International Journal of Psychophysiology 80 (2011) 44–53

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International Journal of Psychophysiology

j ourna l homepage: www.e lsev ie r.com/ locate / i jpsycho

Reciprocal dynamics of EEG alpha and delta oscillations during spontaneous blinkingat rest: A survey on a default mode-based visuo-spatial awareness

Luca Bonfiglio a,⁎, Stefano Sello b, Maria Chiara Carboncini a, Pieranna Arrighi a, Paolo Andre c, Bruno Rossi a

a Department of Neurosciences, Unit of Neurorehabilitation, University of Pisa, Via Roma 67, I-56126 Pisa, Italyb Mathematical and Physical Models, ENEL Research, Via Andrea Pisano 120, I-56122 Pisa, Italyc Department of Physiology, University of Siena, Via Aldo Moro 2, I-53100 Siena, Italy

⁎ Corresponding author. Tel./fax: +39 050995724.E-mail address: l.bonfiglio@ao-pisa.toscana.it (L. Bon

0167-8760/$ – see front matter © 2011 Elsevier B.V. Adoi:10.1016/j.ijpsycho.2011.01.002

a b s t r a c t

a r t i c l e i n f o

Article history:Received 12 July 2010Received in revised form 23 December 2010Accepted 10 January 2011Available online 14 January 2011

Keywords:Event-related synchronization/desynchronization ERS/ERDEvent-related potentials ERPsEvent-related oscillations EROsBlinkingConsciousness

By means of a narrowband wavelet analysis (0.5–6 Hz), EEG delta event-related oscillations (EROs), bothtime- and phase-locked to spontaneous blinking (delta blink-related oscillations or delta BROs), have recentlybeen demonstrated. On the basis of their spatiotemporal characteristics, delta BROs have been proposed asbeing involved in an automatic mechanism ofmaintaining awareness in a visuo-spatial context. The aim of thepresent study was: a) to investigate whether spontaneous blinking was also able to modulate alphaoscillations and, if so, b) whether this modulation was consistent with delta BROs, in order c) to acquireadditional information for a better understanding of the cognitive phenomena underlying blinking.Using a broadband (0.5–100 Hz) continuous wavelet transform (CWT), we analysed a total of 189 three-second EEG epochs time-locked to the blinks of seven healthy volunteers. The EEG signals were submittedboth to band-pass filtered cross-trial averaging (to obtain frequency-specific BROs) and to alpha event-relatedsynchronization/desynchronization (i.e., blink-related synchronization/desynchronization, BRS/BRD).The alpha oscillations showed: a) an early BRS; b) a BRD in the same temporal window of the delta BROs and,c) a late BRS. We postulate that: a) the early BRS represents the short-term memory maintenance of the lastvisually perceived trace of the surroundings; b) the alpha BRD is associated with the comparison between thenewly perceived image of the environment and its mnestic representation, and, lastly, c) the late BRS isconnected with neuronal recovery phenomena.

figlio).

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© 2011 Elsevier B.V. All rights reserved.

1. Introduction

1.1. Spontaneous blinking and cognition

The average rate of spontaneous blinking at rest is around 15blinks per minute (bpm) (Tsubota et al., 1996). However, this canchange according to the cognitive tasks that the subject has toperform (Fogarty and Stern, 1989; Fukuda, 1994; Lesner and Hardick,1982; Orchard and Stern, 1991; Viggiano and Mecacci, 2000). Thevariability and rhythm of blinking depends on the duration of thetemporal span between two consecutive blinks (inter-blink interval,IBI), when information acquired through the attentional filter iselaborated. The IBI lengthens or shortens – and therefore the blinkingfrequency decreases or increases, respectively – depending on theattention involved: it lengthens when the required attentionincreases (as much as the attentive resources of the subject can beactively deployed) (Viggiano and Mecacci, 2000), while it shortens

with fatigue and habituation (Veltman and Gaillard, 1998; Yamada,1998) when intentional attentionwanes. Due to this characteristic, IBIcan be considered a temporal period during which the attentionalfunction is active to a certain degree, that is, as an attentional span.

Moreover, the temporal distribution of blinking is not regular butvaries and adapts according to the different moments of a complexcognitive task. In certain phases, blinking is inhibited while it isfacilitated in others. This alternating pattern is not casual butcorresponds to the serial nature of information processing; that is, itdenotes the subsequent alternating cognitive phases involved duringthe performance of a task. For instance, when reading – whichundoubtedly requires much visual attention – the overall frequency ofblinking is decreased, but the blinks cluster naturally during certainsignificant moments, as when punctuation signs or the end of asentence are encountered (Hall, 1945; Holland and Tarlow, 1975;Orchard and Stern, 1991). Something similar happens when speaking,when the blinks concentrate during the natural pauses betweensentences (Hall, 1945; Holland and Tarlow, 1975), and while viewingvideo stories, when they concentrate at implicit breaks of visualstreams (Nakano et al., 2009). The blinks therefore appear to becomeless frequent during attention and elaboration but cluster duringshort-term memorization of information (Bentivoglio et al., 1997;

45L. Bonfiglio et al. / International Journal of Psychophysiology 80 (2011) 44–53

Orchard and Stern, 1991). In fact, during discriminative experimentaltasks, the probability of a blink occurring during the first 300 ms afterthe administration of a stimulus target (that is, during the attentivephase linked with information processing) is low, while it issignificantly higher between 300 and 800 ms (during updating andshort-term memorization of the information) (Fukuda, 1994).

On the other hand, according to one of the most esteemedneurobiological theories on consciousness (Crick and Koch, 1990), theinteraction between attention and short-term memory (STM) is theactual basis of primary consciousness. Sequential and bi-directionalshifting of the focus of attention (both top-down and bottom-up)seem to permit interaction between the subject and the outsideenvironment. Short-term memorization of information concerningthe attentional spans that have just occurred, over and above theintrinsic discontinuity of the process, guarantees continuous mainte-nance of the conscious experience.

1.2. Spontaneous blinking and visual continuity

Strictly connected with spontaneous blinking is visual continuityor stability; that is, the (subjective) feeling of a continuous flow ofvisual inputs, in spite of transient interruptions caused by blinking.The duration of each blink varies (depending on the different studiesperformed on the topic) between 200 and 400 ms (Bristow et al.,2005). However, interruption in visual input, when there is completecoverage of the pupil, lasts less (around 100–150 ms) and is usuallynot noticed by the subject. This does not depend merely on the factthat it is brief because, on the contrary, a period of ‘environmentaldarkness’ lasting the same length of time is easily perceived.

Two hypotheses have been put forward to explain this: a) that it iscaused by a pronounced loss of visual sensitivity during blinks (blinksuppression) due to neural inhibition triggered by the motorcommandwhich generates the blink (corollary discharge) (Volkmannet al., 1980) and/or b) that it depends on activation of the visuo-spatialworking memory network (Bristow et al., 2005; Hari et al., 1994) thatcontinuously updates the information concerning the objects visiblein the surrounding area (Goodale and Milner, 1992; Stein, 1992) tokeep a continuous and stable image of the environment.

In this latter case, the working memory (WM) might have thesame role as that postulated by Crick and Koch in their theory onconsciousness, concerning the subjective experience of continuousflow of consciousness in spite of the serial character of the attentivemechanism that maintains it: that is, the temporary buffer of mnestictraces (whether pertaining to the external or internal milieu)acquired during the attentional phase just concluded, so that acomparison or match can be recalled and elaborated in relationshipwith the information acquired in the next phase.

1.3. Spontaneous blinking and visuo-spatial awareness

There is now a certain amount of agreement that event-relatedpotentials (ERPs) are composed of a superposition of transientmultiband oscillatory events, among which delta oscillations play a(pre)dominant role (Başar et al., 2001; Karacaş et al., 2000a, 2000b).These delta event-related oscillations (delta EROs) have beenconsidered to mediate various cognitive functions — from sensoryprocessing and change detection to attention selection, STM updatingand emotional processing (Başar et al., 2001; Güntekin and Başar,2009; Karacaş et al., 2000a, 2000b).

In a previous study carried out on subjects who were not asked toperform any response-demanding cognitive tasks (eyes-open restingcondition), a spontaneous blink-related power enhancement of EEGoscillations in the delta (0.5–3 Hz) frequency band (delta blink-relatedoscillations or delta BROs) was observed. Prior to the blink, such anenergy increase had the hallmarks of an amplitude modulation of theongoing delta oscillations (non phase-locked induced oscillations),

whereas it took on the characteristics of substantial phase-resetting(phase-locked evoked oscillations) just after the blink itself (Bonfiglioet al., 2009, 2010). Therefore, on the basis of their spatiotemporalcharacteristics, it was proposed that delta BROs might reflect theactivation of events such as updating and short-term memorization ofthevisual context implicated in anautomaticmechanismofmaintainingvisuo-spatial awareness (Bonfiglio et al., 2009, 2010).

The latter concept has to be differentiated from those of consciousperception and continuity of vision. The difference between visuo-spatial awareness and conscious perception depends on the differentroles played by the type of attention involved in the two phenomena.Attention focused on external objects or internal thoughts determinesconscious perception, whilst distributed attention maintains a global(gestaltic) visuo-spatial awareness of the environment. The differencebetween visuo-spatial awareness and continuity of vision lies in thedifferent role played in the two phenomena by mnestic representa-tion. The latter, in continuity of vision, is simply to bridge the gap dueto blinking in order to ensure the continuity of the visual flow. Invisuo-spatial awareness, however, mnestic representation also worksas an element of comparison with the current image. This allows thevisual system to establish or deny correspondence between visualscenes seen before and after the blink. This, in turn, providesinformation about the environment proneness to change or remainstable.

1.4. Aims and scope

Over the past years, analysis of the reciprocal interaction betweenEEG oscillations belonging to different frequency bands has increasedthe possibilities of functional interpretation of cognitive phenomena(Başar et al., 2001; İşoğlu-Alkaç et al., 2000; Klimesch, 1996; Palva andPalva, 2007; Sauseng and Klimesch, 2008) since it reflects the activityof the multiple oscillatory neural networks or subsystems involved.Likewise, it is known that the event-related oscillations (EROs) in thedelta frequency band are accompanied by an attenuation of the alphaoscillations (Bernat et al., 2007; İşoğlu-Alkaç et al., 2000; İşoğlu-Alkaçand Strüber, 2006; Mazaheri and Picton, 2005; Pesonen et al., 2006;Strüber and Herrmann, 2002; Yordanova and Kolev, 1998; Yordanovaet al., 2001), which have been variously connected to non-specificattentional processes triggered by stimulus evaluation (Yordanovaand Kolev, 1998), general alerting and arousal (Yordanova et al.,2001), attentional resources allocation in relation to memoryupdating following stimulus (Yordanova et al., 2001), and expectancy(İşoğlu-Alkaç and Strüber, 2006).

In this study we have extended the investigation to the alpha bandas well, for the purpose of: a) investigating whether spontaneousblinking is able to modulate ongoing alpha oscillations and, if so, b)whether this modulation is consistently linked to the delta BROs, c)thus integrating complementary information which might lead tobetter functional comprehension of the cognitive phenomena under-lying blinking.

2. Materials and methods

2.1. EEG/EOG recordings

Seven healthy volunteers (2 females and 5 males) between 21 and26 years (mean: 24.3; S.D.: 1.7) participated in the study. The EEGswere recorded by using a BQ132S EEG amplifier (BrainQuick System,Micromed, Treviso, Italy) and an electrode cap (Electro-Cap Interna-tional, Inc., Eaton, Ohio 45320 USA) at 19 positions following the 10–20 International System. This cap provides a reference positionbetween Fz and Fp1–Fp2. Impedance was kept below 5 kΩ. The EEGsignals were band-pass filtered between 0.03 and 70 Hz, with thenotch filter on. Data were digitised at a sampling rate of 256 Hz. Theelectrodes were re-referenced off-line to the mean of all recording

46 L. Bonfiglio et al. / International Journal of Psychophysiology 80 (2011) 44–53

channels. Blinks were also monitored by means of EOG recording. Theelectrodes were arranged diagonally to the horizontal line passing bythe outer corners of the eyes. All the data were exported in EDF formatfor subsequent analyses.

2.2. Experimental set

The EEGs were recorded for subsequent 5-min periods (alternatedwith 5-min free intervals during which the subjects could conversewith the operators, thus avoiding boredom and the onset ofdrowsiness). During each recording period, the subjects were seatedin a chair, in a noise-insulated room of comfortable temperature. Theyhad only to look ahead, letting their eyes wander without payingattention to anything in particular and they were free to think ofwhatever they wished (‘waiting room effect’) (Bonfiglio et al., 2009).In this ecological situation, a) the visual stimuli coincide with theincoming flow of information of everyday vision, when the subject isresting quietly without being engaged in attention-demanding tasksor goal-directed behaviour, and b) attention may be considered theattentional-set wandering spontaneously from one object to anotherwithout the need for a great amount of attentional resources(Bonfiglio et al., 2009). Moreover, under these circumstances theremight be a dynamic interplay between ongoing self-referential orintrospectively-oriented mental activity and general gathering ofinformation from the surrounding environment (according to thedefault-mode concept of brain function) (Delamillieure et al., 2010;Gusnard et al., 2001).

All the experiments followed the tenets of the declaration ofHelsinki. Written informed consent was obtained after the aims andthe experimental techniques were fully explained. The experimentshad the approval of the local ethical committee.

2.3. Blink-artefact removal by means of Independent ComponentAnalysis (ICA)

To remove the blink-artefacts, independent component analysis(ICA) was computed according to the algorithm developed byHyvarinen and Oja (2000) and implemented for MATLAB (FastICApackage). Before performing ICA, data were high-pass filtered with afilter of 0.5 Hz to remove linear trends that would negatively affect it.

Artefact-free 3 s-lasting EEG epochs (±1.5 s) centred on singleblink maxima were then selected from the EEG recording.

2.4. Continuous wavelet transform (CWT) and time-frequency-powerplots

An equal number (27) of epochs per subject, for a total of 189 EEGepochs, was averaged and time-locked to the blink maximum (timezero, T0). Wavelet power spectra were computed by performing aMorlet continuous wavelet transform (CWT) on both single andcoupled (wavelet cross-correlation) EEG signals frommid-frontal (Fz)and mid-parietal (Pz) electrode sites (Torrence and Compo, 1998).Variations in signal power of more than 3 SD compared to the meanbaseline value, corresponding to the parts coloured in yellow in Fig. 1,were considered statistically significant.

2.5. Inverse wavelet transform (IWT), frequency specific blink-relatedoscillations (BROs) and wavelet cross-correlation

Since the wavelet transform is an invertible function, it waspossible to reconstruct the whole original time series using a properdeconvolution process. The time-resolved analysis of the wavelettransform for each scale allowed us to reconstruct the time seriescomponents for the two local-bands of interest in the wavelet map(inverse wavelet transform, IWT).

Thus, we separated both the alpha (8–12 Hz) and the delta (0.5–3 Hz) frequency bands at different spatial locations, in order to studythe relative dynamical properties. The reconstructed signals weresubmitted to cross-trial averaging, obtaining both individual andgroup-averaged BROs.

An essential item of information, related to the global dynamicproperties of local band signals, is their phase relationship andamplitude coherence. This was obtained from the local band signalreconstruction with computation of the Spearman rank correlationcoefficient vs the phase lag (Bendat and Piersol, 1971). In this way, themean phase lag of EEG signals, corresponding to their maximumamplitude coherence, was computed.

2.6. Phase-locked and non-phase-locked alpha (8–12 Hz) blink-relatedsynchronization (BRS) and desynchronization (BRD)

The alpha band event-related synchronization/desynchronization(ERS/ERD) (Pfurtscheller and Lopes da Silva, 1999) on the blink-locked EEG epochs (more properly defined as BRS/BRD) was alsocomputed. Phase-locked and non-phase-locked EEG activity could bediscriminated by calculating band-power amplitude changes usingthe so-called inter-trial variance (Kalcher and Pfurtscheller, 1995).The band-pass filtering of the EEG data was derived in this case by firstusing the wavelet transforms and thereafter by computing the relatedinverse-wavelet transforms or IWT (Bonfiglio et al., 2009). Consider-ing N trials or subjects and following the classical ERD method, theinstantaneous power for EEG data was computed as:

PðjÞ =1N

∑N

i=1x2f ði;jÞ ð1Þ

where P( j) is the averaged power estimation of a given EEG band-passfiltered over all trials, and x f(i,j) is the j-th sample of the i-th trial ofthe EEG band-pass filtered data. The inter-trial variance method wascomputed as:

IVðjÞ =1

N−1∑N

i=1xf ði;jÞ−x

f ðjÞ

n o2 ð2Þ

where N is the total number of trials, x f(i,j) is the j-th sample of thei-th trial of the EEG band-pass filtered data and x f(j) is themean valueof data at the j-th sample averaged over all band-pass filtered trials.

For the ERD (or ERS) calculation, either the power or the inter-trialvariance can be used; here, the ERD (or ERS) was quantified as thepercentage change of the inter-trial variance, IV(j), at each samplepoint, relative to the inter-trial variance, IVr, in a given referenceinterval:

ERD jð Þ = IV jð Þ−IVrð Þ= IVr � 100 ð3Þ

with:

IVr = 1= k ∑n0 + k

j=n0IVðjÞ

where: [n0,n0+k] is the reference interval. Note that when ERDN0,there is an event related synchronization or ERS.

The important feature in the use of the inter-trial variance is thatonly the non-phase-lockedEEG activities contribute to the bandpowerchanges. Moreover, the computation of the power (Eq. (1)) was usedhere to extract, by difference, the phase-locked EEG contributions inthe band power changes (Kalcher and Pfurtscheller, 1995).

For our blink-related EEG data, we considered a time window of500 ms – starting 1500 ms before the blink and with a movingwindow of 62 mswide with no overlapping – as the reference intervalin the computation of ERD (or ERS).

Fig. 1. Wavelet power spectra from 189 EEG epochs (27 epochs per subject, 7 subjects) for Fz (a) and Pz (b) locations. The x axis shows the time in ms (zero value, T0, refers to theblink maximum) and the y axis gives the EEG frequencies in Hz (logarithmic scale). In the colourimetric scale, the warm colours correspond to the high spectral powers (μV2) whilethe cold colours refer to the low ones Variations in signal power of more than 3 SD compared to the mean baseline value, corresponding to the parts coloured in yellow, wereconsidered statistically significant. For further explanations, see the text.

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The significance band for the inter-trial averaged ERD (or ERS)behaviour (Eq. (3)), was computed here using the 2-sigmathreshold (or 95% confidence interval) for the relative amplitudeoscillations.

3. Results

3.1. Alpha band

3.1.1. Time-frequency power, BROs and fronto-parietal cross-correlationThewaveletmaps reveal a reduced alpha band signal (blink-related

alpha attenuation) on both derivations after the blink (Fz, Fig. 1a; Pz,Fig. 1b). In the parietal location it starts about 410 ms after T0 and ends,with a recovery of the signal, about 600 ms after T0 (total duration:about 190 ms); whereas in the frontal location it begins about 530 msafter T0 and finishes about 850 ms after it (lasting overall about320 ms).

Both individual and group-averaged BROs obtained on the alphaband (Fig. 2) show the typical fusiform behaviour of alpha in bothderivations (Fz, Fig. 2a; Pz, Fig. 2b). The mean group cross-correlationanalysis reveals that the maximum value of amplitude coherence

(0.33) corresponds to a phase lag of 12 ms, the posterior site beingleading and anterior trailing.

3.1.2. BRS/BRD fronto-parietal patternAfter T0, a similar BRS/BRD pattern of the alpha signal was seen in

both of the spatial sites with the following sequence of events: earlyBRS, BRD and late BRS (Fig. 3).

In particular, the early parietal BRS remains in the 0–258 mstemporal range, with maximum magnitude of about 35% reachedapproximately 140 ms after T0 (Fig. 3b); whereas, in the frontal area,it occurs in the 0–358 ms temporal range with a peak of about 25%approximately 260 ms after T0 (Fig. 3a). Furthermore, if one takes intoaccount the actual start of the phenomenon (that is, where theascending branch begins after the negative values) rather than justthe portion of the curve above 0%, the early BRS begins before T0 inboth cases: at about 100 ms before in Pz (−100 ms) and at about40 ms before in Fz (−40 ms). Hence, the evolution of early BRS (fromits start to its peak and then into BRD) appears to occur earlier atparietal level than at frontal level, with a time gap that varies between60 and 120 ms according to the phase considered.

Likewise, the parietal BRD (Fig. 3b) ranges between 258 and955 ms, with a peak of over 50% at approximately 460 ms after T0;

Fig. 2. Alpha BROs recorded from Fz (a) and Pz (b). The x axis is the same as in Fig. 1. They axis shows the amplitude of the signal (μV). The grey colouring shows the single alphaBROs referring to the individual subjects. The grand average alpha BROs are in black. Inthis latter point, note both the reduced amplitude and the desynchronization of thesignal at the maximum attenuation of the alpha oscillation (time-window 258–995 msafter T0). See the text for further explanations.

Fig. 3. Alpha ERS/ERD (mean group) referring to the Fz and Pz recording sites (panels aand b, respectively). The x axis is the same as in Fig. 1. The y axis shows the percentagevariations with respect to the baseline period. The positive values correspond to the ERSand the negatives correspond to the ERD. Shown in black, the ERS/ERD calculated byinter-trial variance, which takes into account the non-phase locked component. Thehorizontal lines correspond to the significance threshold at 2-sigma (confidenceinterval: 95%). The phase-locked component is shown in grey. Note the complete lack ofphase-locking both in Fz and in Pz. For further explanations, see the text.

48 L. Bonfiglio et al. / International Journal of Psychophysiology 80 (2011) 44–53

whereas, in the frontal area it ranges between 358 and 996 ms andpeaks at almost 40% about 520 ms after T0 (Fig. 3a). Therefore, even inthe case of BRD, both its start and its peak expression occur earlier atparietal level with a time gap varying between 100 and 60 ms,respectively. Moreover, the BRD in Pz results to be not only moreintense than in Fz but also longer (lasting 737 vs 637 ms).

The late parietal BRS (Fig. 3b) remains in the 955–1472 ms range,with a brief plateau-like peak of over 50% at around 1276 ms after T0and lasting about 60 ms. At the frontal area, the late BRS is within the996–1428 ms span, with a peak of over 50% at around 1268 ms after T0(Fig. 3a). Hence, in the case of the late BRS the differences betweenparietal and frontal areas are greatly reduced. Even though thephenomenon starts earlier in the parietal area in this case as well, itstemporal evolution is almost simultaneous in the two sites, with mostof the time gaps less than 40 ms.

3.2. Delta band

3.2.1. Time–frequency power, BROs and fronto-parietal cross-correlationThewaveletmaps in Fig. 1 show a power increase in the delta band

(blink-related delta response) on both derivations around the time ofthe blink, with different timing and intensity across the two recordingsites (Fz, Fig. 1a; Pz, Fig. 1b).

In the parietal site, this phenomenon starts about 840 ms beforeT0, increases in time to reach its plateau (around 23 μV2) about262 ms after T0, then decreases and fades out about 1110 ms after T0;the entire duration is about 1950 ms. In the frontal site it is shorter(1695 ms) and less intense, starting about 675 ms before T0, reachingits plateau (around 14 μV2) about 133 ms after T0 and fading outabout 1020 ms after T0.

Both individual and group-averaged BROs obtained on the deltaband (Fig. 4) show a blink-related slow positive wave in the parietalsite (Fig. 4b) followed by a negative deflection, with mean peaklatencies at about 300 and 600 ms, respectively, after T0. A similaroscillation takes place on the frontal site (Fig. 4a), with loweramplitude and reversed polarity. The mean group cross-correlationanalysis shows that a phase-lag of 32 ms corresponds to the

Fig. 4. Delta BROs recorded from Fz (a) and Pz (b). The x axis is the same as in Fig. 1. They axis is the same as in Fig. 2. The grey colouring indicates the single delta BROs of theindividual subjects. The grand average delta BROs are shown in black. Note thereproducibility and phase alignment of the delta EROs after T0. See the text for furtherexplanations.

Fig. 5. Synoptic table of the grandaverage delta (black) and alpha (grey) BROs, and ofthe mean group alpha ERS/ERD (red) recorded from the Pz alone. The x axis is the sameas in Fig. 1. The y axes show the amplitude of the signal in μV for the delta and alphabands (left, black) and the percentage variations of the alpha signal with respect to thereference period (right, red). Note the delta BROs and the alpha attenuation co-existingfor the most part of the same temporal window.

49L. Bonfiglio et al. / International Journal of Psychophysiology 80 (2011) 44–53

maximum value of amplitude coherence (−0.57), obtained in anti-correlation, the posterior site being leading and anterior trailing.

3.3. Merged alpha and delta bands

Lastly, Fig. 5 clearly depicts – on a mean group basis – how thedelta BROs largely cover the same time-window in which both alphaBRD and the amplitude attenuation of alpha BROs occur.

4. Discussion

4.1. General findings

In our opinion, the most important outcome of the present studylies in having shown: a) that spontaneous blinking does modulateongoing alpha oscillations, and b) that such a modulation, in bothtemporal and functional terms, is not only consistent but is alsocomplementary to that of delta oscillations (Bonfiglio et al., 2009,2010).

In fact, in the mid-parietal site the alpha oscillations showed thefollowing sequence of events: a) an early BRS within the 0–258 mstime-window, when delta oscillations have yet to achieve theirmaximal phase alignment; b) a BRD between 258 and 955 ms, for themost part in the same time-window as the delta BROs, in agreementwith the well known phenomenon whereby delta EROs areaccompanied by alpha attenuation (Bernat et al., 2007; İşoğlu-Alkaçet al., 2000; İşoğlu-Alkaç and Strüber, 2006; Mazaheri and Picton,2005; Pesonen et al., 2006; Strüber and Herrmann, 2002; Yordanovaand Kolev, 1998; Yordanova et al., 2001); c) a late BRS between 955and 1500 ms, when delta oscillations have almost faded out.Therefore, the two bands have different dynamics – even opposingbut nevertheless interrelated – so that the functional meanings thatcan be attributed to each of them converge on a uniform interpre-tation of this phenomenon (as will be discussed further on).

Furthermore, both evaluation of the temporal gap between theBRS/BRD alpha events and analysis of the cross-correlation of thealpha and delta oscillations on the two recording sites suggest thatthere is a posterior-to-anterior involvement of the fronto-parietalsystem, which, in effect, is the typical pattern of distribution ofbottom-up-like bioelectric phenomena (Klimesch et al., 2007b).

All these considerations confirm a possible role exerted byspontaneous blinking in the automatic maintenance of visuo-spatialawareness of the context while the subject is not engaged in anattention-demanding task.

4.2. The early alpha BRS: functional significance

Can the early alpha BRS be an electrophysiological correlate ofvisuo-spatial WM activity? As already mentioned in the Introduction,the involvement of WM has been linked with blinking to explain thecontinuity of vision. Its role would be to maintain a continuousrepresentation of visual objects in the ego-centred space (Hari et al.,1994; Bristow et al., 2005) despite disruptions of the visual inputduring blinks, even though this interpretation does not take intoaccount the visual sensory (iconic) memory (Sperling, 1960), theduration of which (about 250 ms) in theory would be sufficient tobridge the gap due to the blink.

50 L. Bonfiglio et al. / International Journal of Psychophysiology 80 (2011) 44–53

As far as we know, there are no studies in the literature thatconnect the modulation of blink-related alpha oscillations at rest withthe visuo-spatial WM. Thus, we must necessarily refer to EEG studiescarried out with experimental paradigms specifically modelled toinvestigate WM (e.g., memory scanning task), in which the informa-tion must not only be held in memory but also manipulated. In thesestudies, a pronounced (upper-) alpha ERS can be observed overparietal regions during encoding/retention (Busch and Herrmann,2003; Cooper et al., 2003; Herrmann et al., 2004; Jensen et al., 2002;Klimesch et al., 1999; Sauseng et al., 2005; Schack and Klimesch,2002). The functional significance attributed to this is inhibitory top-down control (provided by prefrontal areas engaged in executive/attentional control) to impede recalling items from previous trials inorder to prevent interference on the encoding and retention of newitems (Klimesch et al., 2007b).

Likewise, the early alpha BRS we saw might serve to suppressvisual inputs from previous visual memory traces (and/or ongoingmental imagery), in order to prevent interfering signals reachingbrain areas involved in actual STM maintenance (Michels et al.,2008). All this occurs so that the comparison between visuo-spatialrepresentation (stored in the STM) and its new perceptive image isalways and exclusively performed through the most recentlyupdated template.

Nevertheless, when interpreting the possible functional signifi-cance of early BRS, the particular characteristics of our study must betaken into account. In effect, the experimental model that we useddiffered from the traditional ones for studying WM in that it lackedthe typical executive components, since our subjects did not have toperform any goal-directed tasks (Cooper et al., 2003, 2006; Klimeschet al., 2006; Ray and Cole, 1985).

4.2.1. The early alpha BRS: a top-down or a bottom-up phenomenon?In the specific experimental condition we have adopted, two

elements of the three-component model of WM proposed byBaddeley and Hitch (1974) may be involved: the visuo-spatialsketchpad and the central executive. The latter is to be understoodin the sense proposed by Norman and Shallice (1986) in their modelof attentional control, which has been accepted by Baddeley himselfas an advancement of his own concept of central executive. TheNorman and Shallice model divides control into two processes.Quoting from Baddeley (2003): “The first relies on the control ofbehaviour by habit patterns and schemas, implicitly guided by cuesprovided by the environment” (i.e., in a bottom-up manner). Thiscondition is comparable to the experimental conditions adopted inour study, where subjects are not required to respond to any task andwhere the environmental situation is stable (i.e., it has a lowprobability of change). Also quoting from Baddeley (2003): “Thesecond comprises an attentionally limited controller, the supervisoryactivating system, which could intervene when routine control wasinsufficient” (i.e., in a top-down manner). This condition was notexamined in our study, but we think that it comes into play whensubjects have to cope with a task and/or when the environment isunstable (i.e., when environmental demands require a behaviouralresponse). Hence, it is reasonable to believe that the functions havinga role in our specific experimental condition might be a distributed(non-intentional) attention rather than a focalized (intentional) oneand, consequently, an automated/routine form of WM. These areundoubtedly bottom-up functions rather than top-down ones.

Is the early BRS the electrophysiological correlate of blinksuppression? That is, could it be an upstream drive coming frommotor or pre-motor areas (Bristow et al., 2005; Volkmann et al.,1980)? According to some recent studies (Cooper et al., 2003; Jensenet al., 2002; Michels et al., 2008; Ray and Cole, 1985; Tuladhar et al.,2007), an early alpha ERSmight reflect inhibition or disengagement ofthe dorsal stream in order to suppress visual inputs. Nevertheless,certain temporal elements clash with this interpretation.

Volkmann et al. (1980) reported that a reduction in visualsensitivity precedes a blink by about 150 ms, reaches its maximumat the beginning of the blink and does not recover completely until200 ms afterwards. This presumably occurs when about 60% of thediameter of the pupil is bared and the input of the first visual imagesstarts. Compared to the data in our study, this occurs about 125 msafter total closure of the eyelid (T0). Consequently, the inhibitionperiod goes from−225 to +125 ms compared to T0, and lasts a totalof 350 ms. Vice versa, the early ERS on Pz has an ascending phase thatstarts at around 100 ms before T0 and reaches its maximum 150–160 ms after T0 (Fig. 3b). Thereafter, the descending phase takesabout another 100 ms to reach the 0% line. Hence, the early BRS goesfrom−100 to +250 ms with respect to T0 and lasts a total of 350 msin this case as well.

Therefore, the two phenomena last the same length of time, buttheir temporal evolution is quite different: in fact, the BRS occursabout 100 ms later than the beginning of the blink suppression. In thiscase, it is unlikely that the BRS is activated by a corollary ‘command’ atthe motor output (since it would begin too late).

Is the early BRS involved with the alpha phase-locking that isresponsible for the P1/N1 complex and for which an early processof top-down phenomena has been suggested (Gruber et al., 2005;Klimesch et al., 2007a)? This seems rather unlikely, because theearly BRS starts a good while before what is normally recognisedas the time-window of the P1/N1 complex (between 50 and250 ms after the stimulus). If we consider the stimulus in ourstudy as the recovery of the visual input (which occurs about125 ms after T0), then the time-window for a blink-related P1/N1complex could be estimated in the 175–375 ms range, which is notvery compatible with the timing commonly accepted for the P1/N1complex. Besides this temporal incongruence, another even moreimportant factor is that in our study, and contrary to others(Gruber et al., 2005; Klimesch et al., 2007a; Kolev et al., 1999,2001), no phase-locked components, neither anterior nor posterior,were found (Fig. 3). As already mentioned, this is consistent withthe lack of top-down control; that is, without any executivecomponent in the experimental conditions used.

Furthermore, we found no antagonistic ERS/ERD in the fronto-parietal system in our study, though the spatiotemporal pattern washomogeneous in the entire system. On the contrary, besides certainquantitative differences (concerning BRS/BRD magnitude, durationand timing of the phenomena), the anterior and posterior regionsappear to behave in a similar manner, to the extent that one mightthink there is only one functional system. Nevertheless, the parietalinvolvement takes place before the frontal one: a) the early alphaBRS on Pz not only precedes Fz but is also of greater amplitude(Fig. 3); b) furthermore, cross-correlation analysis reveals that on allthe temporal segment taken into consideration the maximum valueof coherence amplitude corresponds to a phase lag of 12 ms, theposterior site being leading and anterior trailing. This suggests thatin these conditions the fronto-parietal network activates in aposterior-to-anterior direction; that is, with a bottom-up pattern.Hence, according to this hypothesis, we should see not the twoseparate systems (fronto-parietal and fronto-temporal) as responsi-ble for goal-directed and stimulus-driven attention, suggested byCorbetta and Shulman (2002), but rather an individual system,activated in both directions in the two situations — in the anterior-to-posterior one (when goal-directed) and the posterior-to-anteriorone (when stimulus-driven), respectively.

It is worth noting, however, that these conclusions about alphaoscillations – even if consistent with those relating to deltaoscillations – should be taken with some caution due to the type ofreference that has been used in our EEG recordings. Indeed, the use ofthe average reference with a low-density electrode array, because ofan incomplete estimate of a true zero potential, might haveintroduced a share of ectopic (spurious) alpha on the anterior regions

51L. Bonfiglio et al. / International Journal of Psychophysiology 80 (2011) 44–53

(Hagemann et al., 2001). Therefore, these data will have to beconfirmed by using a high-density montage (more than 64 channels)(Srinivasan et al., 1998). Furthermore, a high-density electrode arraywould also allow using reference-free techniques (such as surfaceLaplacian) – which improve estimates of an infinity reference byre-referencing surface potentials – to the best of their reliability(Srinivasan et al., 1996, 1998).

4.3. The alpha BRD

Might the BRD depend upon re-activation of the visual areas whenvisual input is recovered? If we consider the intersection on the line atzero, that is, the transition to negative values, the ERD would start ataround 268 ms after T0 (about 140 ms after 60% re-opening andrecovery of visual sensitivity) (Fig. 3b). This is not very compatiblewith a ‘perceptive’ re-activation and is much more consistent with are-activation connected to the subsequent processing (more so if oneconsiders the maximum negative that occurs 341 ms after the eyelidsare re-opened). This latter hypothesis appears to find confirmation inthe fact that the BRD is spread to the anterior regions as well; that is, itdoes not remain a local phenomenon restricted to the visual cortexareas but involves even large anterior cortical areas in long-rangeproportions (Klimesch et al., 2006). For instance, this behaviourjustifies the reference to a specific attentional phenomena (Klimeschet al., 2007b). Furthermore, an alpha ERD was described recentlyduring the recognition stage related to the active representation,comparison and/or identification of the stimuli in a memory searchparadigm (Pesonen et al., 2006).

The cognitive meaning of alpha BRD can be confirmed also byconcurrence of delta BROs (Bernat et al., 2007; İşoğlu-Alkaç et al.,2000; İşoğlu-Alkaç and Strüber, 2006; Mazaheri and Picton, 2005;Pesonen et al., 2006; Strüber and Herrmann, 2002; Yordanova andKolev, 1998; Yordanova et al., 2001). It is now an acknowledged factthat the parietal alpha rhythm desynchronizes when the P300component of the ERPs – which is dominated by the delta response(Demiralp et al., 2001; Shürmann et al., 2001) – manifests. Thiscomplementary behaviour has been seen in discriminative tasks(odd-ball) in different sensory channels (Bernat et al., 2007;Yordanova and Kolev, 1998; Yordanova et al., 2001) and during theperceptive reversal of ambiguous figures (İşoğlu-Alkaç and Strüber,2006). Both phenomena (alpha ERD and delta BROs) reach theirmaximum magnitude in the parietal region, where the alphasuppression occurs approximately in the same time-window as thedelta synchronization and re-setting. This has been associated withactivation of a cortical region while it processes the stimulus and, inparticular, with non-specific attentional processes triggered bystimulus evaluation (Yordanova and Kolev, 1998), general alertingand arousal (Yordanova et al., 2001) and changes from a relaxed stateof alert wakefulness to an arousal reaction which triggers attentionalprocessing in a bottom-up manner (İşoğlu-Alkaç and Strüber, 2006).

4.4. The late alpha BRS

The late alpha BRS seen in our study has the same dimension andtemporal characteristics of a post-response or post-stimulus ERS (thatis, an after-discharge alpha) (Klimesch et al., 2006). This phenomenonhas been interpreted as a resynchronization probably associated withthe return of top-down control and, thus, readiness to perform a newtask (Klimesch et al., 2007b).

As we have already mentioned, it is not appropriate to talk of top-down control in our experimental conditions but rather of inhibitionconnected to recovery phenomena, which could, nevertheless,express readiness to perform a new blink or to process informationconcerning a new attentional span.

4.5. Proposal of a general theoretical framework

There is a certain amount of experimental evidence suggestingthat blinking might represent a change in the attentional-set, eitherwhen this is associated with a saccade (thus facilitating the shift ofattention towards another stimulus) (Evinger et al., 1994) or when ittakes place during vision of the same stimulus (therefore renewing itsperception) (Rainwater and Cogan, 1975). Consequently, blinkingbecomes amoment of transition (or resetting) between an attentionalphase that has faded out and a renewed, refreshed attentional phase.This scenario is compatible with the idea that blinking is theexpression of a cognitive change (brain state change); that is, atransition between different settings, ideas and gazes (Holland andTarlow, 1975).

With reference to the experimental situation adopted in our study,we postulate that the renewed perception caused by a blink is able toinduce (through a bottom-up mechanism) a transient (short-lasting,phasic) increase in the distributed attention at an upgraded level ofactivation (a sort of transient, subliminal arousal), as a necessary andsufficient condition for updating the mental representation of thevisuo-spatial context stored in the WM or in the visuo-spatialsketch-pad.

The situation is made more complex by the simultaneous andspontaneous flow of thought, which very likely interacts in acomplicated manner with the stream of information coming fromthe outside surroundings. These two streams probably assumedifferent reciprocal weight according to the environmental require-ments. If much is required (high probability of relevant stimuli and/orcontextual modifications), there is a prevailing need for perceptiveanalysis focused on and aimed at problem-solving and decision-making as a behavioural response. On the other hand, if theserequirements are slight (little or no probability of relevant stimuliand/or stable environment), a drive to introspective activity prevails(i.e., attention is directed mainly inwards) (Klimesch et al., 2007a,2007b). In this latter situation, the possibility of exerting continuouscontrol of the environment at a basic level (without consistentamounts of attentive resources being shifted from the main activity)must, nevertheless, be guaranteed for adaptation purposes. Hence, itis quite reasonable to believe that this mechanism, which is able toguarantee a minimum level (a ‘default-level’) of environmentalawareness, can take place automatically and is delegated tospontaneous blinking.

5. Conclusions

As far as we know, this study has demonstrated for the first timethe existence of dual-band EEG changes – time- (alpha) or phase-locked (delta) to the blink – that are complementary to each other asfar as both temporal evolution and a possible global functionalinterpretation are concerned. In fact, in this latter respect they arecompatible with the subsequent phases of the probable automaticmechanism that maintains perceptive awareness of the ego-centredvisuo-spatial environment at a low processing level (i.e., global orgestaltic) while the subject is not engaged in attention-demandingtasks but rather in internally oriented activities or free association(s).

According to this interpretation, the early alpha BRS might reflectthe activation of a short-term network involved in preserving thelatest mnestic trace of the visuo-spatial environment (concerning themoment immediately prior to the blink), while the visual flow isinterrupted during closure of the eyelids. In this case, the delta BROsmight reflect the functional correlate of the same events ofcomparison between the new image of the surroundings – as it isseen when the eyelids are opened again – and the previousrepresentation that has been stored in the STM, with the relativephenomena of context updating and memorization. This might be,therefore, a continuously updated check on the perceptive stability/

52 L. Bonfiglio et al. / International Journal of Psychophysiology 80 (2011) 44–53

instability of the surroundings that do not require a high level ofattention. The adaptive significance of this bottom-up process lies inthe fact that any environmental mismatching might be immediatelycaptured, and greater attentional resources might be then promptlycalled upon for the event. Consequently, the alpha BRD that is almostsimultaneous to the delta BROs might be associated with the ongoingelaboration of comparison data and, perhaps, with upgrading of theglobal attention to the level required by this elaboration, butsubliminal to true arousal (at least, in relatively stable environmentalconditions). Moreover, the need to keep in memory the visualrepresentation of the environment until the comparison is completedwith its new perceptive image (i.e., in the time-window betweenabout 300 and 1000 ms) goes beyond the temporal limits of sensorymemory (about 250 ms). This leads to a down-scaling of the putativerole of iconic memory in the maintenance of visuo-spatial awareness,except as a preliminary and complementary phenomenon to the WMintervention. This would not be in contrast to what has beenpostulated by Crick and Koch (1990) in their reference theory ofconsciousness, whereby “parts of iconic memory form the basis ofWM”. Lastly, a possible interpretation of the late alpha BRS is that itmight be the expression of neuronal recovery phenomena and,therefore, of readiness to perform a new blink or to processinformation concerning a new attentional span.

In our opinion, the present study shows how analysis ofspontaneous blinking and its neurophysiologic correlates can con-tribute further speculation about the basic aspects involved in themaintenance of visuo-spatial awareness of the surroundings, whichappear promising elements for studying the primary processes ofconsciousness, whether they are normal or altered by central nervoussystem diseases.

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