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Refining Understanding of Working Memory Buffers Through the Construct of Binding cortex xxx (2018) 1e21 Available online at www.sciencedirect.com ScienceDirect Journal homepage: www.elsevier.com/locate/cortex Special issue: Research report Refining understanding of working memory buffers through the construct of binding: Evidence from a single case informs theory and clinical practise * Pierre-Yves Jonin a,b,c, , Clara Calia d, Sophie Muratot a, Serge Belliard c, Quentin Duche b, Emmanuel J. Barbeau a and Mario A. Parra e,f a Centre de Recherche Cerveau et Cognition, Universite de Toulouse, CNRS CERCO, UMR 5549, Toulouse, France b RISA, UMR CNRS 6074, VisAGeS U 1228, Inserm, INRIA, Universite de Rennes 1, Rennes, France c CHU Pontchaillou, Service de Neurologie, Rennes, France d School of Health in Social Science, University of Edinburgh, Edinburgh, UK e School of Social Sciences, Department of Psychology, Heriot-Watt University, Edinburgh, UK f Universidad Autonoma del Caribe, Facultad de Psicologı´a, Barranquilla, Colombia article info abstract Article history: Binding operations carried out in working memory enable the integration of information Received 30 January 2018 from different sources during online performance. While available evidence suggests that Reviewed 11 April 2018 working memory may involve distinct binding functions, whether or not they all involve Revised 15 May 2018 the episodic buffer as a cognitive substrate remains unclear. Similarly, knowledge about Accepted 3 August 2018 the neural underpinnings of working memory buffers is limited, more specifically Published online xxx regarding the involvement of medial temporal lobe structures. In the present study, we report on the case of patient KA, with developmental amnesia and selective damage to the Keywords: whole hippocampal system. We found that KA was unable to hold shape-colours associ- Working memory ations (relational binding) in working memory. In contrast, he could hold integrated col- Episodic buffer oured shapes (conjunctive binding) in two different tasks. Otherwise, and as expected, KA Binding was impaired on three relational memory tasks thought to depend on the hippocampus Amnesia that are widely used in the early detection of Alzheimer's disease. Our results emphasize a Alzheimer's disease dissociation between two binding processes within working memory, suggesting that the visuo-spatial sketchpad could support conjunctive binding, and may rely upon a large cortical network including sub-hippocampal structures. By contrast, we found evidence for a selective impairment of relational binding in working memory when the hippocampal system is compromised, suggesting that the long-term memory deficit observed in amnesic patients may be related to impaired short-term relational binding at encoding. Finally, these findings may inform research on the early detection of Alzheimer's disease as the preservation of conjunctive binding in KA is in sharp contrast with the impaired perfor- mance demonstrated very early in this disease. © 2018 Elsevier Ltd. All rights reserved. * Corresponding author. Centre de Recherche Cerveau et Cognition (CerCo), CNRS CERCO UMR 5549, Pavillon Baudot, CHU Purpan, BP 25202, 31052, Toulouse Cedex, France. E-mail address: [email protected] (P.-Y. Jonin). https://doi.org/10.1016/j.cortex.2018.08.011 0010-9452/© 2018 Elsevier Ltd. All rights reserved. Please cite this article in press as: Jonin, P.-Y., et al., Refining understanding of working memory buffers through the construct of binding: Evidence from a single case informs theory and clinical practise, Cortex (2018), https://doi.org/10.1016/j.cortex.2018.08.011 2 cortex xxx (2018) 1e21 that whereas the requirement to integrate phonological with 1. Introduction long-term linguistic information is not attentionally demanding, the integration of unrelated concepts is effortful. Since its introduction in 1974, the Working Memory (WM) The processes supporting sentence recall reflect the contri- model proposed by Baddeley and Hitch (Baddeley & Hitch, butions from both automatic linguistic functions and 1974) has undergone revisions and refinements. A cognitive controlled binding functions operating on an attentionally construct which has driven substantial amount of research limited WM component i.e., the episodic buffer. Vogel, and revisions of the model is binding, understood as the Woodman, and Luck (2001) and Luck and Vogel (1997) inves- function that enables the integration of information from tigated whether the integration of visual information in WM different sources during online performance (Zimmer, was cognitively demanding. Searching for evidence about the Mecklinger, & Lindenberger, 2006). To account for such an unit of representation of visual WM (i.e., integrated objects or operation in WM, Baddeley proposed the episodic buffer, individual features), the authors found that holding features arguing that this may be the locus of binding functions (i.e., integrated within unified object representations was not chunking) that were hard to accommodate in short-term costlier than holding individuals features. They suggested memory (STM) buffers proposed earlier (Baddeley, 2000). that temporarily storing in visual WM objects defined by This new component attracted considerable amount of multiple features is a cost-free process, in as much as it does attention leading to new questions about the structure and not consume additional WM capacity, and therefore the unit functions of WM and its neurobiological underpinnings of representation of visual WM would likely be integrated (Baddeley, 2007a, 2007b; Baddeley, Allen, & Hitch, 2011). This objects. Wheeler and Treisman (2002) challenged this view by paper reports on the study of a single case, patient KA, whose manipulating the change detection task in a way that required pattern of performance can shed new light on the ongoing binding (i.e., swapping features between objects rather than debate about the function, structure, and neural substrate of adding new feature values as previously done by Vogel et al. WM as a workspace wherein different binding functions (2001) and Luck and Vogel (1997). Under this task conditions operate. Before we report on KA's history and assessment, we binding in visual WM proved costly and such a cost varied will briefly review the role that the construct of binding has depending on whether resources (i.e., feature dimensions) played in shaping our understanding of WM. We will then were drawn from the same or different pools (see Olson & address the literature reporting on neuroimaging and clinical Jiang, 2002 for further testing of this hypothesis). Allen, studies that have sought evidence on the neural correlates of Baddeley, and Hitch (2006) decided to use the paradigm of functions attributed to the episodic buffer and their vulnera- dual-task interference to investigate whether binding in vi- bility to brain damage and cognitive ageing. We will then sual WM features drawn from different pools (i.e., colour and introduce the current study emphasising the contribution that shape) was an automatic or a resource demanding function. the evidence presented here can make to both understanding Through a well-designed series of experiments (Allen, Hitch, of the functional architecture of WM and refinement of & Baddeley, 2009; Allen et al., 2006; Karlsen, Allen, Baddeley, memory assessment. & Hitch, 2010), the authors demonstrated that this form of feature binding does not require executive resources above and beyond those needed to process single objects. This evi- 2. What has the construct of binding taught dence was in line with the suggestions made by Vogel et al. us about the functional organization of WM? (2001) and Luck and Vogel (1997) thus questioning the hy- potheses that the episodic buffer is the seat of binding oper- Baddeley (Baddeley, 2000, 2007a, 2007b) thought of the ations carried out in WM. Following this evidence, Baddeley, episodic buffer as a temporary store that integrates incoming Allen, et al. (2011) and Baddeley, Jarrold, et al. (2011) revised information from other STM buffers and that retrieves them the WM model to propose that this form of low-level feature from long-term memory as unitary multimodal representa- binding may occur in other WM buffers such as the visuo- tions. Once formed, such bound representations become spatial sketchpad. available to conscious awareness (Baddeley et al., 2011; Logie, Allen et al. (2006) acknowledged that there are many 2011; Repovs & Baddeley, 2006). Repovs and Baddeley (2006) different types of binding, depending on what stores, memory postulated that features held by the episodic buffer are domains, or forms of representation are involved, and that stored in unitary representations either as integrated objects visual feature binding is just one particular type. In fact, more or as chunks (see Cowan, 2001; Cowan, 2010). Baddeley, Allen, recent studies have investigated whether other forms of et al. (2011) and Baddeley, Jarrold, et al. (2011)) argued that the binding which had been well characterised in long-term episodic buffer has a central role in providing a multidimen- memory (e.g., associative learning or relational long-term sional medium, allowing binding together chunks or features memory binding; Mayes, Montaldi, & Migo, 2007; Moses & from different sources either visual or verbal, a process that Ryan, 2006) would operate in WM under the same cognitive requires executive control. In the verbal domain, Jefferies, constraints. This research has demonstrated that forms of Lambon Ralph, and Baddeley
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