Searching for the Hebb effect in Down syndrome: evidence for a dissociation between verbal short-term memory and domain-general learning of serial order

Searching for the Hebb effect in Down syndrome:evidence for a dissociation between verbal short-termmemory and domain-general learning of serial orderjir_1257 295..307

E. K. Mosse & C. Jarrold

University of Bristol, Bristol, UK

Abstract

Background The Hebb effect is a form ofrepetition-driven long-term learning that is thoughtto provide an analogue for the processes involved innew word learning. Other evidence suggests thatverbal short-term memory also constrains nowvocabulary acquisition, but if the Hebb effect isindependent of short-term memory, then it may bepossible to demonstrate its preservation in a sampleof individuals with Down syndrome, who typicallyshow a verbal short-term memory deficit alongsidesurprising relative strengths in vocabulary.Methods In two experiments, individuals both withand without Down syndrome (matched for recep-tive vocabulary) completed immediate serial recalltasks incorporating a Hebb repetition paradigm ineither verbal or visuospatial conditions.

Results Both groups demonstrated equivalentbenefit from Hebb repetition, despite individualswith Down syndrome showing significantly lowerverbal short-term memory spans. The resultantHebb effect was equivalent across verbal and visu-ospatial domains.Conclusions These studies suggest that the Hebbeffect is essentially preserved within Down syn-drome, implying that explicit verbal short-termmemory is dissociable from potentially moreimplicit Hebb learning. The relative strength inreceptive vocabulary observed in Down syndromemay therefore be supported by largely intact long-term as opposed to short-term serial order learning.This in turn may have implications for teachingmethods and interventions that present newphonological material to individuals with Downsyndrome.

Keywords Down syndrome, new word learning,the Hebb effect, verbal short-term memory

Searching for the Hebb effect inDown syndrome

The process of learning a new word requires theability to retain in mind an accurate representationof its phonological structure. The capacity for the

Correspondence: Ms Emma Mosse, Department of ExperimentalPsychology, University of Bristol, 12a Priory Road, Bristol BS8

1TU, UK (e-mail: [email protected]).Author note: This research was conducted as partial requirementof a research studentship awarded to the first author by the Eco-nomic and Social Research Council (PTA-030-2005-00868). Weare grateful to the staff and pupils of Air Balloon Hill InfantsSchool, Bristol; Kingsweston School, Bristol; Ravenswood School,Nailsea; Summerhill Infant School, Bristol; and Weybourne InfantSchool, Farnham, for their involvement in this work. We also thankthe individuals with Down syndrome, and their families, for theirparticipation in home visits.

Journal of Intellectual Disability Research doi: 10.1111/j.1365-2788.2010.01257.x

volume 54 part 4 pp 295–307 april 2010295

© 2010 The Authors. Journal Compilation © 2010 Blackwell Publishing Ltd

active retention of verbal material is termed verbalshort-term memory and is typically assessedthrough span tasks whereby lists of auditory itemsare presented for immediate serial recall. Baddeleyet al. (1998) proposed that the fundamental purposeof verbal short-term memory is to support long-term language learning. Specifically, they suggestedthat the central role of the phonological loop withinworking memory (Baddeley 1986) is to enablevocabulary acquisition. When learning a new word,it is essential to maintain not only the constituentfamiliar phonemes but also the order in which theyappear. As a mechanism specialised for the tempo-rary storage and rehearsal of verbal material, andcrucially the sequential relationship between items,the phonological loop fulfils these requirements.

Baddeley et al.’s (1998) assertion that the primaryevolutionary function of verbal short-term memoryis to acquire new language appears to be limited tocontexts where the phonological stimuli to belearned is novel rather than familiar. There is somesupport for this in the neuropsychological literature.Baddeley et al. (1988) report the case of P.V., apatient with left hemisphere damage resulting in aspecific verbal short-term memory deficit, such thatshe was unable to acquire unfamiliar vocabulary.When asked to learn associations between pairs ofwords, P.V. showed typical levels of performance. Bycontrast, when one of the words in each pair wassubstituted for a word in a foreign language, shewas unable to learn any of these new items. Suchfindings are consistent with the suggestion thatshort-term storage of the order of phonologicalmaterial is required for long-term acquisition ofnovel phonological forms (Baddeley et al. 1998).

Furthermore, associations between good phono-logical skills and both richer vocabularies andgreater adeptness at manipulating novel verbalmaterial are evident in the developmental literature.Reliable correlations have consistently been demon-strated between children’s phonological short-termmemory and vocabulary (Gathercole & Baddeley1989; Gathercole & Adams 1994; Gathercole et al.1997; Jarrold et al. 2004a). In addition, Majeruset al. (2006) highlighted the importance of the serialorder component of verbal short-term memory tonon-word learning. Specifically, they found thatshort-term memory for order rather than iteminformation was related to children’s ability to learn

non-words, concluding that while both item andserial order memory are related to new wordlearning, the processes underlying serial ordermemory are the more important for vocabularyacquisition.

Verbal short-term memory capacities are of par-ticular interest when considering individuals withDown syndrome. A substantial body of researchindicates the presence of a specific verbal short-term memory deficit in Down syndrome (seeJarrold et al. 2006), even when accounting forspeech and hearing difficulties. Furthermore, rela-tive to controls matched for receptive vocabulary,individuals with Down syndrome demonstrate sig-nificantly poorer performance on verbal serial orderreconstruction tasks but approximately equivalentperformance on visuospatial serial order reconstruc-tion (Brock & Jarrold 2005). It would seem there-fore that verbal short-term memory is selectivelyimpaired and that this is especially apparent whendemands are placed on serial order memory.Indeed, there is evidence to suggest that the locusof the deficit is not due to the reduction or absenceof rehearsal in Down syndrome (Jarrold et al. 2000;Jarrold et al. 2004b), but rather may stem fromdiminished capacity within the phonological storecomponent of the phonological loop (Purser &Jarrold 2005, in press). For example, Purser &Jarrold (in press) investigated the extent to whichindividuals confused items on a memory list withphonologically similar foils at test. While typicallydeveloping individuals showed phonological confu-sions between test foils that were similar to previ-ously presented items at all four serial positions ofthe presented list, individuals with Down syndromeonly showed confusions when the foil was phono-logically related to the final item on the presentedlist. This suggests that participants with Down syn-drome were only maintaining the final list item inverbal short-term memory. However, Vicari et al.(2004) found comparable capacity estimates forshort-term memory among individuals with Downsyndrome and controls when examining the degreeof recency shown by participants in a free recalltask (cf. Waugh & Norman 1965). Vicari et al.therefore suggest that reduced storage capacities inDown syndrome may result from a reduced contri-bution from central executive resources withinworking memory (Baddeley 1986).

296Journal of Intellectual Disability Research volume 54 part 4 april 2010

E. K. Mosse & C. Jarrold • Hebb learning in Down syndrome


Given the evidence for the link between verbalshort-term memory, and specifically short-termmemory for serial order, and vocabulary, one wouldcertainly expect significant difficulties with vocabu-lary development within the Down syndrome popu-lation. However, while vocabulary is very rarely ageappropriate in Down syndrome, it tends to bebetter than would be predicted given individuals’verbal short-term memory skills (Laws 1998).Lexical and grammatical abilities are usually closelyassociated (Bates & Goodman 1997), but vocabu-lary and syntax comprehension are dissociated inDown syndrome, with particular problems in thelatter (Chapman et al. 1991) suggesting that thetypical process of language development deviates insome way in Down syndrome, and that vocabularydevelopment in particular is a relative strength incomparison with more severely delayed aspects oflanguage.

One possible explanation for the relatively goodvocabulary skills in Down syndrome is that vocabu-lary acquisition in the condition is not whollyreliant upon verbal short-term memory. Instead,some aspects of new word learning in Down syn-drome may place less emphasis on the phonologicalfeatures of words and may rely on alternative,perhaps less specifically verbal, strategies. Indeed,Jarrold et al. (2009) showed that while the ability ofindividuals with Down syndrome to learn theprecise phonological form of new words was relatedto verbal short-term memory performance, theability to determine which item a novel phonologi-cal stimulus referred to was not, and was unim-paired in their sample.

One potential process that may support wordlearning in Down syndrome is the learning of serialorder driven by repetition, as distinct from verbalshort-term memory capacity per se. Ordering infor-mation in this way can be considered as a form oflong-term learning, reliant upon domain-generalprocesses, and contrasts with the short-term,limited capacity domain-specific serial ordering thatoccurs within verbal short-term memory. Within animmediate serial recall task, consistently repeatingone of the sequences at regular intervals results ingreater successive recall of that sequence relative tothe non-repeated sequences. This well-establishedfinding is known as the Hebb effect (Hebb 1961),and it is thought that repeatedly recalling a list of

items leads to the gradual development of a long-term representation of that list. Hebb learning hasbeen described as implicit, and while this claim issomewhat contentious, approximately equivalentbenefits from repeated trials have been observed inparticipants both aware and unaware of list repeti-tion (e.g. Couture & Tremblay 2006). Given thatlearning a new word requires a durable long-termrepresentation of a list of phonemes in the correctserial order, it has been suggested that the Hebbeffect is analogous to one of the processes involvedin natural vocabulary acquisition (Cumming et al.2003).

The majority of work on the Hebb repetitionparadigm has focused on verbal material. However,not only has the Hebb effect been demonstrated forvisual material (Page et al. 2006), but Couture &Tremblay (2006) demonstrated comparable gradi-ents of improvement across trials in both verbal andspatial domains. They concluded that a commonmechanism underpins serial order learning in bothdomains. Certainly, the fact that the Hebb effect ismanifest in visuospatial material in a comparableway to that in verbal material is indicative of alearning process that goes beyond the content ofthe items to be learned.

Not only does the Hebb effect operate acrossverbal and visuospatial domains, but this capacityfor learning because of repetition has been shownto relate directly to the ability to acquire new pho-nological forms. Mosse & Jarrold (2008) gave youngtypically developing children Hebb-type recall tasksin both verbal and spatial domains as well as wordand non-word paired associate learning tasks, andfound relatively small but significant Hebb effects.The degree of observed Hebb effect was correlatedwith the ability to learn non-words, and crucially,was so regardless of the domain of testing. In otherwords, while novel word acquisition is clearlyrelated to ordering within verbal short-termmemory, it also appears to be underpinned by aprocess representing the acquisition of serial orderin a more domain-general manner.

Recently, Szmalec et al. (2009) established amore direct link between the Hebb effect and wordlearning using a lexical decision paradigm. Non-sense syllables repeated across lists in a serial recalltask were associated with increased latencies in asubsequent lexical decision task relative to non-




repeated syllables. Clearly then, the mechanisminvolved in processing the short-term retention ofsequences of phonological material also supportsnew word learning. On the basis of these and otherdata, Page & Norris (2009) have developed a modellinking the Hebb effect with the processes of imme-diate serial recall and new word learning. Accordingto this model, the Hebb effect depends upon thequality of both a short-term representation of theitems contained in a list and a domain-generallearning mechanism which acts upon the represen-tation of those items. It follows therefore that Hebblearning might be demonstrated even in cases whereshort-term memory is compromised, because of theadditional support of a domain-general learningprocess.

Given the verbal short-term memory deficit asso-ciated with Down syndrome, the current study wasinterested in whether the Hebb effect would operatein this population. This was investigated using serialorder reconstruction tasks incorporating the Hebbrepetition paradigm. If the domain-specific facet ofHebb learning is central to determining the magni-tude of the effect, then the current sample of par-ticipants with Down syndrome would not beexpected to demonstrate a typically sized verbalHebb effect. By contrast, if learning in the Hebbeffect does not rely exclusively upon the capacity ofshort-term memory, but rather is supported by amore long-term mechanism for learning serial orderthat is independent of content, then it is possiblethat the Hebb effect will be preserved within Downsyndrome in both verbal and spatial domains. Sucha finding would have educational implications; ifindividuals with Down syndrome are able to utilisea domain-general strategy more easily than a spe-cifically verbal one, teaching could be adjusted totake this into account. If the Hebb effect is foundto operate in such a population, further work couldinvestigate its potential relationship with wordlearning, as seen in typically developing individuals.

Experiment 1

Method

Participants

Two participant groups completed the tasks. TheDown syndrome group consisted of 17 individuals

with a diagnosis of Down syndrome, ranging in agefrom 9:3 to 28:11 (years : months); mean age 19:5.These participants were recruited through schoolsfor children with learning disabilities or from adatabase of individuals who had taken part in previ-ous research carried out by the authors. The typi-cally developing group consisted of 24 individualsranging in age from 4:9 to 6:9 (mean age 5:5)drawn from local mainstream infant schools. Aslightly larger sample of typically developing indi-viduals were recruited, based on availability, inorder to increase the power of the study. All indi-viduals were native English speakers recruited withfull parental consent.

Procedure

The order that the verbal and spatial recall taskswere completed in was counterbalanced across par-ticipants. The British Picture Vocabulary Scale II(BPVS; Dunn et al. 1997) and Raven’s ColouredProgressive Matrices (RCPM; Raven et al. 1998)were administered either immediately before orafter the recall tasks as deemed appropriate on anindividual basis.

Verbal Hebb learning

The verbal Hebb learning task was based uponmethodology employed by Majerus et al. (2006)involving serial reconstruction. In this task, pre-sented as an animal race, the monosyllabic animalnames ‘bird’, ‘cat’, ‘dog’ and ‘fish’ were recorded bya male voice and used to create lists, four items inlength, sampling without replacement. A total ofnine lists were generated, one of which was selectedto be the repeated list (referred to as the Hebb list)and the remaining eight as non repeated lists(referred to as filler lists). These lists were thenamalgamated to create an experimental set ofsixteen trials, consisting of the eight filler lists plusthe Hebb list appearing eight times on every eventrial. In other words, filler and Hebb lists alternatedthroughout the sixteen trials.

The task was presented on a laptop computer.Each trial consisted of auditory presentation of thelist of four animals at a rate of one per second indi-cating the order in which they finished the race.Following this, a vertical array of four imagesdepicting the four animals was displayed on the




right hand side of the screen. An image of a ‘win-ner’s podium’, with four locations representing first,second, third and fourth positions in the race, wasdisplayed on the left of the screen. A tone signalledthe participant to recall items in the correct serialorder either verbally or by pointing to the corre-sponding image (in order to lessen verbaldemands). The experimenter selected each chosenanimal in turn whereupon the image moved ontothe appropriate location on the podium. The orderin which the images of animals were displayed onscreen was randomised for each trial in order toavoid spatial response learning. The dependentmeasure was the number of the items recalled inthe correct serial position giving a maximum scoreof four per trial.

Spatial Hebb learning

The spatial Hebb task was a variant of the Corsiblocks task, designed as an analogue of the verbalHebb task. An array of four images of ‘lily pads’each measuring 30 ¥ 25 mm was presented in a cir-cular display so that each was 45 mm from thecentral point and equally spaced from its nearestneighbours. On each trial an image of a frog waspresented on one lily pad and then it appeared tojump in sequence to the remaining three at a rate ofone per second. The frog then disappeared whilethe pads remained. A tone prompted the participantto respond by attempting to point to the pads inthe correct serial order. Upon selection by theexperimenter, each pad disappeared, and reap-peared at the start of the following trial. The depen-dent measure was the number of items recalled inthe correct serial position, again giving a maximumscore of four per trial.

Intelligence measures

The BPVS and RCPM were administered as mea-sures of receptive vocabulary and non-verbal ability,respectively. BPVS scores were converted into ageequivalent scores whereas raw scores on the RCPMwere utilised.

Results

Participants’ performance on the BPVS andRaven’s can be seen in Table 1. Independent t-testsconfirmed that the two groups were matched forreceptive vocabulary age and general non-verbalability (see table).

Hebb learning across trials

A stringent assessment of the Hebb effect requiresdemonstration that performance across successiveHebb trials is greater relative to a general increasein performance across filler trials. Initial analyseswere carried out on gradients of improvementacross the eight Hebb trials for each individual, butthese gradient measures proved to be unreliable.1

Consequently, in line with Mosse & Jarrold (2008),data from the eight trials of each list type were col-lapsed into first and second half scores (e.g. themean recall score for the first four trials and thesecond four trials independently) for both domainsto produce a measure of improvement across trials(demonstrating good split-half reliability, Spearman-Brown corrected rs ranging from 0.72 to 0.91).

1 Linear regression between performance and consecutive trials didnot provide a good fit to the data (rs ranging from -0.85 to 0.87)and reliability for these slope measures was generally poor(Spearman-Brown corrected rs ranging from -0.26 to 0.57).

Table 1 Descriptive statistics forintelligence measures by group forExperiment 1

DS TD

t PM SD M SD

BPVS in months 76.71 25.57 75.63 13.09 0.16 0.86RCPM 16.94 5.30 17.58 4.55 -0.42 0.68

BPVS, British Picture Vocabulary Scale II; DS, Down syndrome; RCPM, Raven’s ColouredProgressive Matrices; TD, typically developing.




An analysis of variance with domain (verbal/spatial), list type (filler/Hebb) and half (1st/2nd) asrepeated measures factors and group (typicallydeveloping/Down syndrome) as an independentmeasures factor was conducted on the data (seeTable 2). This revealed a main effect of list type,F1,39 = 9.89, P < 0.01, such that mean recall onHebb lists (M = 2.52, SE = 0.15) was greater thanthat on filler lists (M = 2.31, SE = 0.21). The maineffect of group was also significant, F1,39 = 5.93,P = 0.02, with typically developing participantsshowing greater overall performance (M = 2.75,SE = 0.18) than participants with Down syndrome(M = 2.09, SE = 0.21). The main effects of domain,F1,39 = 1.61, P = 0.21, and half, F1,39 = 3.90,P = 0.06, failed to reach significance, although therewas a suggestion of generally superior performanceon the spatial task. Post hoc analysis of the effectsizes for the list type effect showed this to beslightly more marked in the group with Down syn-drome (h2

p = 0.28) than the typically developinggroup (h2

p = 0.18).The interaction between domain and group was

significant, F1,39 = 4.37, P = 0.04 (see Fig. 1). Posthoc analysis revealed significantly greater verbalrecall among the typically developing group thanthe individuals with Down syndrome, t(39) = 3.21,P < 0.01. By contrast, spatial recall was not signifi-cantly greater in the typically developing group thanin the Down syndrome group, t(39) = 1.08, P = 0.29

(see Fig. 1). This pattern is entirely congruent with

what would be expected from a Down syndromepopulation given the existing evidence for a selec-tive verbal short-term memory deficit. All remaininginteractions failed to reach significance, allP-values > 0.05.

Discussion

The central aim of this first experiment was toexplore the possibility of eliciting a Hebb effect inparticipants with Down syndrome. Furthermore,presenting the Hebb recall tasks in both verbal andvisuospatial domains enabled an investigation ofwhether the functional equivalence demonstrated byCouture & Tremblay (2006) could be replicated inthe current samples. If the Hebb effect reflects thesupport of a domain-general mechanism, such thatit is not exclusively supported by verbal short-termmemory, then it may be preserved in Down syn-drome. In addition, if the Hebb effect is linked tothe acquisition of new phonology, this may shedsome light on the relative success in vocabularydevelopment associated with the disorder, and inturn have implications for single cases of acquiredverbal short-term memory deficit.

The data clearly showed that repeating lists ofitems served to significantly improve recall as shownby the significant main effect of list type. In otherwords, participants showed superior recall of Hebblists which repeated every other trial, than non-repeating filler lists, despite there being no reason

Table 2 Descriptive statistics for analysis of variance by group forExperiment 1

Domain List Half

DS TD

M SD M SD

Verbal Filler 1st half 1.69 0.94 2.84 1.162nd half 1.60 0.77 2.48 1.11

Hebb 1st half 1.97 1.14 2.97 1.232nd half 2.06 0.99 2.95 1.27

Spatial Filler 1st half 2.47 1.17 2.73 0.842nd half 2.18 1.13 2.51 0.98


DS, Down syndrome; TD, typically developing.

Figure 1 Mean correct recall for verbal and spatial tasks inExperiment 1 (error bars for this and subsequent figures represent�1 standard error). DS, Down syndrome; TD, typicallydeveloping.




why Hebb lists should be intrinsically easier toremember. This indicates that there is a Hebb effectoperating in the current data, despite the young ageof the control group participants. The relativelysmall, but reliable, improvement because of repeti-tion evident in such a sample of children is entirelyconsistent with both Mosse & Jarrold (2008) andan unpublished study cited by Page & Norris(2009). Both of these studies demonstrate subtleHebb effects in children that are difficult to elicitexperimentally. More interestingly, the Hebb effectemerges to the same extent within Down syndrome.While the typically developing individuals showedslightly higher performance overall, the lack of asignificant interaction between group and list typeindicates that both groups responded to filler andHebb trials in a similar way; indeed the magnitudeof the list type effect was numerically slightly largerin the Down syndrome group than in the typicallydeveloping group. Therefore, despite showingreduced verbal short-term memory performance,individuals with Down syndrome demonstrate thesame degree of repetition-based serial orderlearning.

Perhaps unsurprisingly, given the existing evi-dence of a specific verbal short-term memory deficitassociated with Down syndrome, the group withDown syndrome showed an effect of domain,reflecting superior performance in the spatial taskrelative to the verbal task. In line with Mosse &Jarrold (2008), the current analysis failed to findany interaction between domain and list type, andmore importantly, any interaction between domain,list type and group. Therefore, despite reducedverbal task performance by participants with Downsyndrome, the Hebb effect operated in an approxi-mately equivalent manner in both domains.

Having said this, Hebb learning typically involvesthe divergence of performance on Hebb lists relativeto filler lists across the study. An interactionbetween the list type and half of trials would be aclear indication that such a divergence was occur-ring, although on this occasion, this was notobserved. The fact that there was, however, a listtype effect implies that there is at least some reli-able effect of repetition on serial order recall, andthe lack of list type by half interaction may wellreflect the limitations of employing such a youngcontrol group. Mosse & Jarrold (2008) did find an

interaction between list type and half among aslightly older sample of 5- to 6-year-old typicallydeveloping children, but crucially, the observedHebb effect differed from that seen in typical adultstudies; recall on Hebb trials was maintained in theface of a significant decline in recall of filler trials inthe second half of the task.

Such a decline in filler performance, hinted at inthe current study (see Fig. 2), could potentially bedue to fatigue effects that might well be expected tooperate with particularly young participants. Fur-thermore, in order for the current task difficulty tobe age-appropriate, only four items were presentedper trial. Consequently, with just four items andfour serial positions in which to place them, vari-ability between filler lists was limited. In addition,some filler lists would have been near approxima-tions of the Hebb list itself. Consequently it is pos-sible that a decline in filler list performance mightfollow from the confusability between the presenteditem lists. Simply generating the Hebb and fillerlists from distinct sets of items would reduce theextent to which interference from the Hebb listcould influence recall of filler lists, and thisapproach was adopted in the second study.

In addition, in the first study there may havebeen a degree of interference resulting from therepetition contained in the Hebb lists, whichoccurred on every other trial. Couture et al. (2008)demonstrated that ‘dual learning’ may occur intasks incorporating the Hebb repetition paradigm;in addition to the correct responses, errors may alsobe learned across trials. If learning on Hebb lists,

Figure 2 Mean correct recall of Hebb and filler lists across thefirst and second half of trials in Experiment 1. DS, Downsyndrome; TD, typically developing.




correct or incorrect, carries over from one Hebblist to another, it is plausible to suggest that ithas the potential to likewise influence recall on fillerlists.

Given the now clear evidence for the domain-general nature of Hebb learning, the second studyreported here did not investigate spatial Hebblearning further, but rather focussed on verbal serialrecall, as the domain of greater interest because ofthe typical relationship between verbal memory andvocabulary, and the associated deficit in short-termmemory in Down syndrome. In addition, two mea-sures were taken to address the issues of interfer-ence raised above which may have reduced thepower of the first study to show a divergencebetween Hebb and filler lists. First, in order toexamine more clearly the effect of repetition onrecall, a verbal Hebb task replicating the same basicprocedure as Experiment 1, but with the presenta-tion of a block of consecutive filler lists before ablock of consecutive Hebb lists, was completed. Itwas hoped that this would allow a purer measure ofHebb repetition and general filler performance tobe obtained while reducing cross-list interference.An additional verbal Hebb task was conducted inthe same way as in the first experiment for com-parison. Second, in both tasks, Hebb and filler listswere created from distinct sets of items to reduceinter-list confusability. This manipulation reducedthe similarity between lists of each type andremoved the potential for the transfer of learningacross lists.

Experiment 2

Method

Participants

Thirteen individuals with Down syndrome tookpart in the study, with a mean age of 20:9 (rangingfrom 13:1 to 30:4). Eleven of these individuals hadtaken part in Experiment 1. All participants wererecruited as before. Nineteen children from main-stream schools aged between 4:11 and 6:0, with amean age of 5:6, comprised the typically developinggroup (none of whom took part in Experiment 1).All participants were native English speakersrecruited with full parental consent.

Procedure

Participants completed the BPVS between the twoHebb learning tasks, the order of which was coun-terbalanced across individuals.

Interleaved and Blocked Hebb learning

The two Hebb learning tasks were based upon thesame basic animal race procedure as in the previousstudy. Sixteen animal names were recorded by amale voice and used to create four sets of fouranimals; bee, cow, duck and fox; cat, fish, owl andsnail; bear, dog, mouse and sheep; frog, hen, pig andsnake. These names were selected from a set ofobject names with accompanying pictures compiledby Morrison et al. (1997). The items were matchedon the basis of the norms of ‘age of acquisition’ and‘age of acquisition 75%’; and adults’ estimations of‘imageability’, ‘familiarity’ and ‘picture-nameagreement’.

The experiment consisted of two tasks, an inter-leaved task and a blocked task. In each, filler andHebb lists were drawn from an independent animalset, so that eight animals were presented in a singletask. The four lists were distributed across the twotasks using the Latin square method, so that eachlist appeared in filler and Hebb contexts equally.The procedure for the interleaved Hebb learningtask was identical to that in the first study, with atotal of sixteen trials, with filler and Hebb listsalternating. In the blocked Hebb learning task,eight filler lists were presented consecutively, fol-lowed by eight consecutive Hebb lists. As before,the dependent measure was the number of itemsrecalled in the correct serial order, with a maximumscore of four per trial on each version of the task.

Intelligence measure

The BPVS was completed as a standardisedmeasure of receptive vocabulary.

Results

Performance on the BPVS was shown to be equiva-lent across typically developing participants andthose with Down syndrome (Ms = 79.58 and79.54, SDs = 10.68 and 21.23, respectively),t(16.19) = 0.01, P = 0.99.




As in Experiment 1, each list type was collapsedinto first and second half scores for each version ofthe Hebb task,2 with moderate to good split-halfreliability (Spearman Brown corrected rs rangingfrom 0.41 to 0.83).

An analysis of variance with task (interleaved/blocked), list type (filler/Hebb) and half (1st/2nd) asrepeated measures factors and group (typicallydeveloping/Down syndrome) as an independentmeasures factor was conducted on the data (seeTable 3). A significant main effect of list type wasrevealed, F1,30 = 26.75, P < 0.01, reflecting greaterrecall on Hebb lists (M = 2.44, SE = 0.15) comparedwith filler lists (M = 1.84, SE = 0.15). Post hoc analy-sis of this list type effect showed that both the typi-cally developing group and the group with Downsyndrome demonstrated medium sized effects of listtype (η2 0 53 0 42ps = . .and , respectively).

The main effect of group was also significant,F1,30 = 6.42, P = 0.02, such that participants withDown syndrome showed lower overall performance(M = 1.79, SE = 0.21) than the typically developingparticipants (M = 2.49, SE = 0.18). The main effectof task failed to reach significance, F1,30 = 1.79,P = 0.19, as did the effect of half, F1,30 = 1.12,P = 0.30.

The interaction between task and half was signifi-cant, F1,30 = 5.68, P = 0.02. Figure 3 shows thisinteraction for each group independently. Post hocanalysis indicated that in the blocked task, recallscores increased significantly across the second halfof each block, F1,31 = 5.91, P = 0.02. By contrast,performance did not differ significantly across thetwo halves of the interleaved task, F1,31 = 0.19,P = 0.67.

The list by half interaction also reached signifi-cance, F1,30 = 5.34, P = 0.05. Figure 4 shows thisinteraction for each group independently. Post hocanalysis showed that while performance on fillertrials did not differ as a function of half,F1,31 = 0.09, P = 0.76; performance on Hebb trialswas significantly greater during the second half oftrials relative to the first half of trials, F1,31 = 5.03,P = 0.03. Additionally, identical effect sizes

2 Again linear regression between performance and consecutivetrials did not result in a good fit to the data (rs ranging from -0.76

to 0.88), and the reliability for the slopes was also low to fair(Spearman-Brown corrected rs of -0.37 and 0.58).

Table 3 Descriptive statistics for analysis of variance by group forExperiment 2

Task List Half

DS TD

M SD M SD

Interleaved Filler 1st half 1.83 0.99 2.25 0.952nd half 1.38 1.11 2.03 1.07


Blocked Filler 1st half 1.63 0.94 2.03 0.892nd half 1.50 1.01 2.34 0.99


DS, Down syndrome; TD, typically developing.

Figure 3 Mean correct recall for interleaved and blocked tasksacross the first and second half of trials in Experiment 2 for eachgroup. DS, Down syndrome; TD, typically developing.

Figure 4 Mean correct recall of Hebb and filler lists across thefirst and second half of trials in Experiment 2 for each group. DS,Down syndrome; TD, typically developing.




(h2p = 0.13) were found across both participant

groups for this interaction, and the list by half bygroup interaction was also clearly non-significant,F1,30 = 0.02, P = 0.90. The task by group interactionwas not significant, F1,30 = 0.18, P = 0.68, andneither was the task by list interaction, F1,30 = 0.69,P = 0.41. The remaining two-and-three-way interac-tions, and the four way interaction, also failed toreach significance, all Fs < 1.

Discussion

Restructuring the Hebb recall task, so that repeatedlists are presented consecutively, rather than atregular intervals in between non-repeating lists, canbe considered as a Hebb paradigm in perhaps its‘purest’ form. The central aim of this second studywas to remove the potential for interference and thelearning of errors in filler lists, in order to get aclearer measure of the effect of repetition on serialorder memory among individuals with Down syn-drome, relative to typically developing controls.

Repetition served to significantly increase recall,again reflected in the list type effect, replicating thecentral finding of the previous experiment. Cru-cially, on this occasion, a divergence between Hebband filler lists was demonstrated across the first andsecond half of each set of trials. As indicated by thelist by half interaction, recall on Hebb listsimproved significantly across the first and secondhalf of Hebb trials, in comparison with the consis-tent performance elicited by filler lists. This is astronger manifestation of the Hebb effect than thatevident in the first experiment. Although there wasno reliable effect of task, the task by half interactionwas significant, with recall improving over the twohalves of the blocked task, but not the interleavedtask.

Taken together, the above two interactions aresuggestive of a recall advantage in the blocked task.While improvement in blocked task performanceacross the second half of each block was greater forHebb lists over filler lists, performance in thesecond half of each block was seen to be greaterthan in the first for the blocked task only. Given thelack of significant recall improvement across thetwo halves of the interleaved task, it is highly pos-sible that a degree of fatigue developed during thecourse of the task. By contrast, superior recall in

the second halves of each list type in the blockedtask further reinforces the notion that fatigue mayhave been affecting performance in the interleavedtask.

The most notable finding concerns the relativeperformance of the two participant groups. Thegroup effect indicated that individuals with Downsyndrome were less successful overall on thesetasks, which is unsurprising given their verbalnature. Despite this, participant group failed tointeract with any other factor, demonstrating anessentially equivalent elicitation of the Hebb effectin both groups, a suggestion again supported bysimilar effect size estimates in the two groups. Whilethese were numerically slightly larger for the typi-cally developing participants, both groups showedmedium sized effects of a similar overall magnitude.This key finding strengthens the finding from thefirst experiment that a typically sized Hebb effect isapparent in participants with Down syndrome. Fur-thermore, serial ordering within verbal short-termmemory and repeated serial order learning within averbal short-term memory paradigm can be seen tobe dissociated in the current sample of individualswith Down syndrome. While verbal short-termmemory capacity was evidently reduced relative totypically developing participants, the extent towhich repetition benefited recall was not comprisedin individuals with Down syndrome. Indeed, thetwo groups showed identical effect sizes for theinteraction between list type and experiment half,which is the key test of the Hebb effect, and whichtherefore indicates that both samples showed thesame level of benefit from Hebb repetition.

General discussion

As a measure of long-term learning of serial order,through repetition, the Hebb effect has been shownto relate to the acquisition of new phonology. Thetwo experiments presented here principally investi-gated whether the Hebb effect could be demon-strated in a sample of individuals with Downsyndrome. Most importantly, both experimentsdemonstrated the essential preservation of the Hebbeffect in this population. While the typically devel-oping group produced significantly greater overallrecall scores for verbal material than did the group




with Down syndrome in each experiment, there wasno evidence that group interacted with any of thelist type manipulations within the tasks. Of course,a degree of caution should be exercised when inter-preting null results, especially when relatively smallsamples are employed as was the case here.However, it is important to emphasise that whenHebb effects were observed in these experiments,the analysis of the size of these effects in the twogroups separately showed that the degree of Hebblearning seen among individuals with Down syn-drome was comparable to that seen in controls (andin Experiment 1 was slightly greater).

This key finding, consistent across both experi-ments, supports the notion that the Hebb effect isessentially intact in Down syndrome, and that this,perhaps more implicit, form of memory remainsintact. Non-verbal skills were assessed in Experi-ment 1 using the RCPM. The two groups per-formed comparably on this measure, suggesting thatcomparable Hebb learning in Down syndrome isnot a consequence of superior non-verbal skills inthis sample. Indeed, given our evidence that theHebb effect operates at the domain-general level,matching for language level using the BPVS (as wasperformed in both experiments) should provide ameaningful basis for comparing the effect across thetwo groups. While, the relationship between degreeof Hebb learning and non-verbal ability might be auseful avenue for future research, the key point toemphasise is that an intact Hebb effect wasobserved among individuals with Down syndromein the presence of a clear deficit in verbal short-term memory. These experiments therefore providefurther support for the claim that the Hebb effectoperates independently of absolute verbal short-term memory ability, reflecting the support of adomain-general serial order mechanism.

The Hebb effect is considered to be a potentiallyimplicit effect as awareness of the repetition doesnot appear to be necessary for a benefit to beobserved. However, awareness was not tested hereprimarily because of the perceived difficulty inusing a self-reported measure. There is evidencethat while children as young as five have the capac-ity for some introspection, they are less able atmaking accurate judgments about the course oftheir ideas (Flavell et al. 2000). As such, it was notpossible to verify that the current Hebb effect was

wholly implicit. In order to minimise possibility ofexplicit memory processes, the presentation of itemsin the test phase was varied on each trial in order toavoid any motor-based sequential learning; but therole of explicit memory can not be ruled out.However, it remains plausible that the resultantHebb effect was largely implicit, and on an informallevel, participants did not report awareness of therepetition. Certainly, a discrepancy between implicitand explicit memory processes within Down syn-drome is consistent with research by Vicari et al.(2000). They found that a group of individuals withDown syndrome showed comparable implicitmemory functioning to a group of typically devel-oping children (matched for mental age), regardlessof whether the task demanded verbal or visual per-ceptual processing. By contrast, participants withDown syndrome demonstrated significantly lowerperformance on explicit memory tasks than typi-cally developing participants. Individuals withDown syndrome have also been shown to benefitfrom sequence repetition in an implicit procedurallearning task to the same degree as a mental agematched control group (Vicari et al. 2007).

The second key finding extends work by Couture& Tremblay (2006), who reported a functionalequivalence between verbal and spatial domains inan adult population, to include individuals withDown syndrome. In Experiment 1 no reliable differ-ences were evident in the established Hebb effectacross the two domains for either group of partici-pants. Given that this serial order learning appearsto occur independently of domain, the resultantHebb effect is an example of a domain-generalprocess. Therefore, while verbal and spatial memorymay operate on dissociable representations, theyappear to share a serial order mechanism.

Returning to our original hypotheses, we pro-posed that if the domain-specific facet of Hebblearning is central to the magnitude of the effect,then a typically sized Hebb effect would not beexpected in the current sample of participants withDown syndrome. In contrast, we argued that if theHebb effect is not wholly reliant upon serial order-ing within short-term memory, but is supported bya serial order mechanism independent of content,the Hebb effect would likely be preserved withinDown syndrome in both verbal and spatialdomains. The current data are clearly consistent




with the second of these hypotheses as a Hebbeffect of typical magnitude was evident in Downsyndrome.

Taken together with the earlier findings of Mosse& Jarrold (2008), this result suggests that the rela-tively strong word learning abilities in Down syn-drome may be dependent on an implicit anddomain-general form of memory that focuses onthe serial order of items regardless of their content.In turn, this claim has implications for the way inwhich individuals with Down syndrome are pre-sented with new information in educational ortherapeutic contexts. Specifically, strategies employ-ing a more implicit approach may be more success-ful than those adopting a more direct and complexapproach. For example, multiple presentations withindirect associations and learning opportunities maybe more advantageous than single presentationssupported by explicit instruction.

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Accepted 13 January 2010




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Searching for the Hebb effect in Down syndrome: evidence for a dissociation between verbal short-term memory and domain-general learning of serial order