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This essay examines 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. Additionally, future directions considering other components like phase.
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Titolo originale
The inhibitory role of top-down alpha-band oscillations in the working memory context
This essay examines 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. Additionally, future directions considering other components like phase.
If any contents want to be reproduced, please email christof3.14@gmail.com
This essay examines 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. Additionally, future directions considering other components like phase.
If any contents want to be reproduced, please email christof3.14@gmail.com
The inhibitory role of top-down alpha-band oscillations in the working memory context
Index
I. Introduction : Establishing inhibition
II. The roles of alpha inhibitory activity: Enabling, suppressing and rejecting
- Top-down alpha during pre-encoding, stimulus onset, and encoding of items - Dynamic encoding: Selective processing as a result of instructions - Inhibiting task-irrelevant areas: Default or on-demand inhibition? - Alpha inhibition during maintenance: Rejecting distractors and keeping items uncorrupted.
III. Critical considerations & Future Directions
- Cueing and management of temporal expectations - Setting up tasks: the importance of tasks properties - Detaching roles and measuring sources - Future directions; the interplay between phase and amplitude
IV. Conclusions
V. References
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I. Introduction : Establishing inhibition 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 event- related 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 task- irrelevant 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).
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Apart from its theoretical usability, WM proves to be worth of studying as its impairment have been related with deficits in inhibitory function (Park and Reuter-Lorentz 2009) and failures in inhibition are considered to be key symptoms of Alzheimers disease (Amieva et al, 2004; Belleville et al 2006) schizophrenia (Haenschel and Linden, 2011) or even related to normal ageing (Zanto and Gazzaley, 2009; Belanger et al, 2010).
II. The roles of alpha inhibitory activity: Enabling, suppressing and rejecting 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. Pre-encoding Enabling/disabling Klimesch et al 2007 Stimulus onset Readiness Payne and Sekuler, 2013 Encoding Selective Processing Freunberger et al 2009 Retention Rejecting intruders Bonnefond and Jensen 2012 Timeline CUEING Looking at alpha inhibition in the WM context (Sternberg)
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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.
Top-down alpha during pre-encoding, stimulus onset, and encoding of items
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.
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Figure 2: Wilsch et al, 2014.
Figure 3: Wilsch et al, 2014.
Furthermore, Sauseng et al (2009) conducted an experiment using a WM task which consisted in two ensembles of differently coloured squares (varying from two to six), one in each hemi field and which colours have to be memorized . A cue informed the participant of which of the two arrays have to be ignored and which one has to be remembered. The authors reasoned that if alpha activity is related with the suppression of irrelevant stimuli's processing, and successful ignoring of irrelevant information is required for efficient WM performance, then lateralized alpha (difference of alpha amplitude between hemispheres) must grow as the amount of irrelevant information does. Illustration B below shows how amplitude increases in the ipsilateral hemisphere to relevant information while decreasing in the contralateral one (processing relevant items). Illustration C shows how lateralized alpha predicts capacity to retain items based on the capacity to ignore irrelevant information as alpha grows. Handel et al (2011) and Mathewson et al (2009) have found similar results relating successful ignoring and performance.
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Figure 4: Sauseng et al, 2009
Figure 5 Sauseng et al, 2009
Additionally, Sauseng et al (2009) used rTMS in an attempt to boost retention capacity by inducing alpha (10Hz) activity over the task-irrelevant sites. They also applied entrained alpha activity over task-relevant locations. Results showed a significant increase of short memory capacity when rTMS was applied over task-irrelevant areas, while a decrease took part when applied over task- relevant ones (maintaining items). Cleverly, authors delivered also activity of a diverse range of frequencies, finding these effects specific for induced alpha rhythm, as can be seen in the illustration below. Enhancement in memory capacity for items was specific of alpha rhythm at 10Hz. Romei et al (2010) found similar results using TMS while inducing impairment for stimulis detection using entrainment of alpha waves in an attentional task, inducing blindness to targets when oscillations were delivered over task-irrelevant visual areas.
Figure 6: Sauseng et al, 2009
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Dynamic encoding: Selective encoding and cognitive cherry picking as result of instructions
In a logic extension of the previous role, alpha activity suppression of processing can also be observed in more dynamic, fast-changing environments taking advantage of MEG/EEG temporal resolution. The main difference with the previous section is the intermixed, alternative manner in which the relevant/irrelevant information is presented. In this sense, alpha activity plays a critical role in successful encoding (Rihs et al 2007; Haegens et al 2010 ; Zanto et al, 2011 ;Haegens et al 2011 ;Roux et al 2012; Payne et al 2013 ;Horschig et al 2014). Also, task-relevant and task-irrelevant items might appear according some instructions given at the beginning and without one-to-one cueing, or perhaps without explicit cueing at all (Horschig et al,2014). Relevantly, speed in discrimination has been related with alpha activity (vanRullen et al, 2011). Irrelevant information in a constantly changing environment can be presented in a very diverse sort of situations and under different mixes with relevant items. Therefore, alpha activity has to adapt to the perceptual scene For example, irrelevant information can appear in combination with relevant information but segregated in space (visually, Sauseng et al, 2009,; tactile presentation in different points, Haegens et al, 2012) or in the same spatial location but segregated in time (Freunberger et al, 2009; Payne et al, 2013). It can also be the case that two different features are present in the same stimuli/items, but only one of them is relevant for further processing, making the inhibition work only on some aspects of what looks a unitary scene (Snyder and Foxe, 2010 e.g remember colours and not shapes).Finally, items can appear in different sensorial modalities at the same time (as exemplified in Klimesch et al, 2012). All of these situations represent a challenge while picking the important information and forgetting or not processing information. This cognitive cherry picking selects the relevant information out from the stimuli stream, and it is key any further cognitive functions. Alpha is therefore related with the internal control of attention once again (Klimesch et al, 2007). Given the remarkably storage-limited capacity of WM (Cowan, 2010), this suppression character of alpha activity acquires a critical importance, and efficient performance at WM tasks has been directly related with the successful inhibition of distracting stimuli (Gazzaley and Nobre,2012; Freunberger et al, 2011). Intrusion of task-irrelevant information is a major cause of failures in WM (Hasher and Zacks,1988 as quoted in Freunberger et al, 2009; Zanto and Gazzaley, 2009). Freunberger et al (2009) designed an experiment in the context of a Sternberg WM task. In this study, a set of 16 items per trial were presented to participants, 8 of them have to be remembered. After this trial, a probing item was displayed and the subject should indicate if it is an old (previously presented) or new (not previously presented) item. Activity of alpha waves were expected in parieto-occipital sites, supposedly related with blocking/enabling memory processing. Enhancement of alpha power especially of in its upper frequencies was visible during to-be- remembered items exposition, while functional inhibition took place during the presentation of irrelevant items evidencing a strong top-down regulation (Leiberg et al, 2006, found similar results for auditory Sternberg task) the illustration below shows this last effect. State of the Art Essay (II) - Mario B. Perez 8
Figure 7: Freunberger et al, 2009
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.
Inhibiting task-irrelevant areas: Default or on-demand inhibition?
The definition of what it is a task-irrelevant area is slippery. A task-irrelevant area can be so because the stimulus that is being presented in the perceptual scene is non-pertinent to the task, and thus, its processing must by inhibited. As an example of this apart from the Sauseng et al (2009), Haegens et al (2012) showed how subjects who performed better in a somatosensory WM task and were less affected by the distractors described stronger alpha power ipsilateral to the side in which relevant stimulation is presented. However, task-irrelevant areas are also all those locations in which processing is not expected to happen. Alpha power in these areas has been object of controversy, as some authors consider that such is only possible as a result of a distractors appearance, or in case that those areas are inhibited by default, like if the mere spatial location will be a distractor itself (Klimesch et al, 2007; Payne et al 2013). In this line, Klimesch et al (2012) state that alpha ERS in irrelevant areas reflect protection against potential interfering processes. Worden et al (2000, as quoted in Horschig et al, 2014) has nonetheless demonstrated the incensement in irrelevant areas and the decrease in relevant ones without presence of distractors. Additionally, Haegens et al. (2010) described that alpha activity over occipital sites during the retention period of a somatosensory WM task was observed and correlated with performance, constituting initial evidence for the necessity of alpha waves over task irrelevant locations in distractors absence (see illustration below).
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Tuladhar et al (2007) and Scheeringa et al in a joint EEG/fMRI study (2009) have shown the same pattern of alpha activity over posterior sites during WM maintenance, and alpha during the retention period and without the presence of an obvious distractor has been correlated with the number of items to be remembered (Jensen et al, 2002; Sauseng et al, 2009; Wilsch et al 2014).
Figure 8: Haegens et al, 2010
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.
Alpha inhibitory activity during Maintenance Rejecting distractors and keeping items uncorrupted.
As was mentioned in the previous section, alpha activity has been also observed during WM retention and maintenance (Jensen et al 2002; Jokisch and Jensen, 2007; Haegens et al, 2010; Bonnefond and Jensen 2012; Payne et al 2013 are some examples). Although there is some debate concerning the role that alpha might be accomplishing, that we will examine in the last sections, there are some good examples of the relevance of alpha oscillations in this stage. Thus, Bonnefond and Jensen (2012) used the Sternberg WM memory task paradigm to test the impact of two sets of distracting/intrusion items during the retention phase, one of them labelled as strong, with high resemblance to memorized items, and weak with low resemblance. Appearance of the distracter was expected by explicit cueing. Alpha oscillations increased previously to distracters appearance and predicted individual performance in the task, furthermore, differences in alpha power correlated negatively with divergences in reaction times. Consequently, subjects that showed an increased alpha power before strong distracters appearance were also the subjects with quickest response times during memory probing.
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In a thoughtful study, Payne, Guillroy and Sekuler (2013) carried out an experiment to evaluate the role of alpha oscillations in the protection of retained stimuli using a short-memory task with Gabor patches. Participants have to remember the spatial frequency of a Gabor patch to later reproduce it. Before the reproduction test, other Gabor patch with different spatial frequency was presented to subjects that were instructed to ignore this item. In the test in which the target Gabor patch has to be reproduced, subjects used a software which allow them to manipulate the spatial frequency until participant thinks that matches the target stimuli. This allowed the authors to have a exact measurement of the distortion induced by the presentation of task-irrelevant material over the target one. Participants with higher alpha activity when the distractor stimulus was presented also maintained a less corrupted version of the stimuli to be remembered. The authors interpreted this as evidence that alpha activity acts as a filter for irrelevant information. The illustration below shows the non-target effect influence of distractor over the target Gabor patch in pre-stimulus and onset of the distractor during WM maintenance. Note the value of correlation coefficients.
Figure 9: Payne, Guillroy and Sekuler, 2013
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. Critical considerations & Future Directions Cueing and management of temporal expectations 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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Conversely, the opposite problem might also appear. Late or very early cueing would not lead to an immediate appearance of alpha suppression while when short cueing was provided alpha suppression appeared almost instantly. Payne et al (2013) varied from 300 to 900 ms the cueing of the distractor stimulus, when cueing was presented 300ms modulation of alpha began straight away, whereas 900 ms cueing resulted in a modulatory effect several hundred milliseconds after onset. A possible reason for this delay, as we are talking about top-down modulations, would be that the participant is aware of the incoming appearance of a stimulus, but does not expect it in the immediate term and therefore delays the action of attention focusing. This could be solved setting intervals of appearance or jittering like in the study by Wilsch et al (2014). These issues are especially relevant when we consider the use of time-frequency instead of evoked-response analysis in the field, as expectancy changes in alpha amplitude might be diffuse over time.
Setting up tasks: the importance of tasks properties
The nature of the WM is a common topic of discussion. While there is a trend to use competitive visual stimuli (for example two arrays of different visual targets e.g Sauseng et al, 2009 or Handel et al 2011) there is some controversy about how of appropriated these stimuli are. Thus, modulations in alpha power can be found over the left hemisphere but in occasions not over the right one, as in Horschig et al (2014). There is some consistency about a differential behaviour between the two hemispheres, which states that left parietal regions process right hemi field visual stimuli while right parietal regions process a certain amount of both hem fields output (Sack, 2009 as quoted in Zanto et al, 2014). A similar effect has been claimed in somatosensory tasks (Haegens et al 2011). Task properties are also relevant when it comes to ensure that inhibition or suppression has actually taken place. In the experiment used to exemplify dynamic encoding (Freunberger et al 2009) the reader will note that there is actually no way to ensure that irrelevant items have in fact being ignored and not entered the WM retention system. A way to overcome this problem can be seen in other of the examples, this time by Payne et al (2013) in which Gabor patches were used. In that case, the impact of the task-irrelevant information is made explicit by making a discrete (remember/no remember) category quantifiable in terms of the percentage of the spatial frequency change due to distractors influence in the reproduction made by the subject. Although witty, this task proved to be very easy for participants, in especial when the task-irrelevant item was presented in first place and the task-relevant patch in the second.
Detaching roles and measuring sources
The tasks inherent properties are perhaps especially important regarding WM maintenance and retention studies. It is important to notice that caution is advisable while approaching this kind of experiments as alpha activity can be easily misunderstood if the experimental setting is not correctly settled. When the stimuli that has to be ignored and the stimuli that has to be memorized are shown at the same time, and especially if both stimuli are of the same modality (like two visual figures) to disentangle between the possible contributions of alpha activity can be complicated. This confusion arises from the potential role that alpha might be accomplishing, if intervening directly in items maintenance (Palva and Palva, 2007, Roux and Uhlhaas, 2014) or suppressing and rejecting possible intrusions (Freunberger et al 2009; Bonnefond and Jensen, 2012; Payne and Sekuler, 2013). Normally, this distinction is drawn based on where the activity is located, if in task- relevant or in task-irrelevant sites. Noteworthy, this distinction is often difficult to be established as extensive parts of the current body of evidence supporting the inhibitory role of alpha oscillations are based in EEG recordings, which involve a considerable spatial smearing (Palva and Palva, 2007).
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Is in this framework in which studies involving joint EEG/fMRI recordings have the best opportunity to make a unique contribution in finding an answer for this dilemma. Furthermore, BOLD signal has been found to correlate negatively with alpha activity (Scheeringa et al, 2009; look at Jensen and Mazaheri 2010 for more examples). There is other issue when recording alpha-band activity regarding the place of its origin. Alpha activity is thought to appear from cortico-cortico sources or cortico-thalamic sources (Nicolelis and Fanselow, 2002) and it is thought to accomplish a open/closing function of the thalamic gates thus enabling or disabling processing. It is less clear how efficiently alpha activity can be measured from such sources, again being here relevant complementary studies with fMRI or perhaps using invasive recordings in animal models.
Future directions; the interplay between phase and amplitude
Most of the research to date has focused on amplitude measurements to assess the role of alpha oscillations. However, a significant but yet a reduced part of the research community have claimed that other components might have something to add to this ongoing conversation, like phase or perhaps temporal envelopes (Palva and Palva, 2007; Mazaheri and Jensen, 2009; Payne et al, 2013). More specifically, Palva and Palva (2007) have claimed that it is phase rather than amplitude the component that carries on with the functional significance of alpha oscillations, attributing to alpha-band rhythmicity a key role in attention and consciousness and against the widely accepted alpha amplitude thesis. They also pointed out that alpha phase reordering can take place in the absence of alpha amplitude changes (supported by Hanslmayr et al,2005), and even during alpha amplitude suppression. Palva and Palva base their claims of an active role for alpha phase coherence mainly in studies in which an increase in phase synchrony is spotted around frontal areas (mainly mental calculations Palva et al, 2005, Halgren et al, 2002 or perceptual selection Mima et al 2001) although authors intended a broader generalization. Perhaps more interestingly, Freunberger et al (2009) proposes that alpha phase serves as a mechanism relevant for neural activity timing and in the binding of memory processes, showing how increase in alpha phase locking in low alpha frequencies (7-12Hz) takes place for items that have to be remembered later on in a WM task. Crucially, in this study the amplitude component was also examined, and authors observed an increase in phase coupling around stimulus onset together with a ERD for to-be-remembered items. The increase in phase-locking would be then a marker of information encoding, similarly to the way in which was originally proposed by Klimesch et al (2007), and possibly a marker of phase resetting. In a later article, Freunberger et al (2011) developed that the role played by phase could reside in the segregation of items, while keeping them in a coherent and integrated whole. This series of articles by Fruenberger et al (2009; 2011) can provide powerful enriched framework that might improve our understanding of alpha oscillations in WM tasks as seen in the below graph
*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.
Figure 11: Klimesch et al, 2012
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). State of the Art Essay (II) - Mario B. Perez 14
Potential manipulations over GABA levels looking for a correlate in alpha inhibitory activity and WM performance in studies similar to the one by Freunberger et al (2009) could complement existent TMS evidence (Sauseng et al 2009; Romei et al, 2010) about the role of alpha oscillations. IV. 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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