OPINION ARTICLEpublished: 19 July 2013

doi: 10.3389/fnhum.2013.00387

On the all-or-none rule of conscious perceptionTalis Bachmann*

Institute of Public Law and Institute of Psychology, University of Tartu, Tartu, Estonia*Correspondence: talis.bachmann@ut.ee

Edited by:

Josef Parvizi, Stanford School of Medicine, USA

Reviewed by:

Naotsugu Tsuchiya, Monash University, AustraliaKrithiga Sekar, New York University School of Medicine, USA

What are the true functional under-pinnings of perception, emotion, con-sciousness, and subconscious processesremains an unsolved question (Alivisatoset al., 2012). For example, it seems some-what mysterious how one and the samestructure of neural circuits—the humanbrain—sometimes allows conscious expe-rience and sometimes does not allow it. Weeven do not know whether this owes to thealternating activity of different circuits, thechange in the activity of the same circuits,or both.

Nobody denies accumulation of perti-nent data on where and how the changesin neural activity correlate with consciousexperience. For instance, specific and non-specific thalamocortical systems providecircuits for representing the contents andguaranteeing the state of consciousness(Ribary, 2005; Liu et al., 2013), processesin the higher level sensory-perceptual cor-tical areas tend to correlate with awarenessmore than the processes in the primaryareas (Logothetis et al., 1996; Hesselmannet al., 2011), reentrant activity from higherto lower level nodes seems to constitute atypical feature of circuits involved in con-scious perception (Lamme, 2010), etc. Yet,many principal questions have remainedwithout answers. For example, we do notknow whether conscious experience of astimulus is a gradually emerging attributeof the activity of the corresponding neu-ral circuits or is it an effect appearingabruptly as soon as a corresponding neuralmarker appears. Recently, a notable studywas published trying to shed light on thisunsolved problem (Sekar et al., 2013).

Sekar et al. (2013) recorded neuro-magnetic responses in temporoparietalchannels and found that the MEGresponse peaking about 240 milliseconds(ms) after stimulus reliably discriminatedtrials with stimulus awareness from trials

lacking stimulus awareness. Importantly,this MEG-marker was expressed withan equal magnitude across trials wheresubjects reported different subjectivegradations of stimulus experience, butwas decreased when no awareness wasreported. Conscious experience was inter-preted as emerging according to the allor none, rule. The different subjectivegradations used for sampling the tri-als for comparative event-related fields(ERF) analysis were “didn’t see” for theunaware condition and “couldn’t iden-tify,” “unsure,” and “sure” for the threeconditions with changing awareness lev-els. Several features of this work make it alandmark contribution to the research onneural correlates of consciousness (NCC).

A confound between physical variabil-ity of stimulation and the putative NCC-markers has been a typical obstacle forobtaining clearcut information on NCC(Bachmann, 2009). Sekar et al. (2013)kept threshold-level stimulation invariantand measured variable MEG responsesas a correlate of the varying subjectiveresponses, avoiding co-variation betweenthe effects of varying physical stimula-tion and brain processes underlying sub-jective phenomena. Furthermore, while inthe majority of earlier research on NCCobjective categorical responses have beenused as the dependent measure, gradedsubjective responses in addition to objec-tive discrimination measures were used(Sekar et al., 2013). Obviously, temporalresolution of the brain-imaging methodssuitable for studying the fast formationof conscious perception should be com-patible with the corresponding fast brainprocesses; on the other hand, to under-stand the precise brain circuits involved inproducing conscious perception, imagingshould enable 3D analysis. In the majorityof earlier research on NCC the recording

methods have been either slow (fMRI,PET) or fast but controversial in termsof source analysis (EEG). Furthermore,recently it was shown that subjective expe-rience of a stimulus can vary between“seen” and “unseen” while fMRI recordingdata could not differentiate between thesetwo alternative conditions (Schoenfeldet al., 2011). Using MEG (Sekar et al.,2013) these limitations were surpassed atonce. Yet, in spite of these advantages Sekaret al. paper cannot be conclusive in settlingthe issue about graduality vs. “quantal steplike” nature of conscious perception.

(1) Because MEG recording criticallydepends on synchrony of (dendritic) neu-ral activity, the accounts of conscious-ness mechanisms requiring no synchronyfor NCC and the corresponding recordingmethods may suggest different solutions(He and Raichle, 2009). (2) Whether tran-sition between states is instantaneous orgradual (“quantal” vs. “wave-like”) maydepend on the time scale considered. Thecellular and sub-cellular level processesresponsible for awareness may lead toa gradual change of state (e.g., mem-brane potential) occurring at the millisec-ond time-scale although this may appear“instantaneous” if looked at from thetimescale where the unit time is sev-eral orders higher. Although the peaksof MEG-responses indicative of stimu-lus awareness were statistically invariant(Sekar et al., 2013), the pre-peak ascendingphase of the response was gradual cover-ing about 50–100 ms. Even though supra-threshold stimulus-awareness may be allor none, the formation of the contentsof a conscious percept may be gradual,albeit very fast. (3) Because MEG datawas collected for parieto-temporal areasand analogous data about occipital sourceswere not reported (Sekar et al., 2013) wedo not know whether earlier responses in

Frontiers in Human Neuroscience www.frontiersin.org July 2013 | Volume 7 | Article 387 | 1

HUMAN NEUROSCIENCE

Bachmann On the all-or-none rule of conscious perception

occipital sources also would have shownanalogous results. Moreover, it is uncertainwhether we deal with true NCC or withmarkers of activity of the mechanisms con-trolling response choice or their top-downeffects. Circuits located more dorsally aremore access- and control-related com-pared to the temporal and occipital circuitsthat are more perceptual content related.A recently suggested (Aru et al., 2012; deGraaf et al., 2012) requirement to differ-entiate processes that are prerequisite forNCC, aftereffects of NCC, and true NCCwas not followed by Sekar et al. (2013). (4)According to this study the earliest markerof the varying awareness appears at 240 mspost stimulus. However, peak latency neednot be the only viable indicator of theprocess we are interested in. Instead, ERFdeviation change (e.g., some critical valueof derivatives of wave function) or somecharacteristic of ERF function’s envelopespanning a time epoch inclusive of shorterdelays (compared to peak delay) may showa different time-course. Moreover, whena stimulus with its energy at discrimi-nation threshold is used, the process ofpercept formation typically unfolding ata faster rate may be considerably pro-longed and the estimates of the fastesttimes with which a stimulus can reach con-sciousness become too much conservative.Thus, instead of the 240 ms, about 150 mswould be a correct value for the fastestdelay of visual awareness. (For example,with suprathreshold, high contrast targetsbackward masking disappears when maskis delayed by 150 ms or more—Bachmann,1994.) (5) Although statistical analysis onthe ERF peak amplitude values of the com-ponent delayed by 240 ms showed no dif-ference between three subjective awarenessconditions, visual inspection of the cor-responding magnetic flux data (Figure 4,

Sekar et al., 2013) showed a systematicincrease with increasing subjective esti-mates of the experienced contents. Thus,with more measurements statistically sig-nificant results indicative of the grad-ual change of ERF peak values could beobtained in principle.

Notwithstanding the debatable aspectsof the Sekar et al. (2013) work, it seemsa contribution providing standards forthe researchers who aim at finding howneural circuits help make the processedperceptual data consciously experienced.Invariance of physical stimulation com-bined with variability of subjective mea-sures, using a gradual scale of subjectivemeasurement, and using recording andanalysis methods allowing location of thecircuits of interest in 3D are among theprime requirements. Of course, not alllandmark publications must carry ulti-mate truths, but they at least show howresearch on NCC should be conducted ina methodologically rigorous way.

ACKNOWLEDGMENTSSupport from Estonian Ministry of Scienceand Education (SF0180027s12) is grate-fully acknowledged.

REFERENCESAlivisatos, A. P., Chun, M., Church, G. M., Greenspan,

R. J., Roukes, M. L., and Yuste, R. (2012). Thebrain activity map project and the challenge offunctional connectomics. Neuron 74, 970–974. doi:10.1016/j.neuron.2012.06.006

Aru, J., Bachmann, T., Singer, W., and Melloni, L.(2012). Distilling the neural correlates of con-sciousness. Neurosci. Biobehav. Rev. 36, 737–746.doi: 10.1016/j.neubiorev.2011.12.003

Bachmann, T. (1994). Psychophysiology of VisualMasking. Commack, NY: Nova.

Bachmann, T. (2009). Finding ERP-signatures of tar-get awareness: puzzle persists because of experi-mental co-variation of the objective and subjec-tive variables. Conscious. Cogn. 18, 804–808. doi:10.1016/j.concog.2009.02.011

de Graaf, T. A., Hsieh, P. J., and Sack, A. T. (2012).The ‘correlates’ in neural correlates of conscious-ness. Neurosci. Biobehav. Rev. 36, 191–197. doi:10.1016/j.neubiorev.2011.05.012

He, B. J., and Raichle, M. E. (2009). The fMRIsignal, slow cortical potential and conscious-ness. Trends Cogn. Sci. 13, 302–309. doi:10.1016/j.tics.2009.04.004

Hesselmann, G., Hebart, M., and Malach, R. (2011).Differential BOLD activity associated with subjec-tive and objective reports during “blindsight” innormal observers. J. Neurosci. 31, 12936–12944.doi: 10.1523/JNEUROSCI.1556-11.2011

Lamme, V. A. F. (2010). How neuroscience will changeour view on consciousness. Cogn. Neurosci. 1,204–240. doi: 10.1080/17588921003731586

Liu, X., Lauer, K. K., Ward, D. B., Li, S.-J., and Hudetz,A. G. (2013). Differential effects of deep sedationwith propofol on the specific and nonspecific tha-lamocortical systems. A functional magnetic res-onance imaging study. Anesthesiology 118, 59–69.doi: 10.1097/ALN.0b013e318277a801

Logothetis, N. K., Leopold, D. A., and Sheinberg,D. L.,(1996).What is rivaling during binoc-ular rivalry? Nature 380, 621–624. doi:10.1038/380621a0

Ribary, U. (2005). Dynamics of thalamo-cortical net-work oscillations and human perception. Prog.Brain Res. 150, 127–142. doi: 10.1016/S0079-6123(05)50010-4

Schoenfeld, M. A., Hassa, T., Hop, J.-M., Eulitz, C.,and Schmidt, R. (2011). Neural correlates of hys-terical blindness. Cereb. Cortex 21, 2394–2398. doi:10.1093/cercor/bhr026

Sekar, K., Findley, W. M., Poeppel, D., and Llinás, R.(2013). Cortical response tracking the consciousexperience of threshold duration visual stimuliindicates visual perception is all or none. Proc.Natl. Acad. Sci. U.S.A. 110, 5642–5647. doi:10.1073/pnas.1302229110

Received: 10 June 2013; accepted: 04 July 2013;published online: 19 July 2013.Citation: Bachmann T (2013) On the all-or-none rule ofconscious perception. Front. Hum. Neurosci. 7:387. doi:10.3389/fnhum.2013.00387Copyright © 2013 Bachmann. This is an open-accessarticle distributed under the terms of the CreativeCommons Attribution License, which permits use, dis-tribution and reproduction in other forums, providedthe original authors and source are credited and sub-ject to any copyright notices concerning any third-partygraphics etc.

Frontiers in Human Neuroscience www.frontiersin.org July 2013 | Volume 7 | Article 387 | 2