2014) in which three different types of cueing were used (early,
neutral/uninformative and late) in an auditory delayed-to-match working memory task. This task
consisted in the comparison of two syllables, identifying if the first consonant used was the same in
both cases or different. Items were embedded in a sort of background noise, providing a complex
presentation, perhaps resembling a conversation in a noisy environment.
The authors successfully reasoned that the noise would increase the need of functional
inhibition, thus boosting the presence of alpha rhythm. Critically, temporal expectancy manipulated by
cueing effectively modulated alpha power, which strategically dropped when the task-relevant
information (syllable) was about to be presented knowing when to listen (figures A and B in the
below illustrations). Trials in which a long cueing was provided revealed the higher drops in alpha
inhibition and yielded the best performances (also in Mazaheri et al,2010 and Hanslmayr et al, 2007,
or Obleser and Weisz, 2012 for an auditory example) Moreover, and as can be seen in the illustration
below (figure C), alpha modulations (defined by the difference in power between neutral and cued)
predicted accuracy in the task.
In a more complex way, the remarkable study by Horschig et al (2014) holds an special
importance among the alpha modulatory activity literature. In this experiment the subjects were
exposed to a task in which the to-be-attended hemi field will change without explicit cueing of it.
However, with each trial in which the attended hemi field remained the same the implicit probabilities
of a change were higher, so the subjects were dedicating an increasing amount of covert attention to
the opposite hemi field. This top-down covert attention was operatized by the amount of anticipatory
posterior alpha, which demonstrated to be correlated with performance.
Some researchers have attached to this activity an additional role, ensuring the correct
distribution of resources (Tuladhar et al, 2007; Jensen and Mazaheri, 2010; Payne and Sekuler,
2013). Additionally, Jensen and Mazaheri (2010) proposed a model of brain communication and
information routing based on the presence of these oscillations, which in theory must help to distribute
the information across different areas and subsystems. Evidence in support of this model can at best
be qualified of circumstantial.
Therefore, alpha activity is also key for retaining and maintaining the fidelity of the items in
the WM retention against the possible intrusions. This property is capital as intrusion of task-irrelevant
items is a major cause of failures in WM, particularly in the aged population (Zanto and Gazzaley,
2009).
III.
One of the fundamental problems concerning literature about alpha inhibition in pre-encoding
and dynamic encoding roles is how to establish an appropriate cueing to avoid possible confounds.
Alpha suppression or alpha ERD can appear due to incoming activity in a bottom-up fashion as an
stimulus in being processed, as the stimulus simply appear (Ray and Cole, 1985; Klimesch et al,
1999). Thus, cue processing (or stimulus appearance, for that matter) and cues top-down effect can
mix up if cueing and stimulus onset are too close. According to Klimesch et al (2012) alpha
suppression is expected between 200 500 ms after stimulus onset whereas Rihs et al (2007) says
that alpha ERD as a result of cueing is expected to appear at 400-600 ms after stimulus onset,
revealing an overlap between the two modalities.
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11
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Amplitude
To-be-remembered
amplitude (a)
Phase
(PLI*)
(7-12Hz)
Not-to-be-remembered
amplitude (a)
(PLI*)
(7-12Hz)
*Phase Locking Index -Figure 10: Adapted from Freunberger et al, 2009, made by author.
Klimesch et al (2012) shaped further the Fruenbergers framework of amplitude and phase
suggesting that amplitude manages the width of the encoding slots. This function of amplitude will be
however a question of grading because while in a moderate manner amplitude will serve as referred,
amplitude in the higher extent would inhibit any processing. Is in this sense, phase angle will be
relevant at the start of the information encoding in its interplay with the P1 component.
This hypothesis presented by Klimesch et al (2012) has yet to find solid experimental support,
to the best of the authors knowledge. However, Zanto et al (2014) found promising results when
embracing this framework in an experiment using a WM task context. Briefly, they found improved
performance while TMS pulses were delivered during the peak of the alpha oscillation compared to
when it were delivered in a trough before stimulus onset (illustration above provides a short rationale,
peak must coincide with P1 component appearance). Additional evidence that have taken advantage
of phase can be found in Roux et al (2012), in which interareal phase synchronization was found to
be relevant for WM maintenance.
Perhaps, some of the studies that lack of coherence within the alpha inhibition theory will find
some more sense when phase components are also take into account. Phase measurements might
also prove to be profitable in their integration with cross-frequency models and nested oscillatory
paradigms. To discuss these models will be well beyond the objective of this essay, although the
interested reader could find useful Roux and Uhlhaas (2014) in the WM domain. In a last remark,
studies combining MRS spectroscopy and EEG are suggestive, as alpha is as well thought to be
evoked with the help of inhibitory interneurons (Buzsaki and Chrobak, 1995).
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Conclusions
There are several ways in which alpha oscillations contribute to successful performance in
WM tasks by exerting its inhibitory role. The suppression of irrelevant information in early stages of
processing saves valuable resources needed for the correct encoding of pertinent items and posterior
operations. Also, alpha activity supports the rejection of distracters during retention and maintenance
stages protecting relevant items from external disruption, function which impairment has
demonstrated to be critical for WM deficits in several diseases.
All in all, the exact mechanisms underpinning alpha inhibition are yet to be clarified, and the
emergence of other components like phase coupling promises to shed light upon this matter. The
subsequent shaping of alpha-band activity by measuring phase and amplitude in a coherent
framework, together with further studies that could provide finer spatial specificity and the addition of
alpha activity to studies seeking to define cross-frequency networks sets an exciting moment for the
research community. This scenario promises to generate powerful tools for the understanding of
perceptual and cognitive abilities, which applications will have a predictable application in disease
models.
V.
References
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man. Brain, 57(4), 355-385.
Amieva, H., Phillips, L. H., Della Sala, S., & Henry, J. D. (2004). Inhibitory functioning in Alzheimers
disease. Brain, 127(5), 949-964.
Baddeley, A. (2003). Working memory: looking back and looking forward.Nature Reviews Neuroscience, 4(10),
829-839.
Blanger, S., Belleville, S., & Gauthier, S. (2010). Inhibition impairments in Alzheimer's disease, mild cognitive
impairment and healthy aging: Effect of congruency proportion in a Stroop task. Neuropsychologia, 48(2), 581590.
Belleville, S., Rouleau, N., & Van der Linden, M. (2006). Use of the Hayling task to measure inhibition of
prepotent responses in normal aging and Alzheimers disease. Brain and cognition, 62(2), 113-119.
Bonnefond, M., & Jensen, O. (2012). Alpha oscillations serve to protect working memory maintenance against
anticipated distracters. Current biology, 22(20), 1969-1974.
Buzski, G., & Chrobak, J. J. (1995). Temporal structure in spatially organized neuronal ensembles: a role for
interneuronal networks. Current opinion in neurobiology, 5(4), 504-510.
Cowan, N. (2010). The Magical Mystery Four How Is Working Memory Capacity Limited, and Why?. Current
Directions in Psychological Science, 19(1), 51-57.
Foxe, J. J., & Snyder, A. C. (2011). The role of alpha-band brain oscillations as a sensory suppression mechanism
during selective attention. Frontiers in psychology, 2.
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