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Clarifying frequency-dependent brightness enhancement: delta- and theta-band flicker, not alpha-band flicker, consistently seen as brightest

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Abstract

Frequency-dependent brightness enhancement, a perceptual illusion in which a flickering light can appear twice as bright as a constant light, has historically been reported to produce maximum effects at a flicker rate within the alpha (8–12 Hz) band (Bartley in J Exp Psychol 23(3):313–319, 1938). Our recent examinations of this phenomenon using brightness discrimination between two flickering stimuli, however, have instead revealed the brightest percepts from theta-band (4–7 Hz) flicker (Bertrand et al. in Sci Rep 8(1):6152, 2018). Two primary questions arise from these seemingly contradictory findings: first, could task differences between these studies have caused recruitment of discrete oscillatory processes? Second, could the reported theta-band flicker enhancement be the result of an aliased alpha rhythm, sequentially sampling two stimulus locations, resulting in an ~ 5 Hz half-alpha rhythm? Here, we investigated these questions with two experiments: one replicating Bartley’s (1938) adjustment paradigm, and one containing both Bartley’s adjustment task and Bertrand’s (2018) discrimination task, but presenting stimuli only sequentially (rather than concurrently). Examination of a range of frequencies (2–12 Hz) revealed the greatest brightness enhancement arising from flicker in the delta- and theta-band across all conditions, regardless of the spatial or temporal configuration of the stimuli. We speculate that these slower rhythms play an integral role in complex visual operations (e.g., a discrimination decision) where the entrainment of the endogenous neural rhythm to matched exogenous rhythmic stimulation promotes more efficient processing of visual information and thus produces perceptual biases as seen in frequency-dependent brightness enhancement.

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References

  • Bartley SH (1938) Subjective brightness in relation to flash rate and the light–dark ratio. J Exp Psychol 23(3):313–319

    Article  Google Scholar 

  • Bertrand JK, Wispinski NJ, Mathewson KE, Chapman CS (2018) Entrainment of theta, not alpha, oscillations is predictive of the brightness enhancement of a flickering stimulus. Sci Rep 8(1):6152

    Article  Google Scholar 

  • Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436

    CAS  Article  Google Scholar 

  • Burgess AP, Gruzelier JH (1997) Short duration synchronization of human theta rhythm during recognition memory. Neuroreport 8(4):1039–1042

    CAS  Article  Google Scholar 

  • Busch NA, VanRullen R (2010) Spontaneous EEG oscillations reveal periodic sampling of visual attention. Proc Natl Acad Sci USA 107(37):16048–16053

    CAS  Article  Google Scholar 

  • Busch NA, Dubois J, VanRullen R (2009) The phase of ongoing EEG oscillations predicts visual perception. J Neurosci 29(24):7869–7876

    CAS  Article  Google Scholar 

  • Buschman TJ, Kastner S (2015) From behavior to neural dynamics: an integrated theory of attention. Neuron 88(1):127–144

    CAS  Article  Google Scholar 

  • Buzsaki G (2006) Rhythms of the brain. Oxford University Press, Oxford

    Book  Google Scholar 

  • Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926–1929

    Article  Google Scholar 

  • Calderone DJ, Lakatos P, Butler PD, Castellanos FX (2014) Entrainment of neural oscillations as a modifiable substrate of attention. Trends Cogn Sci 18(6):300–309

    Article  Google Scholar 

  • Cramer AOJ, van Ravenzwaaij D, Matzke D, Steingroever H, Wetzels R, Grasman RPPP, Waldrop LJ, Wagenmakers EJ (2016) Hidden multiplicity in exploratory multiway ANOVA: prevalence and remedies. Psychon Bull Rev 23(2):640–647

    Article  Google Scholar 

  • Cravo AM, Rohenkohl G, Wyart V, Nobre AC (2013) Temporal expectation enhances contrast sensitivity by phase entrainment of low-frequency oscillations in visual cortex. J Neurosci 33(9):4002–4010

    CAS  Article  Google Scholar 

  • Crouzet SM, VanRullen R (2017) The rhythm of attentional stimulus selection during visual competition. bioRxiv. https://doi.org/10.1101/105239

    Article  Google Scholar 

  • Dugué L, Marque P, VanRullen R (2015) Theta oscillations modulate attentional search performance periodically. J Cogn Neurosci 27(5):945–958

    Article  Google Scholar 

  • Fiebelkorn IC, Kastner S (2018) A rhythmic theory of attention. Trends Cogn Sci 23(2):87–101

    Article  Google Scholar 

  • Fiebelkorn IC, Saalmann YB, Kastner S (2013) Rhythmic sampling within and between objects despite sustained attention at a cued location. Curr Biol 23(24):2553–2558

    CAS  Article  Google Scholar 

  • Glad A, Magnussen S (1972) Darkness enhancement in intermittent light: an experimental demonstration. Vis Res 12(1):111–115

    CAS  Article  Google Scholar 

  • Gulbinaite R, van Viegen T, Wieling M, Cohen MX, VanRullen R (2017) Individual alpha peak frequency predicts 10 Hz flicker effects on selective attention. J Neurosci 37(42):10173–10184

    CAS  Article  Google Scholar 

  • Han B, VanRullen R (2016) Shape perception enhances perceived contrast: evidence for excitatory predictive feedback? Sci Rep. https://doi.org/10.1038/srep22944

    Article  PubMed  PubMed Central  Google Scholar 

  • Han B, VanRullen R (2017) The rhythms of predictive coding? Pre-stimulus phase modulates the influence of shape perception on luminance judgments. Sci Rep. https://doi.org/10.1038/srep43573

    Article  PubMed  PubMed Central  Google Scholar 

  • Harris AM, Dux PE, Jones CN, Mattingley JB (2017) Distinct roles of theta and alpha oscillations in the involuntary capture of goal-directed attention. Neuroimage 152:171–183

    Article  Google Scholar 

  • Harris AM, Dux PE, Mattingley JB (2018) Detecting unattended stimuli depends on the phase of prestimulus neural oscillations. J Neurosci 38(12):3092–3101

    CAS  Article  Google Scholar 

  • Hogendoorn H (2016) Voluntary saccadic eye movements ride the attentional rhythm. J Cogn Neurosci 28(10):1625–1635

    Article  Google Scholar 

  • Holcombe AO, Chen WY (2013) Splitting attention reduces temporal resolution from 7 Hz for tracking one object to < 3 Hz when tracking three. J Vis 13:1–19

    Article  Google Scholar 

  • Hutcheon B, Yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23(5):216–222

    CAS  Article  Google Scholar 

  • Jensen O, Mazaheri A (2010) Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2010.00186

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim YJ, Grabowecky M, Paller K, Suzuki S (2011) Differential roles of frequency-following and frequency-doubling visual responses revealed by evoked neural harmonics. J Cogn Neurosci 23(8):1875–1886

    Article  Google Scholar 

  • Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Rev 29(2–3):169–195

    CAS  Article  Google Scholar 

  • Klimesch W, Doppelmayr M, Russegger H, Pachinger T (1996) Theta band power in the human scalp EEG and the encoding of new information. Neuroreport 7:1235–1240

    CAS  Article  Google Scholar 

  • Klimesch W, Doppelmayr M, Schimke H, Ripper B (1997) Theta synchronization and alpha desynchronization in a memory task. Psychophysiology 34(2):169–176

    CAS  Article  Google Scholar 

  • Klimesch W, Doppelmayr M, Russegger H, Pachinger T, Schwaiger J (1998) Induced alpha band power changes in the human EEG and attention. Neurosci Lett 244(2):73–76

    CAS  Article  Google Scholar 

  • Klimesch W, Sauseng P, Hanslmayr S (2007) EEG alpha oscillations: the inhibition–timing hypothesis. Brain Res Rev 53(1):63–88

    Article  Google Scholar 

  • Kohn H, Salisbury I (1967) Electroencephalographic indications of brightness enhancement. Vis Res 7(5–6):461–468

    CAS  Article  Google Scholar 

  • Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE (2008) Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320(5872):110–113

    CAS  Article  Google Scholar 

  • Landau AN, Fries P (2012) Attention samples stimuli rhythmically. Curr Biol 22(11):1000–1004

    CAS  Article  Google Scholar 

  • Lopes da Silva F (1992) The rhythmic slow activity (theta) of the limbic cortex: an oscillation in search of a function. In: Baar E et al (eds) Induced rhythms in the brain. Springer Science, New York, pp 83–102

    Chapter  Google Scholar 

  • Macdonald JS, Cavanagh P, VanRullen R (2014) Attentional sampling of multiple wagon wheels. Atten Percept Psychophys 76(1):64–72

    Article  Google Scholar 

  • Magnussen S, Glad A (1975) Brightness and darkness enhancement during flicker: perceptual correlates of neuronal B-and D-systems in human vision. Exp Brain Res 22(4):399–413

    Article  Google Scholar 

  • Mathewson KE, Gratton G, Fabiani M, Beck DM, Ro T (2009) To see or not to see: prestimulus α phase predicts visual awareness. J Neurosci 29(9):2725–2732

    CAS  Article  Google Scholar 

  • Mathewson KE, Prudhomme C, Fabiani M, Beck DM, Lleras A, Gratton G (2012) Making waves in the stream of consciousness: entraining oscillations in EEG alpha and fluctuations in visual awareness with rhythmic visual stimulation. J Cogn Neurosci 24(12):2321–2333

    Article  Google Scholar 

  • Nelson TM, Bartley SH, Jewell RM (1963) Effects upon brightness produced by varying the length of the null interval separating successive “single” pulses: sensory implications of the alternation of response theory, I. J Psychol 56(1):99–106

    Article  Google Scholar 

  • Palva S, Palva JM (2011) Functional roles of alpha-band phase synchronization in local and large-scale cortical networks. Front Psychol. https://doi.org/10.3389/fpsyg.2011.00204

    Article  PubMed  PubMed Central  Google Scholar 

  • Rager G, Singer W (1998) The response of cat visual cortex to flicker stimuli of variable frequency. Eur J Neurosci 10:1856–1877

    CAS  Article  Google Scholar 

  • Sokoliuk R, VanRullen R (2013) The flickering wheel illusion: when α rhythms make a static wheel flicker. J Neurosci 33(33):13498–13504

    CAS  Article  Google Scholar 

  • Spaak E, de Lange FP, Jensen O (2014) Local entrainment of alpha oscillations by visual stimuli causes cyclic modulation of perception. J Neurosci 34(10):3536–3544

    CAS  Article  Google Scholar 

  • VanRullen R (2016) Perceptual cycles. Trends Cogn Sci 20(10):723–735

    Article  Google Scholar 

  • VanRullen R, Koch C (2003) Is perception discrete or continuous? Trends Cogn Sci 7(5):207–213

    Article  Google Scholar 

  • Wang XJ (2010) Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90(3):1195–1268

    Article  Google Scholar 

  • Wang D, Clouter A, Chen Q, Shapiro KL, Hanslmayr S (2018) Single-trial phase entrainment of theta oscillations in sensory regions predicts human associative memory performance. J Neurosci. https://doi.org/10.1523/jneurosci.0349-18.2018

    Article  PubMed  PubMed Central  Google Scholar 

  • Wispinski NJ, Gallivan JP, Chapman CS (2018) Model, movements, and minds: bridging the gap between decision making and action. Ann N Y Acad Sci. https://doi.org/10.1111/nyas.13973

    Article  PubMed  Google Scholar 

  • Wutz A, Muschter E, van Koningsbruggen MG, Weisz N, Melcher D (2016) Temporal integration windows in neural processing and perception aligned to saccadic eye movements. Curr Biol 26(13):1659–1668

    CAS  Article  Google Scholar 

  • Wyart V, De Gardelle V, Scholl J, Summerfield C (2012) Rhythmic fluctuations in evidence accumulation during decision making in the human brain. Neuron 76(4):847–858

    CAS  Article  Google Scholar 

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Correspondence to Jennifer K. Bertrand.

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Bertrand, J.K., Ouellette Zuk, A.A. & Chapman, C.S. Clarifying frequency-dependent brightness enhancement: delta- and theta-band flicker, not alpha-band flicker, consistently seen as brightest. Exp Brain Res 237, 2061–2073 (2019). https://doi.org/10.1007/s00221-019-05568-1

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Keywords

  • Visual perception
  • Flicker
  • Brightness enhancement
  • Neural oscillations
  • Discrimination