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Does the Medial Temporal Lobe Bind Phonological Memories?

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Does the Medial Temporal Lobe Bind Phonological Memories? Does the Medial Temporal Lobe Bind Phonological Memories? Raymond Knott and William Marslen-Wilson Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/13/5/593/1760383/089892901750363181.pdf by guest on 18 May 2021 Abstract & The medial temporal lobes play a central role in the terized by a distinctive pattern of phonological errors, where consolidation of new memories. Medial temporal lesions he recombined phonemes from the original list to form new impair episodic learning in amnesia, and disrupt vocabulary response words. These were similar to errors observed earlier acquisition. To investigate the role of consolidation processes for patients with specifically semantic deficits. Amnesic Korsak- in phonological memory and to understand where and how, in off's patients showed a similar, though much less marked, amnesia, these processes begin to fail, we reexamined pattern. We interpret the data in terms of a model of lexical phonological memory in the amnesic patient HM. While representation where temporal lobe damage disrupts the HM's word span performance was normal, his supraspan recall processes that normally bind semantic and phonological was shown to be markedly impaired, with his recall charac- representations. & INTRODUCTION mediate serial recall performance of three patients with How do transient phonological patterns in short-term semantic dementia, a neurodegenerative condition, memory become consolidated into new long-term mem- which in the initial stages, gives rise to a profound but ories? More than 40 years of research have provided relatively circumscribed semantic impairment, particu- many elegant models of auditory±verbal short-term larly affecting knowledge of word meanings. Asked to memory (AVSTM) that explain a wealth of experimental repeat short sequences of three to four content words, findings, but they have so far offered only rather meager all the patients showed a marked superiority for repeat- insights into how new phonological representations ing words that they still appeared to ``know'' compared become established. Much recent research does never- to words that are now ``unknown''Ðas established by theless suggest that AVSTM plays a central role in their performance on tests of semantic knowledge and acquiring new phonemic forms, and new vocabulary, naming. Moreover, all patients showed a distinctive in general. Gathercole and colleagues have shown that pattern of errors in their word list recall, making numer- children's performance on AVSTM tasks correlates ous phonological approximations to the original targets highly with their vocabulary knowledge (Gathercole & (e.g., ``candle sword cotton'' ! /tñndMl/ sword /t4tMn/; 1 Baddeley, 1989; Gathercole, Willis, Emslie, & Baddeley, ``number mint rug'' ! number /rInt/ /m^g/). Phono- 1992; Gathercole & Adams, 1994; Gathercole, Service, logically related errors were also noted in a variant of the Hitch, Adams, & Martin, 1999). In experimental inves- Brown±Peterson task where subjects were asked to tigations, AVSTM performance has been shown to be a repeat single spoken words after a short (3±8 sec) filled good predictor of the rate at which new phonological delay. Subsequent studies by Knott, Patterson, and forms are acquired (Gathercole & Baddeley, 1990), and Hodges (1997, 2000) suggest that this marked pattern studies using laboratory-based learning paradigms have of phonological errors is associated with semantic and/ demonstrated that the acquisition of new phonological or lexical deficits. Evidence from the normal literature vocabulary is strongly affected by the same range of supporting this view comes from a study by Treiman and factors that affect the operation of AVSTMÐi.e., phono- Danis (1988), which reported a marked and highly logical similarity, word length, and articulatory suppres- similar pattern of phonologically related errors in unim- sion (Ellis & Sinclair, 1996; Papagno & Vallar, 1992). paired subjects who were asked to repeat sequences of If AVSTM is known to affect vocabulary acquisition, monosyllabic nonwords. By definition, nonwords lack there is also strong evidence for a reciprocal influence of lexical representations. The phonological errors made vocabulary knowledge on short-term memory. Patter- by normal subjects in nonword serial recall are, there- son, Graham, and Hodges (1994) investigated the im- fore, also explicable in terms of the absence of lexical or semantic support. Further confirmation comes from a study by Knott, Patterson, and Hodges (1999), which MRC Cognition and Brain Sciences Unit, Cambridge, UK directly compared the immediate serial recall errors of D 2001 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 13:5, pp. 593±609 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892901750363181 by guest on 30 September 2021 unimpaired speakers repeating mixed sequences of the decayed trace would only provide a partial and words and nonwords. Nonwords were found to be incomplete record of the original list, attempts at recall particularly susceptible to phonological errors and re- would be characterized by phonological approximations lated studies (Poirier and St. Aubin, 1995, 1996; Bourassa to the original targetsÐi.e., phonological errors. & Besner, 1994) point to a much closer connection Toinvestigateinmoredepththewaylong-term between AVSTM and long-term memory, particularly memory interacts with short-term memory processing, long-term linguistic representations, than is often ac- it may be instructive to look at the word list recall knowledged in the short-term memory literature. They performance of other patient populations classically also suggest that in attempting to understand the rela- regarded as having impairments to long-term memory. tionship between short-and long-term memory process- Patients with anterograde amnesia are generally re- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/13/5/593/1760383/089892901750363181.pdf by guest on 18 May 2021 ing, an important and underexploited source of garded as having largely intact AVSTM, as measured by evidence may be the errors that subjects make in digit span (Parkinson, 1982; Warrington, 1982), but they short-term memory tasks. exhibit difficulty in establishing longer-term memories If phonological errors in short-term memory are in- (Baddeley & Warrington, 1970; Drachman & Arbit, dicative of the absence of long-term memory support, 1966). In addition to difficulties on tests of episodic or what can these errors tell us about the way long-term recognition memory, studies have also demonstrated memory effects are mediated? Knott et al. (1997) offered that amnesic patients may have profound difficulties an explanation of these phonological errors in terms of acquiring new vocabulary (Kitchener, Hodges, & Mc- an interactive activation model of speech production and Carthy, 1998; Verfaellie, Croce, & Milberg, 1995). Since comprehension (Martin & Saffran, 1997; Dell & O'Seagh- auditory±verbal span remains intact in these cases, there da, 1992). On this view, lexical and semantic representa- appears to be a failure of some subsequent process that tions directly support phonological short-term memory achieves the transition to longer-term storage. The through reciprocal interactions that are continuously densely amnesic patient, HM, offers a well-documented exchanged between lexical, semantic, and phonological example (Gabrieli, Cohen, & Corkin, 1988). HM under- levels within the language system.2 Interpreted in this went bilateral medial temporal lobectomy in 1953 to manner, phonological short-term memory essentially alleviate intractable epilepsy (Scoville & Milner, 1957). reflects the pooled storage capacities of representations While this reduced the frequency and severity of his normally used in speech production and comprehen- seizures, it left him with a profound anterograde am- sion. In lexically impaired subjects, phonological errors nesia that has been extensively investigated over the arise because of the disruption of these mutually sup- intervening 45 years. In studies of both experimental portive interlevel interactions, which normally stabilize and naturalistic learning, HM has shown minimal evi- and maintain the activity of the phonological trace.3 dence of acquiring new vocabulary, and has only ac- An alternative account of phonological errors in short- quired very meager amounts of postmorbid semantic term memory can be derived from the work of Hulme, knowledge. Gabrieli et al. (1988), however, concluded Maughan, and Brown (1991) and Hulme et al. (1997). that this was not due to any additional semantic impair- This account regards long-term memory influence on ments, as HM's premorbid semantic knowledge was short-term memory as more indirect. Whereas the mod- found to be normal. HM's oral definitions of words from el described in Knott et al. (1997) assumes that short- the WAIS-R, lexical decision responses to the same term storage involves activation of phonological, lexical, words, and recognition performance for famous names and semantic representations, Hulme et al. (1991) as- from the 1930s and 1940s (Marslen-Wilson & Teuber, sume that there is a dedicated phonological storage 1975), all fell within the normal range. A detailed retro- device, or short-term store, which represents the to- spective study by Mackay, Burke, and Stewart (1998a, be-recalled list without recourse to lexical knowledge. 1998b) has, however, offered evidence that HM's seman- The phonological
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