Elsevier

Neuropsychologia

Volume 66, January 2015, Pages 18-31
Neuropsychologia

A robust index of lexical representation in the left occipito-temporal cortex as evidenced by EEG responses to fast periodic visual stimulation

https://doi.org/10.1016/j.neuropsychologia.2014.11.007Get rights and content

Highlights

  • We identify a robust electrophysiological response for written words vs. pseudowords.

  • The selective response to words is found over left occipito-temporal sites.

  • Discrimination responses are found in individual participants in a few minutes.

  • The effect is discussed as stemming from orthographic or lexico-semantic level.

  • Fast periodic visual stimulation opens an avenue to study written language.

Abstract

Despite decades of research on reading, including the relatively recent contributions of neuroimaging and electrophysiology, identifying selective representations of whole visual words (in contrast to pseudowords) in the human brain remains challenging, in particular without an explicit linguistic task. Here we measured discrimination responses to written words by means of electroencephalography (EEG) during fast periodic visual stimulation. Sequences of pseudofonts, nonwords, or pseudowords were presented through sinusoidal contrast modulation at a periodic 10 Hz frequency rate (F), in which words were interspersed at regular intervals of every fifth item (i.e., F/5, 2 Hz). Participants monitored a central cross color change and had no linguistic task to perform. Within only 3 min of stimulation, a robust discrimination response for words at 2 Hz (and its harmonics, i.e., 4 and 6 Hz) was observed in all conditions, located predominantly over the left occipito-temporal cortex. The magnitude of the response was largest for words embedded in pseudofonts, and larger in nonwords than in pseudowords, showing that list context effects classically reported in behavioral lexical decision tasks are due to visual discrimination rather than decisional processes. Remarkably, the oddball response was significant even for the critical words/pseudowords discrimination condition in every individual participant. A second experiment replicated this words/pseudowords discrimination, and showed that this effect is not accounted for by a higher bigram frequency of words than pseudowords. Without any explicit task, our results highlight the potential of an EEG fast periodic visual stimulation approach for understanding the representation of written language. Its development in the scientific community might be valuable to rapidly and objectively measure sensitivity to word processing in different human populations, including neuropsychological patients with dyslexia and other reading difficulties.

Introduction

In alphabetic script, words are constituted of letters combined with specific orthographic and phonological rules and conveying a meaning. Though complex, reading proceeds rapidly and effortlessly in literate adults (85–90% of adults across the world). A skilled reader reads about five words per second in a text, so that word identification takes only about 200 ms (Rayner, 1998, Rayner et al., 2012). However, despite decades of research on this uniquely human ability, whether there are brain processes dedicated to automatic (i.e. without any explicit judgment task) discrimination of a valid visual word from a meaningless orthographically legal string of letters (i.e., a pseudoword) remains an outstanding issue. To address this issue, the present study introduces an original paradigm of EEG recording during fast periodic stimulation of visual words.

Behaviorally, a widely used task for assessing word recognition is the lexical decision task (LDT, Rubenstein et al., 1970), in which participants decide as rapidly as possible if a visually presented letter string is a word as opposed to a nonword (i.e., orthographically illegal) or a pseudoword (i.e., orthographically legal). This task has allowed to identify many variables that affect lexical decision performance, whether intrinsic to stimuli (e.g., frequency, length, orthographic regularity, semantic concreteness, number of semantic attributes, etc.), or extrinsic to stimuli (e.g., effects of the surrounding list as word-likeness at phonological or orthographic levels), constraining functional models of reading to account for these influences along the visual word recognition processes (see Balota et al. (2006) for a review; Grainger, 2008). The LDT has also helped distinguishing between subtypes of surface dyslexia since it provides access to the functional locus of a patient’s deficit without requiring a phonological output (Friedmann and Lukov, 2008). However, since the LDT requires explicit attention to, and decision about, strings of letters, it measures the outcome of several perceptual, cognitive and decisional processes. Consequently, behavioral studies using LDTs have been unable to determine whether selective representations of visual words can be activated without explicit judgments of the words, an outstanding issue in the reading literature (Shtyrov et al., 2013).

At first glance, since electro- or magneto-encephalography (EEG, MEG) can reveal differential brain responses without requiring explicit processing of the stimuli, this technique seems particularly well suited to address this issue. A visual word presented centrally triggers a negative event-related potential (ERP) peaking over left occipito-temporal sites around 170 milliseconds (ms), the word-related N170 (e.g., Bentin et al., 1999; Rossion et al., 2003; Maurer et al., 2005; Yoncheva et al., 2010) or the M170 in MEG (e.g. Tarkiainen et al., 1999). This component is larger in response to alphabetic items than to nonalphabetic strings such as pseudofonts, symbols and shapes (Bentin et al., 1999, Tarkiainen et al., 2002, Brem et al., 2009) and has been associated with a source in the left ventral occipito-temporal region (Maurer et al., 2005, Cohen et al., 2000). However, most studies report no N170 difference between words and pseudowords, or relatively late differential responses (after 200 ms) over more anterior regions (Bentin et al., 1999; Cohen et al., 2002; Wydell et al., 2003; Pammer et al., 2004; Tarkiainen et al., 1999; see also Nobre et al. (1994) for a lack of words/nonwords difference on N200 visual potentials recorded on the ventral occipito-temporal cortical surface) and a few studies have reported inconsistent effects, i.e. a small increase (Hauk and Pulvermüller, 2004, Maurer et al., 2005) or a decrease (McCandliss et al., 1997) of the N170 to words relative to pseudowords.

The lack of consistent (i.e., reliable) indexes of selective visual word representation in ERP studies is in line with the lack of systematic discriminative response in the left ventral occipito-temporal cortex in neuroimaging (Price, 2012, Seghier et al., 2012), suggesting that selective visual representation of words (i.e. different from pseudowords) do not exist. For instance, in the interactive account framework (Price and Devlin, 2011), responses to visual words merely arise as an interaction between bottom-up visual input and higher level phonological/semantic processing, and not from any selective tuning to orthographic representations. It may also be that selective responses to words are heavily task-dependent (Bentin et al., 1999, Ziegler and Goswami, 2005, Ziegler et al., 1997), so that lexicality-related N170 modulations (e.g., Hauk et al., 2012) require explicit processing of the visual stimuli. Yet, at this stage, one cannot exclude that the lack of consistent indexes of automatic selective visual word representation arises due to the difficulty of isolating selective differences between visual stimuli with a poor signal-to-noise ratio (SNR) approach such as ERPs, or an approach that accumulates neural activity over seconds such as fMRI.

Here we introduce a fast periodic visual stimulation paradigm in EEG for visual word stimulation, to potentially provide a reliable index of visual word vs. pseudoword discrimination without an explicit word-related task. Such an index would not only support the proposal of automatic activation of whole word representations (Glezer et al., 2009, Shtyrov et al., 2013), but would be valuable in assessing potential defective processes of reading in patient populations (e.g., dyslexia) and during both typical and abnormal development. Our approach is based on scalp EEG recordings during periodic visual stimulation, which results in periodic responses defined as “steady-state visual evoked potentials” (SSVEPs, Regan, 1966, Regan, 1989). Although this approach has long been confined to the study of low-level visual processes and attention, it has recently been used to measure visual discrimination responses of complex visual stimuli such as faces (Rossion and Boremanse, 2011). Most recently, Liu-Shuang et al. (2014) measured the discrimination of individual faces by presenting a sequence of identical face stimuli at a fast periodic rate (base frequency=F, 6 Hz) interspersed with different identity face stimuli (“oddball”) at a slower periodic rate (i.e., 1 novel face every 5 identical faces). In this study, a robust individual face discrimination response was recorded over the right occipito-temporal cortex, specifically at the oddball frequency rate (F/5=1.2 Hz) and its harmonics (2F=2.4 Hz, etc.). This approach, with two embedded periodic frequency rates and an analysis of the responses of interest in the frequency-domain (Braddick et al., 1986, Heinrich et al., 2009, Liu-Shuang et al., 2014), has several important advantages for the present question of interest (for review see Rossion, 2014). That is, within a few minutes of stimulation, it provides (1) high SNR visual discrimination responses that are (2) selective to the contrast between the frequent and rare stimuli, (3) objectively identifiable (i.e., at an experimentally-defined frequency rate) and directly quantifiable in the EEG spectrum and (4) obtained without any behavioral task requiring the processing of the parameter of interest, i.e. implicitly.

Considering that these advantages may prove crucial for identifying an automatic representation of visual word form, we applied this approach to the discrimination of written words from control stimuli. Specifically, human observers were presented with visual stimuli at a fast rate of 10 Hz (stimulus onset asynchrony of 100 ms), in sequences structured as follows: xxxxWxxxxWxxxxW…, where “W” refers to words, and “x”, depending on the experimental condition, to one of the following stimulus types: pseudofonts (PF), nonwords (NW, sequences of orthographically illegal letter strings), or pseudowords (PW, sequences of orthographically legal letter strings). We hypothesized that if words are discriminated from pseudofonts, nonwords, or even pseudowords, their periodic occurrence should lead to a periodic EEG response at the oddball frequency, i.e., at 2 Hz and its harmonics. Further, we hypothesized that if behavioral list context effects as reported in the literature (e.g., the more or less word-like sequence; Lupker and Pexman, 2010; Stone and Van Orden, 1993; Pugh et al., 1994) are due to visual discrimination processes rather than decisional levels, then the sequence type should determine the strength of the discrimination response. More precisely, the oddball response to words should be larger in nonword sequences (which are less word-like) than in pseudoword sequences (which are more word-like).

Section snippets

Participants

Ten right-handed healthy participants (2 males, mean age=25.3; range 20–42), all native French speakers, with normal/corrected-to-normal vision, were tested after giving written informed consent for a study that was approved by the Biomedical Ethical Committee of the University of Louvain. They received financial compensation for their participation. They were unaware of the goals of the experiment and that a change of stimulus type occurred at a periodic rate.

Stimuli

Words, pseudowords, nonwords, and

Participants

Ten right-handed healthy participants (2 males, mean age=22.7; range 20−24), all native French speakers, with normal/corrected-to-normal vision, were tested after giving written informed consent for a study that was approved by the Biomedical Ethical Committee of the University of Louvain. They received financial compensation for their participation. They were not informed about the goal of the experiment and that a change of stimulus type occurred at a periodic rate.

Stimuli

Words (W), pseudowords with

An index of automatic lexical access

The present study innovated in the domain of visual word recognition by introducing a fast periodic stimulation EEG approach that is rarely used in cognitive electrophysiology (Luck, 2014). This approach revealed automaticity and specificity of word discrimination: visual words elicited clear differential responses from letter-like control stimuli (experiment 1) and from alphabetic control stimuli (experiments 1 and 2), within a few minutes of stimulation. Remarkably, this response was recorded

Conflict of interest

None.

Acknowledgements

This work was supported by a Grant from the European Research Council (facessvep 284025) to BR. AL was supported by the ERC Grant and a PAI/UIAP Grant PAI/33. BR and GVB are supported by the Belgian National Fund for Scientific Research. The authors would like to thank Joan Liu for her advices in data analysis and Talia Retter for her careful reading of a previous version of this manuscript.

References (92)

  • O. Hauk et al.

    The time course of visual word recognition as revealed by linear regression analysis of ERP data

    NeuroImage

    (2006)
  • O. Hauk et al.

    Effects of word length and frequency on the human event-related potential

    Clin. Neurophysiol.: Off. J. Int. Fed. Clin. Neurophysiol.

    (2004)
  • S.P. Heinrich et al.

    Frequency-domain analysis of fast oddball responses to visual stimuli: a feasibility study

    Int. J. Psychophysiol.

    (2009)
  • M. Kutas et al.

    Electrophysiology reveals semantic memory use in language comprehension

    Trends Cogn. Sci.

    (2000)
  • J. Liu-Shuang et al.

    An objective index of individual face discrimination in the right occipito-temporal cortex by means of fast periodic oddball stimulation

    Neuropsychologia

    (2014)
  • B.D. McCandliss et al.

    The visual word form area: expertise for reading in the fusiform gyrus

    Trends Cogn. Sci.

    (2003)
  • B.D. McCandliss et al.

    Brain plasticity in learning visual words

    Cogn. Psychol.

    (1997)
  • K. Pammer et al.

    Visual word recognition: the first half second

    NeuroImage

    (2004)
  • C.J. Price

    A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading

    NeuroImage

    (2012)
  • C.J. Price et al.

    The myth of the visual word form area

    NeuroImage

    (2003)
  • C.J. Price et al.

    The interactive account of ventral occipitotemporal contributions to reading

    Trends Cogn. Sci.

    (2011)
  • B. Rossion et al.

    Early lateralization and orientation tuning for face, word, and object processing in the visual cortex

    Neuroimage

    (2003)
  • B. Rossion et al.

    A steady-state visual evoked potential approach to individual face perception: effect of inversion, contrast-reversal and temporal dynamics

    NeuroImage

    (2012)
  • H. Rubenstein et al.

    Homographic entries in the internal lexicon

    J. Verbal Learn. Verbal Behav.

    (1970)
  • M.L. Seghier et al.

    Reading without the left ventral occipito-temporal cortex

    Neuropsychologia

    (2012)
  • D. Sutoyo et al.

    Nonlinear SSVEP responses are sensitive to the perceptual binding of visual hemifields during conventional ‘eye’ rivalry and interocular ‘percept’ rivalry

    Brain Res.

    (2009)
  • T. Twomey et al.

    Top-down modulation of ventral occipito-temporal responses during visual word recognition

    NeuroImage

    (2011)
  • F. Vinckier et al.

    Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system

    Neuron

    (2007)
  • S. Walter et al.

    Effects of overt and covert attention on the steady-state visual evoked potential

    Neurosci. Lett.

    (2012)
  • S. Bentin et al.

    ERP manifestations of processing printed words at different psycholinguistic levels: time course and scalp distribution

    J. Cogn. Neurosci.

    (1999)
  • D.H. Brainard

    The psychophysics toolbox

    Spatial Vis.

    (1997)
  • O.J. Braddick et al.

    Orientation-specific cortical responses develop in early infancy

    Nature

    (1986)
  • S. Brem et al.

    Tuning of the visual word processing system: distinct developmental ERP and fMRI effects

    Hum. Brain Mapp.

    (2009)
  • Y. Chen et al.

    The power of human brain magnetoencephalographic signals can be modulated up or down by changes in an attentive visual task

    Proc. Natl. Acad. Sci. USA

    (2003)
  • L. Cohen et al.

    The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients

    Brain : J. Neurol.

    (2000)
  • L. Cohen et al.

    Language-specific tuning of visual cortex? Functional properties of the visual word form area

    Brain: J. Neurol.

    (2002)
  • M. Coltheart et al.

    DRC: a dual route cascaded model of visual word recognition and reading aloud

    Psychol. Rev.

    (2001)
  • A.M. Cravo et al.

    Temporal expectation enhances contrast sensitivity by phase entrainment of low-frequency oscillations in visual cortex

    J. Neurosci.

    (2013)
  • S. Dehaene et al.

    Cerebral mechanisms of word masking and unconscious repetition priming

    Nat. Neurosci.

    (2001)
  • S. Dehaene et al.

    How learning to read changes the cortical networks for vision and language

    Science

    (2010)
  • E.M. Dundas et al.

    The joint development of hemispheric lateralization for words and faces

    J. Exp. Psychol.: Gen.

    (2012)
  • W. Duyck et al.

    WordGen: a tool for word selection and non-word generation in Dutch, German, English, and French

    Behav. Res. Methods, Instrum. Comput.

    (2004)
  • M. Dzhelyova et al.

    The effect of parametric stimulus size variation on individual face discrimination indexed by fast periodic visual stimulation

    BMC Neurosci.

    (2014)
  • M.J. Farah

    Patterns of co-occurrence among the associative agnosias: implications for visual object representation

    Cogn. Neuropsychol.

    (1991)
  • N. Friedmann et al.

    Developmental surface dyslexias

    Cortex; J. Devot. Study Nerv. Syst. Behav.

    (2008)
  • W.R. Glaser et al.

    Context effects in stroop-like word and picture processing

    J. Exp. Psychol.: Gen.

    (1989)
  • Cited by (0)

    View full text