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The Neural Correlates of Visual Imagery: a Co-Ordinate-Based Meta-Analysis

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The Neural Correlates of Visual Imagery: a Co-Ordinate-Based Meta-Analysis cortex 105 (2018) 4e25 Available online at www.sciencedirect.com ScienceDirect Journal homepage: www.elsevier.com/locate/cortex Special issue: Research report The neural correlates of visual imagery: A co-ordinate-based meta-analysis * Crawford I.P. Winlove a, , Fraser Milton b, Jake Ranson c, Jon Fulford a, Matthew MacKisack a, Fiona Macpherson d and Adam Zeman a a Medical School, University of Exeter, UK b School of Psychology, University of Exeter, UK c St George's Medical School, London, UK d Department of Philosophy, University of Glasgow, UK article info abstract Article history: Visual imagery is a form of sensory imagination, involving subjective experiences typi- Received 4 August 2017 cally described as similar to perception, but which occur in the absence of corresponding Reviewed 2 October 2017 external stimuli. We used the Activation Likelihood Estimation algorithm (ALE) to iden- Revised 11 December 2017 tify regions consistently activated by visual imagery across 40 neuroimaging studies, the Accepted 18 December 2017 first such meta-analysis. We also employed a recently developed multi-modal parcella- Published online 2 January 2018 tion of the human brain to attribute stereotactic co-ordinates to one of 180 anatomical regions, the first time this approach has been combined with the ALE algorithm. We Keywords: identified a total 634 foci, based on measurements from 464 participants. Our overall fMRI comparison identified activation in the superior parietal lobule, particularly in the left Neuroimaging hemisphere, consistent with the proposed ‘top-down’ role for this brain region in im- Imagery agery. Inferior premotor areas and the inferior frontal sulcus were reliably activated, a Imagination finding consistent with the prominent semantic demands made by many visual imagery ALE tasks. We observed bilateral activation in several areas associated with the integration of eye movements and visual information, including the supplementary and cingulate eye fields (SCEFs) and the frontal eye fields (FEFs), suggesting that enactive processes are important in visual imagery. V1 was typically activated during visual imagery, even when participants have their eyes closed, consistent with influential depictive theories of vi- sual imagery. Temporal lobe activation was restricted to area PH and regions of the fusiform gyrus, adjacent to the fusiform face complex (FFC). These results provide a secure foundation for future work to characterise in greater detail the functional con- tributions of specific areas to visual imagery. Crown Copyright © 2018 Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). * Corresponding author. Medical School, University of Exeter, UK. E-mail address: [email protected] (C.I.P. Winlove). https://doi.org/10.1016/j.cortex.2017.12.014 0010-9452/Crown Copyright © 2018 Published by Elsevier Ltd. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/4.0/). cortex 105 (2018) 4e25 5 imagery and more generally, has been only partly fulfilled 1. Introduction (Aue, Lavelle, & Cacioppo, 2009). An important reason for this is the diversity of terminology used to describe human Imagination has attracted human interest for at least two neuroanatomy, with multiple distinct terms used to refer to thousand years (Hume, 1784; Mithen, 1998; Modrak, 1987; see the same anatomical or functional brain region, or the same MacKisack et al., 2016 for a recent review), was disavowed by term used to refer to different regions (Bohland, Bokil, Allen, much of the academic community in the first half of the 20th & Mitra, 2009). This threatens to confound meaningful dis- century (Watson, 1913), then played a central role in the cussion: how could we judge the role of fusiform face area in subsequent Cognitive Revolution (Neisser, 1967). The protean visual imagery without consensus as to which locations nature of imagination confounds its clear definition (Thomas, should carry this name? 2003), yet facilitates its implication in diverse phenomena: The challenge of neuroanatomical nomenclature is not motivation (McMahon, 1973), memory (Yates, 2014), new (Wilder, 1896), but remained unresolved by attempts to emotional disorders (Holmes & Mathews, 2010), prospective compile comprehensive lists of names for neuroanatomical thought (Addis, Wong, & Schacter, 2007), breast enlargement regions (Federative Committee on Anatomical Terminology, (Willard, 1977). 1998), thesauri to relate these terms (Anthoney, 1993), or We explore one specific aspect of imagination e visual machine-readable ontologies (Bowden & Dubach, 2003; Rosse imagery. This is a form of sensory imagination characterised & Mejino, 2003; Rubin et al., 2006). Terminological problems by subjective experiences similar to perception, or at least by are especially pronounced in human brain imaging, as the mental representations that underlie such experiences anatomical regions in these images must be identified without (Block, 1983; Dennet, 1978), with these experiences occurring immediate recourse to classical cytoarchitectural boundaries in the absence of corresponding external stimuli (Finke, 1989; such as those of Brodmann areas. An element of stand- Richardson, 1998). First considered by philosophers, visual ardisation was introduced through the widespread adoption imagery was influentially suggested to provide a foundation of the Talairach atlas (Talairach & Tournoux, 1988), especially for thought (Hume, 1784), with the intentionality of images once these labels could be automatically applied to the co- suggested to provide a secure foundation for the meaning of ordinates of observed activation (Lancaster et al., 2000). language (Russell, 1921). Subsequent work powerfully chal- However, such an approach is problematic (Bohland et al., lenged this view (Wittgenstein, 1953), and was followed by 2009; Devlin & Poldrack, 2007; Evans, Janke, Collins, & Baillet, compelling arguments that invert the previously suggested 2012; Toga & Thompson, 2007), most obviously because the relationship between language and imagery: much of the in- atlas is based on the left hemisphere of a single brain, that of a determinacy of images may actually be resolved through the 60-year old Caucasian woman, and therefore accurately rep- addition of a language-based description (Fodor, 1975; Tye, resents neither the wider population nor any other individual. 1991). Within cognitive science, most conceptual discussions To address this, we used the cortical parcellation of 180 have centred on whether the mental representations that areas recently released as part of the Human Connectome mediate visual imagery are depictive, in that they arise from Project (HCP) (Glasser et al., 2016). These areas, of which 97 are activity in a visual buffer with crucial spatial properties newly identified, were defined on the basis of differences in (Kosslyn, 1981, 2005), or propositional: one product amongst cortical architecture, function, connectivity, and topography in many of a syntactically structured system (Pylyshyn, 2003). a precisely aligned group average of 210 healthy young adults. These influential alternatives have been comprehensively This new resource is highly regarded (Gilmore, Diaz, Wyble, & evaluated (Thomas, 2014a; Tye, 1991); more recent enactive Yarkoni, 2017; Jenkinson, Bannister, Brady, & Smith, 2002; theories, which prioritise the role of attentional mechanisms Okano & Yamamori, 2016), and used in notable recent publi- and seem especially well-placed to explain phenomena such cations (e.g., Mackey, Winawer, & Curtis, 2017; Moreira, as perceptual and representational neglect (Bartolomeo, Marques, & Magalhaes,~ 2016; Waskom & Wagner, 2017). Bourgeois, Bourlon, & Migliaccio, 2013; Thomas, 2003), have The detailed interpretation of neuroimaging results is so-far received considerably less consideration (Thomas, further complicated by the diversity of behavioural tasks used 2014b). Empirically, the neural events associated with visual to evoke visual imagery but, even when studies use uncon- imagery can be studied using neuroimaging. In a typical task, troversial anatomical terms as well as similar methods and participants are asked to imagine a generic example of a participants, striking differences in results remain. Perhaps common concrete object, such as a household item or a spe- the most important example of such disagreement concerns cies of animal (D'Esposito et al., 1997; Ishai, Ungerleider, & whether the activity of the primary visual cortex, V1, in- Haxby, 2000; see Table 1 for further details). Neural events creases during visual imagery At least seven Functional within these periods are contrasted with the patterns of ac- Magnetic Resonance Imaging (fMRI) studies report that V1 is tivity observed at baseline, such as those observed when active during visual imagery (Amedi, Malach, & Pascual- participants judge whether a given number is even (Mazard, Leone, 2005; Ganis, Thompson, & Kosslyn, 2004; Handy et al., Laou, Joliot, & Mellet, 2005). 2004; Ishai et al., 2000; Klein, Paradis, Poline, Kosslyn, & Le Crucially, the results of these studies bear directly upon Bihan, 2000; Lambert, Sampaio, Scheiber, & Mauss, 2002; Le the conceptual debates. For example, an absence of activity Bihan et al., 1993), but at least six report that V1 is not active in V1 e the putative location of a prominently visual repre- (D'Esposito et al., 1997; Formisano et al., 2002; Ishai et al., 2000;
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