doi: 10.1152/jn.00728.2015114:3023-3028, 2015. First published 2 September 2015;J Neurophysiol 

Zhongtian Dai, James Tao, Shasha Wu and Marcia GraboweckyDavid Brang, Vernon L. Towle, Satoru Suzuki, Steven A. Hillyard, Senneca Di Tusa,from electrocorticographyPeripheral sounds rapidly activate visual cortex: evidence

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Rapid Report

Peripheral sounds rapidly activate visual cortex: evidence fromelectrocorticography

X David Brang,1,2,3 Vernon L. Towle,3 Satoru Suzuki,1,2 Steven A. Hillyard,4 Senneca Di Tusa,1

Zhongtian Dai,3 James Tao,3 Shasha Wu,3 and Marcia Grabowecky1,2

1Department of Psychology, Northwestern University, Evanston, Illinois; 2Interdepartmental Neuroscience Program,Northwestern University, Evanston, Illinois; 3Department of Neurology, University of Chicago, Chicago, Illinois; and4Department of Neurosciences, University of California, San Diego, La Jolla, California

Submitted 21 July 2015; accepted in final form 28 August 2015

Brang D, Towle VL, Suzuki S, Hillyard SA, Di Tusa S, Dai Z,Tao J, Wu S, Grabowecky M. Peripheral sounds rapidly activatevisual cortex: evidence from electrocorticography. J Neurophysiol114: 3023–3028, 2015. First published September 2, 2015;doi:10.1152/jn.00728.2015.—Neurophysiological studies with ani-mals suggest that sounds modulate activity in primary visual cortex inthe presence of concurrent visual stimulation. Noninvasive neuroim-aging studies in humans have similarly shown that sounds modulateactivity in visual areas even in the absence of visual stimuli or visualtask demands. However, the spatial and temporal limitations of thesenoninvasive methods prevent the determination of how rapidly soundsactivate early visual cortex and what information about the sounds isrelayed there. Using spatially and temporally precise measures oflocal synaptic activity acquired from depth electrodes in humans, wedemonstrate that peripherally presented sounds evoke activity in theanterior portion of the contralateral, but not ipsilateral, calcarinesulcus within 28 ms of sound onset. These results suggestthat auditory stimuli rapidly evoke spatially specific activity in visualcortex even in the absence of concurrent visual stimulation or visualtask demands. This rapid auditory-evoked activation of primaryvisual cortex is likely to be mediated by subcortical pathways or directcortical projections from auditory to visual areas.

multisensory; auditory localization; intracranial; ECoG

SOUNDS FACILITATE VISUAL PROCESSES in natural environments:concurrent auditory stimuli lower the threshold to detect anddiscriminate visual stimuli (McDonald et al. 2000; Noesselt etal. 2010), increase their subjective intensity (Stormer et al.2009), and speed perceptual and motor responses to visualtargets (Brang et al. 2013; Cappe et al. 2010; Miller 1982).These benefits of sounds on visual perception are due in part tothe redundancy of spatial/temporal information across modal-ities (for a review, see Stein and Stanford 2008). However, itremains poorly understood precisely what types of informationcan be relayed between the senses and the mechanisms thatmediate cross-modal facilitation.

Neuroimaging research in humans indicates that sounds canmodulate activity in early visual cortex (e.g., Mercier et al.2013; Raij et al. 2010) leading to increased cortical excitabilityin visual areas (Romei et al. 2007). However, research onsound-evoked activation of visual cortex in humans has notsystematically investigated what auditory information is re-layed to primary visual cortex. Recently, McDonald and col-leagues (2013) reported event-related potential (ERP) results

suggesting that peripherally presented sounds activate visualcortex with some spatial selectivity, consistent with priorneurophysiological demonstrations in cats (Morrell 1972).They demonstrated a late (�200 ms postsound onset) ERPpositivity for contralateral (relative to ipsilateral) sounds thatwas localized to neural generators in extrastriate visual areasusing dipole modeling, suggesting that sounds activate visualareas in a hemifield-specific manner. However, the poor spatialresolution of scalp-recorded ERPs does not permit a precisespecification of the neural locus of this cross-modal effect,making it difficult to identify any rapid auditory-evoked acti-vation of primary visual cortex or its spatial selectivity withina visual hemifield. In particular, if peripheral sounds elicitedshort-latency neural activity in anterior regions of the calcarinesulcus, which maps retinotopically to the peripheral position ofthe sound source, ERP recordings from the scalp would berelatively insensitive to the electrical activity generated fromthis region of cortex because it lies several centimeters awayfrom the surface of the scalp.

To overcome these limitations, we recorded electrocortico-graphic (ECoG) activity from intracranial depth electrodeslocalized to the calcarine sulcus (primary visual cortex) in twopatients with intractable epilepsy. ECoG affords excellentspatial and temporal resolution as well as a high signal-to-noiseratio, permitting the direct evaluation of auditory-evoked ac-tivity in primary visual cortex. Patients performed a central-sound detection task similar to that used by McDonald andcolleagues (2013). On each trial, either a tone was presentedcentrally or a noise burst was presented peripherally at 45° tothe left or right of the patient’s midline. Patients were requiredto respond only to the central tone so that neural responses tothe peripheral sounds were obtained without potentially con-founding response-related activity (Fig. 1A). ECoG activitywas examined to determine whether the peripherally presentedsounds evoked early visual cortical activity in a spatiallyspecific manner.

MATERIALS AND METHODS

Patients. Two right-handed male patients with mesial temporallobe epilepsy (27 and 41 yr of age) participated in this study duringclinical monitoring for medically intractable seizures (due to hip-pocampal sclerosis in patient 1 and viral encephalitis in patient 2)using ECoG recordings from chronically implanted depth electrodes(5-mm center-to-center spacing, 2-mm diameter). Patient 1 was im-planted with four temporal and one frontal depth electrode probes inthe left hemisphere as well as scalp EEG; the posterior portion of ananterior-posterior probe passed through medial temporal areas and

Address for reprint requests and other correspondence: D. Brang, Dept. ofPsychology, Northwestern Univ., 2029 Sheridan Rd., Evanston, IL 60208-2710 (e-mail: dbrang@gmail.com).

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included coverage of the calcarine sulcus as did the posterior portionof a medial-lateral probe angled posteriorly from the middle temporalgyrus (Fig. 1B). Patient 2 was implanted with 2 depth electrodeprobes, 1 in each of the left and right temporal lobes with the posteriorhalf of the left probe including coverage of the calcarine sulcus (Fig.1C), and 56 subdural electrodes along the right frontal and parietallobes and right superior temporal gyrus. Suspected mesial temporallobe epilepsies commonly require an anterior-posterior probe through

visual cortex to reach the hippocampus. Use of this probe does notproduce any detectable visual scotoma. Electrodes were placed ac-cording to the clinical needs of the patients. This study was approvedby the Institutional Review Board at the University of Chicago.Informed, written consent was obtained from each patient.

MRI and CT acquisition and processing. Preoperative T1-weighted MRI and postoperative computerized tomography (CT)scans were acquired for each patient to aid in localization ofelectrodes. Cortical reconstruction and volumetric segmentation ofeach patient’s MRI was performed with the Freesurfer (Dale et al.1999). Postoperative CT scans were registered to the T1-weightedMRI using Statistical Parametric Mapping (SPM), and electrodeswere localized using software developed in our laboratories(https://github.com/towle-lab/electrode-registration-app/).

Sound localization paradigm. Patients were seated in a hospital bedor nearby chair. Stimuli were delivered using a laptop (using Psych-toolbox; Brainard 1997) and 2 free-field speakers placed �45° to theright and left of the patient’s midline. Three types of sounds werepresented in random order during the experiment: a 53-ms, 1,000-Hzsinewave tone presented from both speakers simultaneously and thuslocalized centrally (30 trials) and a 83-ms pink noise burst presentedfrom either the left (60 trials) or right (60 trials) speaker. Stimuli wereselected for consistency with the paradigm used by McDonald andcolleagues (2013). A central fixation cross was displayed on the laptopthroughout the experiment. Patients were instructed to maintain cen-tral fixation and to respond via button press to the central 1,000-Hztone while making no response to the peripheral noise bursts (forwhich ECoG responses were analyzed). The interstimulus intervalvaried randomly between 2.0 and 2.5 s (uniform distribution).

Visual localizer. While retinotopic mapping was unavailable, weused two methods to record visual-evoked responses in visual cortex.Patient 2 viewed centrally presented visual images (1,000 ms perimage) spanning �20° visual angle at a rate of 1 picture every 3 sduring a control task. A drawback was that these central images wouldnot effectively stimulate visual neurons that were tuned to peripherallocations. For patient 1, we measured visual-evoked responses toluminance changes across the entire visual field by identifying 60natural eye blinks using the frontally recorded scalp EEG (electrodeFP1) taken during rest periods. Events were time-locked to the offsetof the blink (when eyes began to open), which has been shown to elicitincreased neuronal firing in V1 (Gawne and Martin 2000). Unfortu-nately, scalp-EEG data were unavailable from patient 2.

ECoG recordings and analyses. ECoG signals were analyzed from5 depth electrode probes in patient 1 (60 electrode contacts) and 2depth electrode probes in patient 2 (24 contacts) at sampling rate of1,024 Hz with no filtering for maximal temporal resolution. Data fromelectrodes near regions previously or subsequently surgically resectedwere removed from analyses, as were excessively noisy electrodes(with average amplitude variability exceeding 3 SD). Electrodeswithin primary visual cortex were selected for analyses based on theiranatomic location within the calcarine sulcus. Studies examining thecytoarchitectonically delineated border of V1 in humans show that ina small subset of individuals secondary visual cortex and visual regionprostriata expand into the anterior calcarine sulcus (Amunts et al.2000; Yu et al. 2012), introducing the possibility that the recordedactivity in our patients included neural responses from these regionsas well as from primary visual cortex.

The onset of the auditory stimulus was marked on ECoG record-ings with a voltage-isolated transistor-transistor logic (TTL). ECoG-ERPs were obtained by averaging ECoG signals offline across trialswith a time window of �100 to 500 ms around auditory onset. Epochscontaining excessively variable activity (�3 SD from the meanvariance of all epochs) were rejected offline (�1% of trials). The50-ms period preceding auditory onset served as the baseline for eachepoch. Statistical significance of the difference between the contralat-eral and ipsilateral conditions was estimated at each electrode/timepoint by comparing the observed contralateral-ipsilateral difference in

Fig. 1. A: auditory detection paradigm. Patients responded to a central tone andwithheld responses to peripheral noise bursts, allowing measurement of audi-tory-evoked visual responses to contralateral and ipsilateral sounds withoutresponse-related neural activation. ITI, intertone interval. B and C: coronal andsagittal images showing electrode locations (1-9) relative to the calcarinesulcus for patients 1 (B) and 2 (C).

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the ECoG-ERP with a null distribution generated by randomly shuf-fling the contralateral and ipsilateral labels across trials, computing themean contralateral-ipsilateral difference, and repeating this procedure1,000 times (2-sample permutation tests). This analysis revealedthe hemifield dependence of auditory-evoked visual activity. Toevaluate the effects of the contralateral and ipsilateral sounds sepa-rately, we also compared the observed contralateral or ipsilateralECoG-ERP with a corresponding null baseline that was generated byrandomly shuffling the sign (positive or negative) of the ECoG-ERPat each time bin for each trial, computing the mean waveform, andrepeating this procedure 1,000 times (1-sample permutation tests;Cohen 2014). To control for the identification of spuriously significantdifferences, an ECoG-ERP effect at each time bin was considered tobe statistically significant only if the time bin was a part of a series of10 contiguous significant time bins (Guthrie and Buchwald 1991).Figures 2–4 highlight these significant regions with gray boxes.Separately, we applied time-point-based multiple-comparison correc-tions (Cohen 2014) between �100 and 100 ms in which a distributionof maximum difference values was constructed from the permuted(null) data and the 95th percentile of that distribution was used as acutoff for significance across all time points in the real data; thismethod controls for multiple comparisons of ERP data at the family-wise error rate (FWER) of 0.05 (Cohen 2014).

RESULTS

In patient 1, ECoG-ERPs obtained from three of the fourelectrodes implanted in the anterior-inferior portion of thecalcarine sulcus (Fig. 2A) revealed significantly greater posi-tive amplitudes to contralateral than ipsilateral sounds at laten-cies under 100 ms. Significant differences (P � 0.05) wereidentified at electrode 1 (28–70 ms postsound onset), electrode3 (51–64 ms), and electrode 4 (35–71 ms). Applying FWERmultiple-comparison corrections between the prestimulus in-terval and a priori time points of interest (�100 to 100 ms), thedifferences observed before 100 ms remained significant atelectrodes 1 and 4. The short onset times at these electrodessuggest the presence of a fast mechanism through whichcontralateral sounds evoke neural activity in the anterior por-tion of primary visual cortex.

Patient 2, who had five depth electrodes along the lateraledge of the calcarine sulcus (Fig. 2B), showed a similar patternof results, demonstrating significant early (�100 ms) differ-ences in ECoG-ERPs evoked by contralateral and ipsilateralsounds during 45–97 ms postsound onset at electrode 6 and53–76 ms at electrode 7. Using FWER corrections, the differ-ences observed before 100 ms remained significant at electrode6. Interestingly, this electrode was near the anterior calcarinesulcus, a region that retinotopically maps onto the peripheralvisual field, whereas the early auditory-evoked response wasabsent at electrodes 8 and 9 in the posterior calcarine sulcus, aregion that retinotopically maps onto the central visual field,suggestive of a coarse retinotopic mapping of peripheralsounds within a visual hemifield (note that all electrodes inpatient 1 were located in the anterior calcarine sulcus).

In addition to the early contralateral-ipsilateral differences(�100 ms), electrodes 2 and 3 in patient 1 and electrodes 6-9in patient 2 showed significant differences in later time win-dows (200–500 ms; see Fig. 2). These later differences, ob-tained from both the anterior and posterior calcarine electrodes,may underlie the long-latency contralateral occipital positivity(over 200–500 ms) observed by McDonald and colleagues(2013) using scalp recordings.

To confirm that these early differences were driven bymodulation of neural activity elicited by the contralateralsounds (and not by the ipsilateral sounds), we separatelyanalyzed the contralateral and ipsilateral ECoG-ERP wave-forms for the anterior calcarine electrodes (electrodes 1-4 inpatient 1 and electrodes 5-7 in patient 2) relative to theirrespective null baselines (see MATERIALS AND METHODS). In fiveof these seven electrodes, the early differences were driven by

Fig. 2. Electrocorticographic (ECoG)-event-related potentials (ERPs) evokedby sounds presented contralateral (orange lines) or ipsilateral (blue lines) todepth electrodes (yellow circles) along the calcarine sulcus (green regions). A:patient 1. B: patient 2. Maximal differences between contralateral and ipsilat-eral conditions were obtained along the anterior calcarine sulcus (electrodes 1,3, and 4 for patient 1 and electrode 6 for patient 2), which maps to peripheralvisual locations. Orange and blue shaded regions represent means � SE. Grayboxes highlight statistically significant intervals based on P � 0.05 across 10or more contiguous time points (see main text for a more conservativeanalysis). R, right; L, left.

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increased responses to contralateral sounds over baseline be-ginning 28–53 ms after sound onset: electrode 1 (28–87 ms),electrode 2 (53–87 ms), electrode 3 (52–72 ms), electrode 4(34–97 ms), and electrode 6 (50–76 ms); these significantdifferences were confirmed at electrodes 1, 4, and 6 aftercontrolling for the FWER at P � 0.05. Critically, ipsilateralsounds evoked no significant changes in activity relative tobaseline in the 1st 100 ms at any of these seven electrodes,suggesting that peripheral sounds have privileged early accessto contralateral visual cortex.

To compare the timing of auditory-evoked and visual-evoked activity in visual cortex, we analyzed responses tovisual stimuli at these electrodes. Although retinotopic map-ping was unavailable for these patients, we recorded responsesto full-field luminance changes elicited by eye blinks (Gawneand Martin 2000) in patient 1 and responses to centrally flashedvisual stimuli in patient 2. Significant visual activity beganbetween 39 and 58 ms (Fig. 3; significant responses before 100ms at electrodes 1-4 and 9 were confirmed after controlling forthe FWER at P � 0.05). The full-field luminance changesevoked strong activity from all four anterior calcarine elec-trodes (Fig. 3A), whereas the centrally flashed images evokedactivity only from electrodes neighboring the posterior calca-rine sulcus (Fig. 3B). Importantly, contralateral sounds elicitedvisual cortical responses (Fig. 2) as rapidly as did visual stimuli(Fig. 3).

To compare the timing of auditory-evoked activity betweenvisual and auditory cortices, we analyzed auditory corticalresponses to the noise bursts for patient 1 (patient 2 did nothave any superior temporal gyrus electrodes that showed sig-nificant auditory responses). Figure 4 shows the auditory ac-tivity from 6 electrodes along a single depth probe penetratingthe inferior side of the superior temporal sulcus. Maximal earlyresponses were observed at the 2 most medial electrodes (15mm inferior to primary auditory cortex; Fig. 4, top 2 panels)beginning at 26 ms (confirmed after controlling for the FWERat P � 0.05). Crucially, contralateral sounds elicited visualcortical responses (Fig. 2) nearly as rapidly as they elicitedauditory cortical responses (Fig. 4).

As we observed maximal auditory-evoked responses fromperipheral sounds at electrodes along the anterior calcarinesulcus, which maps retinotopically to peripheral regions ofvisual space, these data provide preliminary evidence of asound-based spatial topography in visual cortex that operates ata resolution finer than visual hemifields. Although this patternwas observed in both patients, unexpectedly, no differencebetween contralateral and ipsilateral sounds was observed atthe most anterior electrode in patient 2 (electrode 5). However,as Fig. 3 shows, the responses to visual stimuli at this electrodediffered markedly from those at the remaining electrodes inpatient 2, raising the possibility that this electrode was in factoutside of calcarine sulcus. If so, our results of anterior calca-rine activation by peripheral sounds (Fig. 2) and posteriorcalcarine activation by central visual images (Fig. 3B) isconsistent with the possibility that sounds generate spatiallyselective activity in primary visual cortex. However, the de-termination of the extent of sound-based spatial selectivity invisual cortex would require systematic spatial sampling ofvisual and auditory stimuli to compare the visual and auditoryspatial selectivity for each calcarine electrode.

A general concern of both surface and intracranial electro-physiological recordings is an uncertainty of the spatial spec-ificity of the observed potentials as dipolar electrical activitymay spread through neighboring tissue (i.e., far-field effects).To mitigate this risk, we additionally examined the ECoG-ERPs using local common average referencing in which theaverage electrical activity generated by all electrodes alongeach depth probe was subtracted from the activity generated by

Fig. 3. ECoG-ERPs evoked by full-field luminance changes at blink offsets inpatient 1 (A) or by centrally flashed visual images in patient 2 (B) recordedfrom depth electrodes (white circles) along the calcarine sulcus (dark grayregions). As seen in A, full-field luminance changes evoked strong activityfrom all 4 anterior calcarine electrodes. As seen in B, central flashes evokedactivity only from posterior calcarine electrodes that map to central visuallocations, with significant activity obtained from the most posterior electrode.Shaded regions represent means � SE. Gray boxes highlight statisticallysignificant intervals based on P � 0.05 across 10 or more contiguous timepoints (see main text for a more conservative analysis).

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each electrode on the probe. This local referencing schemeensures that any spatially dispersed activity present broadly ateach of the 5.5-cm depth electrode probes is removed whilepreserving the signal unique to the local cortex. Using thislocal referencing framework, the pattern of results was un-changed. To confirm further that the observed potentials weregenerated locally along the calcarine sulci, we examined ac-tivity at the depth electrodes adjacent to (but not along) thecalcarine sulcus (gray circles closest to the yellow circles in

Fig. 2); neither of the two electrodes in patient 1 nor the twoelectrodes in patient 2 showed significant differences betweencontralateral and ipsilateral sounds at any time point.

Another potential concern could be the impact of patients’inadvertent eye movements to the sound source. Although eyemovements were not rigorously monitored in these patients, inthe study of McDonald et al. (2013), which presented lateral-ized sounds very similar to those used here, the sounds did notelicit any eye deviations as measured by the electrooculogram.In addition, the early onset of the auditory-evoked visualcortical responses (�50 ms) precludes the possibility that eyemovements contaminated our ECoG-ERP results because sac-cade-induced neural responses in primary visual cortex occur50–100 ms postsaccade onset (e.g., Kagan et al. 2008). More-over, experimenters monitored patients’ gaze position through-out the study, providing feedback to the patients if their eyesdeviated from the central fixation cross.

DISCUSSION

In two patients with uncommon but fortuitously locateddepth electrodes within the calcarine sulcus, we found evi-dence that peripheral auditory signals rapidly (beginning be-tween 28 and 45 ms) evoke spatially specific responses inprimary visual cortex. The early responses were driven bycontralateral (but not ipsilateral) sounds and were maximal atanterior calcarine sites, suggesting that auditory spatial infor-mation coarsely follows retinotopic mapping in visual cortex.This rapid transfer of peripheral spatial information fromauditory to visual processing may play a role in initiatingattentional and/or saccadic shifts. Whereas the present resultsshowed both early (28–100 ms) and later (200–500 ms)activation of visual cortex by sounds, McDonald and col-leagues (2013) only observed the late component possibilitydue to the low sensitivity of scalp-recorded ERPs to calcarineactivity originating several centimeters away from the surfaceof the scalp.

The current finding is consistent with well-documentedperceptual benefits of sounds on visual perception (e.g., Mc-Donald et al. 2000; Romei et al. 2007) particularly whensounds and visual targets are spatially coincident. It is alsoconsistent with reports of early multisensory interactions inhuman visual cortex (Cappe et al. 2010; Raij et al. 2010) andthe broadly spatiotopic responses of visual cortical neurons tosounds in the cat (Morrell 1972). Intriguingly, we found thatthe earliest auditory activation (28 ms) of primary visual cortexby contralateral sounds preceded the earliest visual activation(39 ms) of primary visual cortex by visual stimuli, raising thepossibility that a contralateral auditory cue might spatiotopi-cally bias visual processing toward the location of an upcomingvisual object before the onset of visually evoked activity.Additional research is necessary to confirm this possibility aswell as to investigate what additional types of auditory infor-mation are rapidly relayed to primary visual cortex and howthey benefit perceptual processing.

The rapid auditory activation of visual cortex that we foundcould be mediated by direct connections between primaryauditory and primary visual cortices (Falchier et al. 2002;Rockland and Ojima 2003) and/or by auditory subcorticalinputs to visual cortex (Cappe et al. 2009). Whatever the neuralconnections that mediate the rapid auditory input to visual

Fig. 4. ECoG-ERPs evoked by sounds at depth electrodes (white circles) in auditoryareas in patient 1 (averaged for sounds presented contralateral and ipsilateral to theelectrodes). ECoG-ERPs show a short latency negative deflection followed by apositive deflection at 100 ms. Shaded regions represent means � SE. Gray boxeshighlight statistically significant intervals based on P � 0.05 across 10 or morecontiguous time points (see main text for a more conservative analysis).

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cortex, the current findings suggest that those connections mapearly auditory spatial coding in primary auditory cortex (Leeand Middlebrooks 2011) or in subcortical areas (Cappe et al.2009) onto the retinotopic coding of visual space in primaryvisual cortex.

GRANTS

This study was supported by National Institute on Deafness and OtherCommunication Disorders Grant K99-DC-013828, National Eye InstituteGrant R01-EY-021184, National Science Foundation Grant BCS-1029084,National Institute of Mental Health Grant 7P50-MH-086385, and NationalInstitute of Neurological Disorders and Stroke Grant 2T32-NS-047987.

DISCLOSURES

No conflicts of interest, financial or otherwise, are declared by the author(s).

AUTHOR CONTRIBUTIONS

D.B., S.S., S.A.H., and M.G. conception and design of research; D.B.,V.L.T., Z.D., J.T., and S.W. performed experiments; D.B., S.D.T., and Z.D.analyzed data; D.B., S.S., S.A.H., and M.G. interpreted results of experiments;D.B. prepared figures; D.B. drafted manuscript; D.B., V.L.T., S.S., S.A.H.,S.D.T., Z.D., J.T., S.W., and M.G. edited and revised manuscript; D.B.,V.L.T., S.S., S.A.H., S.D.T., Z.D., J.T., S.W., and M.G. approved final versionof manuscript.

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