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A complementary systems account of word learning: neural and behavioural evidence

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      Abstract

      In this paper we present a novel theory of the cognitive and neural processes by which adults learn new spoken words. This proposal builds on neurocomputational accounts of lexical processing and spoken word recognition and complementary learning systems (CLS) models of memory. We review evidence from behavioural studies of word learning that, consistent with the CLS account, show two stages of lexical acquisition: rapid initial familiarization followed by slow lexical consolidation. These stages map broadly onto two systems involved in different aspects of word learning: (i) rapid, initial acquisition supported by medial temporal and hippocampal learning, (ii) slower neocortical learning achieved by offline consolidation of previously acquired information. We review behavioural and neuroscientific evidence consistent with this account, including a meta-analysis of PET and functional Magnetic Resonance Imaging (fMRI) studies that contrast responses to spoken words and pseudowords. From this meta-analysis we derive predictions for the location and direction of cortical response changes following familiarization with pseudowords. This allows us to assess evidence for learning-induced changes that convert pseudoword responses into real word responses. Results provide unique support for the CLS account since hippocampal responses change during initial learning, whereas cortical responses to pseudowords only become word-like if overnight consolidation follows initial learning.

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      Most cited references 138

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      The cortical organization of speech processing.

      Despite decades of research, the functional neuroanatomy of speech processing has been difficult to characterize. A major impediment to progress may have been the failure to consider task effects when mapping speech-related processing systems. We outline a dual-stream model of speech processing that remedies this situation. In this model, a ventral stream processes speech signals for comprehension, and a dorsal stream maps acoustic speech signals to frontal lobe articulatory networks. The model assumes that the ventral stream is largely bilaterally organized--although there are important computational differences between the left- and right-hemisphere systems--and that the dorsal stream is strongly left-hemisphere dominant.
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        Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory.

        Damage to the hippocampal system disrupts recent memory but leaves remote memory intact. The account presented here suggests that memories are first stored via synaptic changes in the hippocampal system, that these changes support reinstatement of recent memories in the neocortex, that neocortical synapses change a little on each reinstatement, and that remote memory is based on accumulated neocortical changes. Models that learn via changes to connections help explain this organization. These models discover the structure in ensembles of items if learning of each item is gradual and interleaved with learning about other items. This suggests that the neocortex learns slowly to discover the structure in ensembles of experiences. The hippocampal system permits rapid learning of new items without disrupting this structure, and reinstatement of new memories interleaves them with others to integrate them into structured neocortical memory systems.
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          Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans.

           Larry Squire (1992)
          This article considers the role of the hippocampus in memory function. A central thesis is that work with rats, monkeys, and humans--which has sometimes seemed to proceed independently in 3 separate literatures--is now largely in agreement about the function of the hippocampus and related structures. A biological perspective is presented, which proposes multiple memory systems with different functions and distinct anatomical organizations. The hippocampus (together with anatomically related structures) is essential for a specific kind of memory, here termed declarative memory (similar terms include explicit and relational). Declarative memory is contrasted with a heterogeneous collection of nondeclarative (implicit) memory abilities that do not require the hippocampus (skills and habits, simple conditioning, and the phenomenon of priming). The hippocampus is needed temporarily to bind together distributed sites in neocortex that together represent a whole memory.
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            Author and article information

            Affiliations
            [1 ]MRC Cognition and Brain Sciences Unit, Cambridge, UK
            [2 ]Department of Psychology, simpleUniversity of York , York, UK
            Author notes
            [* ]Author for correspondence ( matt.davis@ 123456mrc-cbu.cam.ac.uk ).
            Journal
            Philos Trans R Soc Lond B Biol Sci
            RSTB
            royptb
            Philosophical Transactions of the Royal Society B: Biological Sciences
            The Royal Society
            0962-8436
            1471-2970
            27 December 2009
            27 December 2009
            : 364
            : 1536 , Theme Issue 'Word learning and lexical development across the lifespan' compiled and edited by M. Gareth Gaskell and Andrew W. Ellis
            : 3773-3800
            2846311
            19933145
            10.1098/rstb.2009.0111
            rstb20090111
            © 2009 The Royal Society

            This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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            Philosophy of science

            meta-analysis, sleep, speech, hippocampus, memory, pseudoword

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