Dissociating the Neural Correlates of Intra-Item and Inter-Item Working-Memory Binding

PLOS ONE, Apr 2010

Background Integration of information streams into a unitary representation is an important task of our cognitive system. Within working memory, the medial temporal lobe (MTL) has been conceptually linked to the maintenance of bound representations. In a previous fMRI study, we have shown that the MTL is indeed more active during working-memory maintenance of spatial associations as compared to non-spatial associations or single items. There are two explanations for this result, the mere presence of the spatial component activates the MTL, or the MTL is recruited to bind associations between neurally non-overlapping representations. Methodology/Principal Findings The current fMRI study investigates this issue further by directly comparing intrinsic intra-item binding (object/colour), extrinsic intra-item binding (object/location), and inter-item binding (object/object). The three binding conditions resulted in differential activation of brain regions. Specifically, we show that the MTL is important for establishing extrinsic intra-item associations and inter-item associations, in line with the notion that binding of information processed in different brain regions depends on the MTL. Conclusions/Significance Our findings indicate that different forms of working-memory binding rely on specific neural structures. In addition, these results extend previous reports indicating that the MTL is implicated in working-memory maintenance, challenging the classic distinction between short-term and long-term memory systems.

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Dissociating the Neural Correlates of Intra-Item and Inter-Item Working-Memory Binding

Kessels RPC (2010) Dissociating the Neural Correlates of Intra-Item and Inter-Item Working-Memory Binding. PLoS ONE 5(4): e10214. doi:10.1371/journal.pone.0010214 Dissociating the Neural Correlates of Intra-Item and Inter-Item Working-Memory Binding Carinne Piekema 0 Mark Rijpkema 0 Guille n Ferna ndez 0 Roy P. C. Kessels 0 Andre Aleman, University of Groningen, Netherlands 0 1 Donders Institute for Brain , Cognition and Behaviour , Radboud University Nijmegen , Nijmegen , The Netherlands , 2 Department of Experimental Psychology, Oxford University , Oxford , United Kingdom , 3 Department of Neurology, Radboud University Nijmegen Medical Centre , Nijmegen , The Netherlands , 4 Departments of Medical Psychology and Geriatric Medicine, Radboud University Nijmegen Medical Centre , Nijmegen , The Netherlands Background: Integration of information streams into a unitary representation is an important task of our cognitive system. Within working memory, the medial temporal lobe (MTL) has been conceptually linked to the maintenance of bound representations. In a previous fMRI study, we have shown that the MTL is indeed more active during working-memory maintenance of spatial associations as compared to non-spatial associations or single items. There are two explanations for this result, the mere presence of the spatial component activates the MTL, or the MTL is recruited to bind associations between neurally non-overlapping representations. Methodology/Principal Findings: The current fMRI study investigates this issue further by directly comparing intrinsic intraitem binding (object/colour), extrinsic intra-item binding (object/location), and inter-item binding (object/object). The three binding conditions resulted in differential activation of brain regions. Specifically, we show that the MTL is important for establishing extrinsic intra-item associations and inter-item associations, in line with the notion that binding of information processed in different brain regions depends on the MTL. Conclusions/Significance: Our findings indicate that different forms of working-memory binding rely on specific neural structures. In addition, these results extend previous reports indicating that the MTL is implicated in working-memory maintenance, challenging the classic distinction between short-term and long-term memory systems. - Funding: This study was funded by a grant from the Brain Foundation of the Netherlands (no. 13F05.03) and a VIDI innovational grant from the Netherlands Organisation for Scientific Research (NWO, no. 452-08-005), both awarded to the last author. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. An important quality of human cognition is the ability to associate and integrate different aspects of an experience into one coherent episode. The separate features of items, such as spatial characteristics, shape, colour, and semantic content, are generally processed in specialized regions distributed across the brain [1], and have to be bound together as conjunctions in order to be perceived and stored as part of a coherent episode [2]. Furthermore, the binding of different items - i.e., forming associations or relations between itemsis also crucial for the formation of episodic memories. The MTL has been implicated in binding operations within long-term memory [35], but evidence on the specific nature of its contribution to binding operations in working memory has emerged only recently. That is, lesion data have demonstrated deficits in short-term maintenance of conjunctions in patients with hippocampal amnesia [6] and a neuroimaging study comparing young and older adults revealed differences in hippocampal activation during working-memory binding [7]. However, most studies only examined spatial binding, although it has been suggested that different binding mechanisms may exist that rely on distinct brain regions [8]. Indeed, in a previous working-memory study, we showed that the MTL was more active in a condition that required the association of a number and its location on the screen (spatial binding) as compared to associations formed between a number and its colour (non-spatial binding) [9]. This pattern of results has two possible interpretations. The first highlights the specific role of the hippocampus in spatial processing [10,11], that is, the activation of the MTL is driven by the spatial nature of the binding. The second is based on the notion that different forms of memory binding exist, which may differentially rely on hippocampal activation [8]. Different distinctions can be made here. For example, a distinction can be made between intraand inter-item associations [12]. Intra-item associations are associations between objects and their features that, when bound together, are commonly perceived as a single entity [1316], oft (...truncated)


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Carinne Piekema, Mark Rijpkema, Guillén Fernández, Roy P. C. Kessels. Dissociating the Neural Correlates of Intra-Item and Inter-Item Working-Memory Binding, PLOS ONE, 2010, Volume 5, Issue 4, DOI: 10.1371/journal.pone.0010214