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Brain Structure and Function

Erschienen in:

03.11.2021 | Review

Is human face recognition lateralized to the right hemisphere due to neural competition with left-lateralized visual word recognition? A critical review

verfasst von: Bruno Rossion, Aliette Lochy

Erschienen in: Brain Structure and Function | Ausgabe 2/2022

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Abstract

The right hemispheric lateralization of face recognition, which is well documented and appears to be specific to the human species, remains a scientific mystery. According to a long-standing view, the evolution of language, which is typically substantiated in the left hemisphere, competes with the cortical space in that hemisphere available for visuospatial processes, including face recognition. Over the last decade, a specific hypothesis derived from this view according to which neural competition in the left ventral occipito-temporal cortex with selective representations of letter strings causes right hemispheric lateralization of face recognition, has generated considerable interest and research in the scientific community. Here, a systematic review of studies performed in various populations (infants, children, literate and illiterate adults, left-handed adults) and methodologies (behavior, lesion studies, (intra)electroencephalography, neuroimaging) offers little if any support for this reading lateralized neural competition hypothesis. Specifically, right-lateralized face-selective neural activity already emerges at a few months of age, well before reading acquisition. Moreover, consistent evidence of face recognition performance and its right hemispheric lateralization being modulated by literacy level during development or at adulthood is lacking. Given the absence of solid alternative hypotheses and the key role of neural competition in the sensory–motor cortices for selectivity of representations, learning, and plasticity, a revised language-related neural competition hypothesis for the right hemispheric lateralization of face recognition should be further explored in future research, albeit with substantial conceptual clarification and advances in methodological rigor.

In psychology, the term “recognition” is often used to refer to the judgment of previous occurrence (specifically “the ability to identify information as having been encountered before”, APA Dictionary of Psychology; see also Mandler 1980). In psychological research on human faces, the term is even often restricted to the judgment of a previous occurrence of specific identities of faces (i.e., familiar faces). Here it is used in a more general biological sense as the reliable production of selective (i.e., differential) responses to sensory inputs at different levels, ranging from the recognition of a visual stimulus as a face (“generic face recognition”) to its specific identity (“face identity recognition”) or its emotional expression (“emotional facial expression recognition”).

The definition of prosopagnosia used here does not include cases of developmental disorders at FIR in the absence of neurological history, which are often referred to as developmental prosopagnosia or congenital prosopagnosia (Behrmann and Avidan 2005; Duchaine and Nakayama 2006), but more correctly as prosopdysgnosia (Rossion 2018b; Sorensen and Overgaard 2018).

Fast periodic visual stimulation or “frequency-tagging” in EEG is a technique in which stimuli are presented at a (usually fast) periodic rate, leading to neural responses expressed in the EEG frequency spectrum (Regan 1966). This technique has considerable advantages in terms of sensitivity and objectivity of measurement (see Norcia et al. 2015; Rossion et al. 2020 for reviews).

The term ‘representation’ as used here refers merely to (a pattern of) activity in the neural system that has a systematic relationship with a sensory stimulus of the environment. Although the term ‘representation’ has sometimes been used in neuroimaging in the restrictive context of multivariate pattern analysis (Kriegeskorte et al. 2008), the neural activity does not have to be distributed across spatial units such as voxels (e.g., larger neural activity to faces than non-face stimuli in the right lateral middle fusiform gyrus as a whole “represents” face stimuli).

In the remainder of the text, we will typically use the term ‘letter strings’ as a general term that encompasses words (e.g., familiar written forms), non-words (unmeaningful strings of letters), or even consonant strings. The distinction is relevant given the debate of whether the visual word form area (VWFA) processes only pre-lexical (McCandliss et al. 2003) or also lexical representations (Glezer et al. 2009, 2015; Kronbichler et al. 2004).

Note that the spatial frequency hypothesis is not supported by training studies on reading acquisition with atypical visual shapes (such as faces or houses) differing greatly from the natural script characteristics, but also revealing the left middle fusiform gyrus as the site of learning effects (Moore et al. 2014; Hirshorn et al. 2016; Martin et al. 2019).

https://science.sciencemag.org/content/330/6009/1359.

Technically, a response recorded over EEG electrodes positioned over the RH could potentially be generated from sources in the LH, although this is unlikely for the focal occipito-temporal response as displayed in Figs. 4 and 5

. Due to the undetermined inverse problem in EEG (or MEG), source localization algorithms applied to such data would not enable substantial progress on this issue. However, testing an adapted frequency-tagging paradigm with functional near-infrared spectroscopy (e.g., slowing down the face stimulation frequency as in fMRI, see Gao et al. 2019), recording neural signals under the sampled area, could provide decisive evidence.

To the best of our understanding, this negative correlation interpreted in support of the hypothesis cannot be due to the negative polarity of the N170 component.

As also noted by an anonymous reviewer of this manuscript, the prosopagnosic patient reported by Barton (2008) was ambidextrous and had in fact a bilateral VOTC lesion and is therefore not considered here.

Early developmental studies of face recognition have instead argued in favor of a dip of performance at a later age, at around 11 years old (Carey 1992), but this has not been supported by subsequent studies.

The terms ‘holistic’ and ‘configural’ are sometimes used to refer to different concepts in human face recognition research, but they are used as synonyms here (as proposed and discussed extensively in Rossion 2009, 2013).

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Titel: Is human face recognition lateralized to the right hemisphere due to neural competition with left-lateralized visual word recognition? A critical review
verfasst von: Bruno Rossion
Aliette Lochy
Publikationsdatum: 03.11.2021
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 2/2022
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-021-02370-0

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Is human face recognition lateralized to the right hemisphere due to neural competition with left-lateralized visual word recognition? A critical review

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