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The British Psychological Society
Journal of Neuropsychology (2010), 4, 147–166 q 2010 The British Psychological Society
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Evidence for a workspace model of working memory from semantic implicit processing in neglect Sergio Della Sala*, Marian van der Meulen, Patricia Bestelmeyer and Robert H. Logie Human Cognitive Neuroscience and Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, UK Three experiments tested the hypothesis that activation of semantic memory from perceptual input does not require initial retention of the perceptual material in working memory as assumed by a widely held view of information processing. In Expt 1, two brain-damaged patients with left-sided unilateral spatial neglect were tested. They were asked to listen to and read a series of familiar (British) and unfamiliar (foreign) proverbs and to choose which proverb was the best match to a depicted figure shown with the target object(s) on the left (neglected side) of the patients’ visual field. Expt 2 simulated the testing conditions for the neglect patients with healthy participants using subliminal presentation of one half of each picture. Using different materials, Expt 3 replicated the outcomes of Expts 1 and 2 with a third neglect patient and a new group of controls. In all three experiments, participants appeared to be unaware of target features; however they selected familiar, but not unfamiliar, target proverbs above chance. The results showing implicit processing of semantic material can be explained by a model in which working memory is a separate system that deals with activated contents of semantic memory, and in which there is direct activation of semantic memory from perception without intermediate stages of processing in working memory.
Working memory is often viewed as a form of transit lounge that acts to hold perceptual input on its way to long-term memory (LTM). This was the view in the widely cited model proposed by Atkinson and Shiffrin (1968), and still appears as an assumption in a wide range of contemporary, introductory textbooks (e.g., Atkinson, Atkinson, Smith, Bem, & Nolen-Hoeksema, 2003; Kosslyn & Rosenberg, 2004) as well as in some contemporary theory (e.g., Baddeley, 2002, 2007; Kosslyn, 2005). However, a body of evidence now points to the contents of working memory being interpreted, rather than raw sensory images (e.g., Barquero & Logie, 1999; Chambers & Reisberg, 1985, 1992;
* Correspondence should be addressed to Professor Sergio Della Sala, Human Cognitive Neuroscience, Psychology, Edinburgh University, 7 George Square, Edinburgh EH8 9JZ, UK (e-mail:
[email protected]). DOI:10.1348/174866410X489679
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for a review see Logie & van der Meulen, 2009). This suggests that perceptual input activates prior knowledge and experiences in semantic LTM, and it is the product of that activation which is held and manipulated within working memory. Visuospatial working memory offers a medium in which to form and store representations of the environment on which we can act mentally or which we can enact physically. The fact that the contents of working memory are interpreted also allows the participant to report and communicate these contents to others. In this paper, we investigate the hypothesis that working memory does not act as a gateway between perception and LTM. We do this by studying individuals who suffer from unilateral spatial neglect, and in particular whether patients with neglect show evidence of semantic processing of material from their neglected field. Some evidence for the contents of working memory not functioning as a gateway comes from studies of healthy adult participants who, for example, appear to have difficulty in reinterpreting the contents of a mental image. Chambers and Reisberg (1992) presented for 2 s an ambiguous figure which could be interpreted either as the head of a rabbit or as the head of a duck (Jastrow, 1900), and asked participants what they had seen. In all cases, participants interpreted the figure as depicting only one of the animals and were unable to change their initial interpretation of the figure based on their visual memory. They could only ‘see’ the alternative interpretation when again viewing the figure or after drawing their own mental image on paper. This suggests that initially viewing the stimulus directly activated stored semantic knowledge which generated a particular interpretation, and it was this interpretation that was held in working memory, not the ambiguous raw sensory information (for a detailed discussion, see Cornoldi, Logie, Brandimonte, Kaufman, & Reisberg, 1996). More recent evidence comes from an experiment reported by van der Meulen, Logie, and Della Sala (2009) in which participants were asked to remember the visual appearance of a sequence of four letters shown as a mixture of upper and lower case. During a retention interval participants either tapped out a figure-of-eight pattern or were presented with a series of irrelevant line drawings of objects. The gateway model for working memory would predict that retention of the letter appearance should be disrupted by irrelevant pictures given that the gateway is also considered to be the temporary memory system, whereas it should be relatively impervious to the effects of concurrent tapping. Results showed quite the opposite. Concurrent tapping disrupted the visual memory task while irrelevant pictures had no effect. This result did not arise simply because of differing overall cognitive load of the secondary tasks. In a second experiment, irrelevant pictures, but not tapping, were shown to disrupt the ability to make judgments about the visual appearance of letters generated as images from stored knowledge of letters in LTM. This fits with previous studies showing that irrelevant visual input disrupts image generation but not visual temporary memory (e.g., Andrade, Kemps, Werniers, May, & Szmalec, 2002). Irrelevant visual input is particularly disruptive of tasks that require activation of the semantic as well as visual properties of stored knowledge, such as in the peg-word imagery-based mnemonic technique (e.g., Logie, 1986; Quinn & McConnell, 1996, 2006). In other words, perceptual input appears to interfere with the process of retrieving the visual properties of material from stored knowledge, suggesting that perceptual input has direct access to stored knowledge about visual stimuli. It does not disrupt the contents of working memory, suggesting that working memory does not function as a gateway between perception and LTM, and nor is there substantial overlap between the system for generating images and the system for retaining visual appearance in memory.
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A second, converging, source of evidence comes from experimental studies of braindamaged individuals (see review in Della Sala & Logie, 2002). Some brain-damaged patients appear to be able to process perceptual input without being able to report what they have perceived. This suggests access to stored semantic knowledge without the involvement of working memory. The best example comes from patients who suffer from unilateral spatial neglect. A key cognitive deficit in such patients is that they ignore one half of extra personal space, most commonly the left, following a lesion in the right parietal lobe (Kinsbourne, 2006). Thus, when asked to copy a picture, they will reproduce only the right half of the picture. When asked to describe their immediate environment, they will describe only the right half of the scene in front of them. In formal testing, when asked to mark all items in an array of stimuli, they will ignore stimuli within the left half of the array. This deficit does not arise from failure of the visual sensory system, and is generally interpreted as a lateralized impairment of spatial attentional control (e.g., Danckert & Ferber, 2006; Ellis, Jordan, & Sullivan, 2006; Husain & Nachev, 2007; Pisella & Mattingley, 2004; Ptak, Golay, Mu ¨ ri, & Schnider, 2009). Several researchers have also shown a deficit in spatial working memory in patients with neglect (e.g., Beschin, Cocchini, Della Sala, & Logie, 1997; Logie, Beschin, Della Sala, & Denis, 2005; Malhotra et al., 2005; Wojciulik, Husain, Clarke, & Driver, 2001). The hypothesis being tested in the experiments we report is entirely compatible with this view in that we would argue that activation of LTM from perception is not dependent on an intact working memory system. Of core interest to the topic discussed in this paper, namely the understanding of the relationship between LTM and working memory, is that people with neglect appear to be affected implicitly by some of the visual information on their left side that they appear to ignore. A now classic example is that of patient P. S. (Marshall & Halligan, 1988), who was shown a picture of two houses, one above the other. One of the houses looked perfectly symmetrical and normal, while the other house was identical except that it was depicted with flames emerging from a window on the left of the picture. The patient was asked to indicate whether the two houses were the same or different in any way. She consistently reported that the houses were identical. However, when P. S. was asked to choose in which house she would prefer to live, she chose the house without the flames well above chance level while claiming that this was a complete guess. The ‘burning house’ result has been replicated in later studies (e.g., Doricchi & Galati, 2000) and interpreted as being the result of an automatic reaction to fearful stimuli (Vuilleumier, Schwartz, Clarke, Husain, & Driver, 2002). However, while a real fire might generate such an automatic response, the response to a depicted fire would be more likely a learned response. Indeed, similar findings have been reported from studies using pictures of chimeric figures (e.g., Buxbaum & Coslett, 1994; Cantagallo & Della Sala, 1998; Peru, Moro, Avesani, & Aglioti, 1996, 1997; Young, Hellawell, & Welch, 1992), that show the right half of one object/animal joined to left half of another object/animal. Some neglect patients demonstrated that they were implicitly processing the left half of the stimulus while maintaining that the two pictures were identical despite their chimeric nature. For example, Cantagallo and Della Sala’s (1998) patient was presented with the drawing of a trombone with a rifle butt coming out from its left side. Spontaneously, he reported that he was seeing a ‘trombone which fired notes’. Evidence that implicit processing in neglect can result in access to semantic knowledge comes from a study by McGlinchey-Berroth, Milberg, Verfaellie, Alexander, and Kilduff (1993). They showed that neglect patients improved their performance in a lexical decision task after they were primed by brief presentation of relevant
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(semantically related) pictures in their neglected field. Similar results have been shown by Berti and Rizzolatti (1992), Ladavas, Paladini, and Cubelli (1993), and McGlincheyBerroth et al. (1996). An analogous finding has been reported in patients with extinction, showing that they can successfully make categorical judgments, based on same–different judgments about material in the extinguished field of which they are unaware, either in the visual (Berti et al., 1992; Mattingley, Davis, & Driver, 1997; Volpe, Ledoux, & Gazzaniga, 1979) or in the tactile (Berti et al., 1999) modality. Priming effects have been observed also in a number comparison task with primes presented to the left (neglected) hemifield (Sackur et al., 2008; Schweinberger & Stief, 2001), and implicit semantic processing has been shown in neglect dyslexia (Ladavas, Umilta´, & Mapelli, 1997). Recently, Esterman et al. (2002) presented pictures for 200 ms in the neglected field followed by a verbal stem for completion. In one condition, neglect patients were told to try to complete the stem based on the picture that had recently been presented. In a second condition, the patients were told to complete the stem specifically not based on the previous picture. The patients tended to complete the stem based on the previous picture in both conditions, showing that they were unable to inhibit the effect of the picture prime. However, when pictures were presented in the non-neglected field, patients could readily generate a stem completion that was unrelated to the picture content. This poor inhibition of the material in the neglected field was interpreted as evidence that the patients were indeed not aware of its contents even if they showed effects of semantic priming. The results further indicate that the implicit semantic processing in neglect does not arise from residual explicit processing from the neglected field. Taken together, the data from neglect suggest that sensory inputs are not necessarily held within working memory en route to LTM. All the above studies demonstrate that there may be semantic priming in some patients with neglect, and as such offer additional insight into what processing might still be intact in these patients. However, semantic priming that results in faster lexical decision times and in correct verbal stem completion leaves open the question as to whether more complex, integrated representations can be activated in the neglected field and whether these activations can influence more complex explicit processing. If implicit effects of these more complex processes were to be observed, they would very substantially extend the findings of more subtle effects of implicit processing in previous studies of neglect. They also would have implications for the relationship between working memory and long-term semantic knowledge in the healthy brain. Specifically, they would point to a direct activation of semantic knowledge from perception, without the need for any processing or representation in a working memory system. This link between implicit processing in neglect and the role of working memory in information processing has not been made explicit in the studies we discuss above, and we address this directly in the study we describe here. A further theoretical issue is the extent and nature of the implicit processing that occurs and that is necessary to allow patients to respond without apparent awareness of the stimuli in the neglected field. One possibility is that there is activation of the representation of individual features of the depicted items without the formation of an integrated representation or identification of objects. This might allow spreading of activation, for example from depictions of single objects to single words that are both part of the same semantic network (e.g., Esterman et al., 2002). This idea fits with our own argument that perceptual processing and activation of semantic memory occur prior to access to working memory in the healthy brain. However, as we have also argued, the identification of objects and the interpretation of scenes may, in the healthy
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brain be accomplished in advance of the involvement of working memory. Therefore, it is possible that in neglect patients, rather more complete and integrated representations are formed from depicted objects, but their disorder prevents those representations from accessing working memory. This should allow patients to link complete objects depicted in their neglected field with associated complex verbal material (rather than single words) that refers to those objects and which is stored in, and easily accessible from semantic LTM. Here, it is important to note that neglect patients typically have intact verbal short-term memory, and intact semantic and episodic LTM (Denis, Beschin, Logie, & Della Sala, 2002). We tested this hypothesis with two new single case studies (Expt 1) by asking patients with severe neglect to listen to a series of proverbs and to choose which proverb was the best match to a depicted human figure who was shown with the target object(s) in the left of the patients’ visual field. Expt 2 followed a similar procedure by simulating neglect in a group study of healthy individuals using subliminal presentation. Expt 3 replicated Expts 1 and 2 with a third patient, a new group of controls and with different materials. Proverbs were chosen because they are memorable forms of language given their concrete contents (Highbee & Millard, 1983) and familiar proverbs are often highly overlearned (Pasamanick, 1983). They are also easily represented as visual images (Gibbs, Stro¨m, & Spivey-Knowlton, 1997), and materials that can be represented in multiple modalities lead to robust memory representations (Paivio, 1971). This fits with previous studies showing that perceptual input appears to interfere with the process of retrieving the visual properties of material from stored knowledge, suggesting that perceptual input has direct access to stored knowledge about visual stimuli (e.g., Andrade et al., 2002; Logie, 1986). In other words, direct visual perceptual input does not disrupt the contents of working memory, suggesting that working memory does not function as a gateway between perception and LTM. If the implicit processing extends only to individual features of depicted material on the neglected side, then patients should show no difference between familiar and unfamiliar proverbs as both types of proverb will contain single words related to the target features. As such we would expect that if neglect patients do show evidence of implicit activation of related verbal material, then any such effect would be much stronger in cases where there is an established representation in semantic memory, such as for familiar proverbs, than for text which refers to the depicted object(s) but is new to the patient (unfamiliar proverbs).
EXPERIMENT 1 This experiment involved testing two brain-damaged patients who showed clear unilateral spatial neglect. It is worth noting that in order to identify the cases reported here, seven additional neglect patients were considered. However, these other patients were not appropriate for the experimental procedure; in some cases the neglect was relatively mild and the patients could explicitly process some of the material on the neglected side. In other cases, the neglect was too severe or patients were unwilling to complete the testing session and so testing was curtailed for ethical reasons. Indeed, previous studies have reported that, for very similar reasons, only some neglect patients show evidence of implicit processing (e.g., Peru et al., 1996). The selected patients are identified by anonymized initials.
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Case 1 C. K., was a 78-year-old man, left-handed, and blind in his right eye. He was tested 11 days after his stroke, while still on the acute stroke ward, at which time he was able to sit up straight next to his bed and communicate well. He was diagnosed with left arm weakness due to a right-sided stroke. A CT scan carried out 1 day after the stroke showed an area of low attenuation in the right fronto-temporal lobe, consistent with an ischemic infarct. C. K. also presented with clear clinical symptoms of visuospatial neglect, and clear signs of neglect on formal diagnostic tests from the behavioural inattention test (BIT; Wilson, Cockburn, & Halligan, 1987). For example, he systematically bisected lines substantially to the right of the mid-point, and failed to score out target letters or line segments displayed on the left of large arrays. However, he had no difficulty matching pictures shown in the non-neglected field with auditory verbal descriptions. This further suggested that he had no comprehension difficulties. There was no evidence of representational neglect, tested with the drawing from memory task from the BIT.
Case 2 H. R. was an 86-year-old right-handed woman. She was tested 1 month after a right partial anterior circulation stroke. She was diagnosed with left hemispatial neglect, left upper motor neurone facial weakness, and moderate left arm and leg weakness. A CT scan showed a small infarct in the right corona radiata, as well as diffuse small infarcts. H. R. presented clear signs of neglect on formal diagnostic tests from the BIT (Wilson et al., 1987) such as bias to bisect lines substantially to the right of centre or failing to copy objects displayed on the left-hand side of a picture. Drawing from memory was within the normal range, suggesting no representational neglect. Like Case 1, H. R. showed no verbal comprehension problems.
Material Pictures Visual stimuli were 40 compound pictures, consisting of coherent (although sometimes bizarre) scenes of a number of objects, or with a central person holding different objects (e.g., a man holding a basket with eggs in his right hand, and a watering can in his left). The left half of each picture depicted features of a specific proverb (e.g., ‘Don’t put all your eggs in one basket’), while the right half was completely unrelated to this proverb. Pictures were compiled from a range of sources: Corel Gallery, 2005 (online database - retrieved January 2005 from http://www.corel. com); Huitema, 1996; Microsoft Office Clip Art, 2003 (computer software); Snodgrass and Vanderwart, 1980. All items within one picture were images chosen to be of similar style and quality, to maintain the uniformity and consistency within each stimulus. Stimuli ranged in size from 15 to 20 cm in width and height and were printed on A4 paper. They were always in black and white or shades of grey, apart from one left-sided item that functioned as the main clue to the correct proverb (e.g., the basket with eggs), and one unrelated right-sided item of similar size and in roughly the same position on the right of the midline (the watering can). These two items were always presented in realistic colours.
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To avoid the possibility that the patient learned that the left halves of the pictures always contained the clues to the correct proverbs, mirror versions of all stimuli were constructed. A quarter of all trials (i.e., 10 of the 40 stimuli) were given in mirror version. Proverbs The proverbs presented with each picture were taken from various published collections (Flavell & Flavell, 2004; Miedler & Dundes, 1994; Stoett, 1901) and online databases (website of manythings.org; website of ucla.edu). The set of 40 stimuli was divided into two subsets of 20, one representing common familiar British proverbs, the other unfamiliar foreign (Dutch) proverbs. An additional 8 stimuli were used in practice trials. The Dutch proverbs were translated literally, and modified when necessary to make them grammatically correct and flow well in English. For each of the 40 target proverbs, a foil and two distracter proverbs were selected. The foil was a proverb that contained the same keyword as the target (e.g., ‘You can’t teach grandma to suck eggs’, in the above example). The distracters were two proverbs that were completely unrelated to the target and foil, and to the picture. However, the distracters also shared a keyword between them, to prevent a response bias of patients to one of the two proverbs that had a word in common. Each set of four proverbs therefore contained two pairs of proverbs with the same keyword. The sets of proverbs were recorded digitally by a male native English speaker who was blind to the aim of the experiment. A series of pilot studies with English native speakers assured familiarity versus unfamiliarity by ranking the proverbs until the two sets were completely separate and clearly categories as familiar and unfamiliar. Examples of a picture, target proverb, and distracters for a familiar and unfamiliar proverb are given, respectively, in Figures 1 and 2. Pictures were piloted with healthy volunteers until the clues in the left half were clear and unambiguous, and the right halves were clearly unrelated to any of the four proverbs. With the definitive set of materials, 10 healthy control participants and 9 right hemisphere damaged patients with no neglect all performed at ceiling – selected the correct proverb for all 40 trials – on the experimental test. Experimental procedure The procedure followed that used by a range of previous studies (e.g., Bisiach & Rusconi, 1990; Forti & Humphreys, 2007; Marshall & Halligan, 1988) to examine implicit processing in neglect. Pictorial stimuli were placed one by one in front of the patient centred on his/her midline with no time constraint for inspection. He/she was asked to examine each picture carefully, and to name all items that could be seen. Trials were then classified according to whether (aware) or not (unaware) he/she described target features on the left of the picture. While each picture was in view, the four associated proverbs were presented from the audio recording, and he/she was asked to choose one that he/she thought best matched the picture. Proverbs were repeated as often as requested by the patient, but this was rarely more often than twice. He/she was told that some of the proverbs would be familiar and that others might be less familiar, and that the choice would not always be obvious. On those trials whereby he/she could see no relationship between any of the
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One man’s loss is another man’s gain One rotten apple spoils the barrel An apple a day keeps the doctor away A man is known by his friends
Figure 1. Example of a picture used in the experiments, with target feature on the left of the picture to be matched with a familiar proverb. The correct proverb is shown here in bold, and the foil proverb is shown in italics. Fonts were identical for all proverbs in the actual experiment.
proverbs and the picture, he/she was asked to guess. His/her response was only considered valid if he/she could repeat the complete proverb that had been chosen. When only one or two words or a vague description was given, all four proverbs were repeated until the patient was able to repeat the complete proverb selected. After having made a choice, the patient was asked why they chose that particular proverb. If they gave a response that referred to the contents of the target features in the neglected field, then this was taken as an indication that the patient had been aware of this material.
Results Case 1 Patient C. K. identified correctly all of the 10 proverbs on the mirror trials in which target features were on the right (non-neglected) side of the picture. For the remaining 30 trials, we considered separately the ‘aware’ and ‘unaware’ trials. There were 11 trials on which he reported being aware of target features depicted on the left. Of these, there were 4 familiar proverbs and 5 unfamiliar proverbs selected correctly, plus 1 foil incorrectly selected for each of the familiar and unfamiliar sets. In sum, familiarity did not drive awareness, and for those trials on which he was aware, there was no greater tendency to select the correct familiar or the correct unfamiliar proverb. Data from trials on which C. K. was unaware are summarized in Table 1. One-tailed binomial tests yielded a significantly above chance correct selection for the familiar proverbs, p , :02, and at chance performance for unfamiliar proverbs, p ¼ :40. When
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The clock ticks nowhere the way it does at home Don't jump from the ox to the donkey Don’t hang anything on the large clock Jump in the corner for someone else
Figure 2. Example of a picture used in the experiments, with target feature on the left of the picture to be matched with an unfamiliar proverb. The correct proverb is shown here in bold, and the foil proverb is shown in italics. Fonts were identical for all proverbs in the actual experiment.
asked about his reasons for each correct response he maintained that he had guessed, or he generated a confabulation unrelated to the target features presented. Case 2 When target features were on the right (non-neglected) side of the picture, Patient H. R. correctly identified all five familiar proverbs but selected three target and two foils for the unfamiliar proverbs. For the remaining 30 trials in which target features were displayed on the neglected side of the image, we considered the ‘aware’ and ‘unaware’ trials separately. On 4 out of 15 familiar trials, H. R. was aware of the target features depicted on the left. She selected the correct proverb for all four of these trials. Data from the 11 familiar and 9 unfamiliar trials on which H. R. was unaware of target features depicted on the left are summarized in Table 1. It was striking that on the 11 familiar Table 1. Number (proportion) of trials on which patients C. K. and H. R. were unaware of target features and selected the correct target, or incorrect item (foil or distracter) for familiar and unfamiliar proverbs Patient C. K. H. R.
Proverb type
Target
Foil
Distracter
Familiar (10 trials) Unfamiliar (9 trials) Familiar (11 trials) Unamiliar (10 trials)
6 (.60) 3 (.33) 10 (.91) 5 (.56)
2 (.20) 3 (.33) 1 (.09) 3 (.33)
2 (.02) 3 (.33) 0 (.00) 1 (.11)
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trials she selected 10 target proverbs and 1 foil. On a one-tailed binomial test, this performance was highly significantly above chance, p , :00001. In contrast, on the nine unfamiliar trials she selected five target proverbs, three foils, and one distracter, a performance level that is not significantly different from chance. When asked about her reasons for each correct response on the familiar or the unfamiliar ‘unaware’ trials, she maintained that she had guessed, or she generated a confabulation unrelated to the target features presented.
Discussion of single case studies Across two patients we have found evidence for above chance selection of meaningful familiar proverbs that are linked with depicted material of which each patient appeared to be unaware. The procedure and materials for Cases 1 and 2 ruled out the possibility that selection of proverbs was based on single words. The results from these two single case studies therefore are consistent with previous literature (Marshall & Halligan, 1988; McGlinchey-Berroth et al., 1993), demonstrating that some neglect patients appear to process target features, even if they were unaware of what had been presented. However, these results considerably extend those previous findings by showing that the current results cannot be interpreted as implicit processing of individual surface features of the depicted items. They point to implicit processing of material at the semantic level and suggest formation of an integrated representation of the neglected components of the scene. In terms of our earlier theoretical discussion, these results can be explained by a model of information processing in which perceptual input directly activates stored representations in LTM. In the case of our two patients, the activation is not sufficient to reach conscious awareness, even if it can affect decisions based on semantic processing. The results are much more difficult to explain in a model that assumes direct access to visual working memory from perceptual input, and then access from working memory to semantic knowledge. The stimulus material is present at the time of test, and therefore according to such a model, any material that is being processed perceptually should also be available within visual working memory for explicit report. However, we have demonstrated that the two patients cannot report features from one side of a visual stimulus, and yet show evidence that they have processed those features at a semantic level allowing activation of integrated interpretations of familiar verbal sentences. In sum, the results are compatible with models which assume direct activation of long-term stored knowledge directly from perception (Beschin et al., 1997; Cowan, 2005; Logie, 2003). Although the results for the patients were fairly clear, the question remains as to whether results derived from brain injured individuals can be extended to the characteristics of information processing in the healthy brain. This was the purpose of Expt 2 in which we tested healthy participants in the same age range as the patients. In order to simulate the testing conditions for the neglect patients, the healthy participants were shown the target pictures taken from single Cases 1 and 2, but with one half of each picture displayed very briefly and below the perceptual detection threshold for each individual participant. As for the patient studies, each picture was accompanied by sets of proverbs. The aim of Expt 2 was to explore whether healthy participants could select the target familiar proverb above chance in a paradigm intended to mimic neglect.
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EXPERIMENT 2 The major aim in this experiment was to investigate the possibility of implicit semantic processing in healthy individuals. First, a group of healthy younger adults was tested to ensure that the paradigm that we used could effectively simulate neglect with subthreshold presentations. This then acted as a feasibility study.1 Next, we tested the main group of healthy older people who were matched with the two single cases.
Methods Participants The group of healthy older volunteers comprised 30 participants (13 men, 17 women), ages 60–84 (mean 72, SD 5.69) drawn from the University of Edinburgh Psychology Department panel of volunteer members of the general public. All participants reported being in good health, were right-handed, had no known neurological deficits, and had normal or corrected-to-normal vision. They were each reimbursed £6 for their time. Materials There were two sets of materials. The first set was used to establish the perceptual threshold of each participant. They consisted of black and white line drawings of various objects (Snodgrass & Vanderwart, 1980) which subtended a visual area of 118 horizontally and 78 vertically. The second set was used for the main experimental task (matching proverbs to line drawings) and comprised the same materials (pictures and proverbs) as were used for single Case 2, described earlier, except that, in order to avoid any lateralized attentional bias across trials, the target features in the pictures were presented on the right for half of the trials and on the left for the remaining trials. Mirror versions of the images were used to counterbalance the side used for the specific targets and specific distracter features across participants. Also, stimuli were presented on a computer screen rather than on paper. Hence, materials for the proverb–picture matching task consisted of 40 images which subtended an approximate visual area of 15–208 horizontally and 15–208 vertically. All images and proverbs were presented on a computer screen with a refresh rate of 160 Hz at a viewing distance of approximately 60 cm. Procedure First, the perceptual threshold of each participant for detecting line drawings of objects was assessed. Four trials were presented in the centre of the computer screen at each of 12 different exposure times starting with 84 ms and descending to 18 ms at 6 ms intervals. Each trial consisted of a ‘ready’ message displayed for 1,000 ms, a fixation cross for 1,000 ms, a forward static noise mask for 250 ms, the object presented at the aforementioned exposure rates and a backward static noise mask for 1
Sixteen younger adults (8M, 8F), (mean age 22.6, SD 2.87) took part in the feasibility study. These were students at the University of Edinburgh. They were tested with the same procedure as for the healthy elderly participants. Results showed the predicted outcome, namely that familiar proverbs (38.8%) were identified significantly more successfully than unfamiliar proverbs (29.1%), Fð1; 15Þ ¼ 1:78, p , :02.
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250 ms. The participant was then asked to name the object and the experimenter recorded the response. The perceptual threshold was defined as failure to name the object on all four trials at a given exposure time. The presentation time for the proverb task was individually set at 6 ms below the perceptual threshold of each participant. Following the threshold task, participants were asked to perform the picture– proverb matching task. This consisted of a ‘ready’ message and a fixation cross each of which were displayed for 1,000 ms. The image was then presented for 2,000 ms plus the threshold duration. The half of the stimulus which depicted the target feature was covered by a forward static noise mask of 1,500 ms. After that the mask disappeared for the threshold duration and a backward mask of 500 ms then obscured the target side of the stimulus again. After the presentation of each picture, four proverbs were presented centrally on the computer screen, and participants were asked to select the one that matched the previously presented picture. The proverbs remained on screen until the choice was made.
Results The mean perceptual threshold of the elderly participants was 36.00 ms (range 18–72 and SD 10.08). An initial analysis showed that the side of presentation did not significantly affect performance, Fð1; 29Þ ¼ 1:29, ns. The mean correct selection of the target proverb for the British set was 34.83% (range 15–50, SD 8.71), which was significantly higher, Fð1; 29Þ ¼ 16:03; p , :001, than the mean for the foreign proverbs (25.67%, range 10–45, SD 9.01). Chance performance was 25% which was almost identical to that found for the foreign proverbs. At the end of each trial, all participants confirmed that they were consistently unaware of the target features displayed on the masked side of the stimuli, as would be expected from the thresholding procedure. However, if participants had been aware of the stimulus on occasional, individual trials and failed to report this, there is no reason to assume that this would have been more likely for pictures associated with the familiar rather than the unfamiliar proverbs.
Discussion The data from a paradigm designed to simulate in healthy participants some characteristic of neglect replicated the pattern of results from two single cases of neglect patients, suggesting that the simulation was successful. Although participants appeared to be unaware of target features depicted in subthreshold visual presentations, they nevertheless selected familiar, but not unfamiliar, target proverbs above chance. This suggests that there was activation of semantic knowledge from the subthreshold presentations. One possible caveat arises from criticisms of implicit processing in healthy participants (e.g., Shanks, Rowland, & Ranger, 2005), suggesting that it has not been proven beyond reasonable doubt that what is thought to be implicit processing is indeed non-conscious. That is, despite the care taken to make sure that our healthy participants were not aware of material presented subthreshold, there is no guarantee
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that they were not actually aware of the target material at the time of presentation. Since we have to rely on subjective reports, it is possible that the healthy participants were indeed aware of the subthreshold stimuli despite their reports to the contrary. This might then have led to them selecting the correct target proverb. However, it would be difficult to then explain the success in identifying the familiar target proverbs compared with the unfamiliar target proverbs; there is no reason to expect that participants are more likely to be aware of subthreshold stimuli for the former than for the latter. Even if we were to assume that there is some form of fleeting awareness during the trial that is forgotten at the time of the debriefing following each trial, we would have expected the foil proverbs to have been selected more frequently than the distracters, and this was not the case. Moreover, this caveat cannot apply to those instances whereby the neglect patients lacked awareness of the neglected stimuli. We were careful to select a wide range of materials to avoid the possibility of results arising from particular characteristics of the pictures or familiar/unfamiliar proverbs chosen. However, to strengthen the evidence, we conducted a further study with a third patient and a new set of control participants, using different stimulus materials and a modified procedure. The patient was selected from a group of seven neglect patients. The other six patients were not tested further for the same reasons described in Expt 1.
EXPERIMENT 3 Case 3 (R. M.) was a man, aged 75 years, who had suffered an ischemic stroke 2 months prior to testing. A structural MRI scan revealed a right posterior parietal lesion, encroaching on white matter. He showed no evidence of language or comprehension problems, as shown by normal performance on the Boston Naming Test (Kaplan, Goodglass, & Weintraub, 1976) and in understanding long complex sentences (De Renzi & Vignolo, 1962). Neglect was assessed by using tests that are widely recognized in the cognitive neuropsychology literature as being sensitive and specific to the impairment (see review in Robertson & Halligan, 1999). Specifically, he failed to copy details from the left half of geometrical shapes while they were in view or from memory. When asked to mark each item in an array of short lines arranged randomly across the page, he succeeded in marking only lines depicted on the right and when asked to detect bell shapes depicted along with a range of animal and object shapes on a page, he again detected only the bell shapes on the right. When asked to mark the mid-point of 20 cm lines, he showed the typical bias towards the right that is characteristic of neglect. In sum, he showed consistent evidence of neglect across several different tests. As for Cases 1 and 2, there was no clinical evidence of representational neglect.
Materials A new pool of British proverbs was collated by asking a wide range of friends and colleagues who were native speakers of English to list proverbs that were familiar to them. A further set of proverbs that would be unfamiliar to British participants was constructed from examples in published compendia of Russian and Chinese proverbs translated into English. For each proverb in both sets, a black and white line drawing of a human figure was made to depict referents to the proverb on the left side of the figure,
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following a similar procedure to that used before, but all were different from the pictures used for our previous study. A pilot study with 15 healthy participants was used to select a set of 20 familiar target proverbs, and 20 unfamiliar target proverbs each of which was consistently selected as being linked with the left half (but not the right half) of its relevant drawing. Two of the familiar proverbs were the same as those used for our previous study, but with different pictures. An additional 40 familiar and 40 unfamiliar proverbs were selected as non-target proverbs to give a total of 60 familiar and 60 unfamiliar items. From these, sets of six familiar or six unfamiliar proverbs were constructed; each proverb was used twice across proverb sets, so that each target proverb became a non-target proverb in another set. No proverb was used more than once as a target. This resulted in 20 trials in each of the two conditions.
Procedure and results The 20 British and 20 foreign stimulus sets were then presented to the patient in a random order on each of a series of A4 size flash cards. Both sides of each figure were shown clearly, and the figure was centred on the patient’s mid saggital plane. There were no movement restrictions. Below each figure, the target proverb was shown in a random position among five distracter proverbs. In addition, the list of six proverbs was read aloud twice (the second time in reverse order) with the figure remaining in view throughout. Patient R. M. was first asked to describe the picture in view to check if he noticed any features on the left side of the picture. He was then asked to choose the proverb that seemed most appropriate for each picture presented. After each selection, he was asked to give a reason for the selection with the picture still in view. He correctly selected eight British proverbs, which was significantly above the chance level of 3.3 (binomial test, p , :02), but was at chance (four items) for the foreign proverbs. When asked about his reasons for each correct response he maintained that he had guessed, or he generated a confabulation unrelated to the target features presented. The same materials were used with a group of 20 healthy controls (12 men, 8 women), ages 57–75 (mean 64.6), using the same procedure as in Expt 2 for subliminal presentation of the target side of the picture (half on left, half on right). The mean correct selection of the target proverb for the British set was 5.30 (range 3–9, SD 1.84), which was significantly higher, tð19Þ ¼ 3:047; p , :01, than the mean for the foreign proverbs (3.60, range 1–5, SD 1.49). Chance performance was 3.3 out of a maximum score of 20. A t test showed that performance for the British set was significantly higher than that for the foreign set tð19Þ ¼ 3:047; p , :01.
Discussion The evidence for semantic processing of material in the neglected field was shown for a third patient, replicating the results of Expt 1, together with a replication of the results from Expt 2 with a new set of controls tested with a new set of materials. This outcome adds confidence in the generalizability of the result, consistent with our hypothesis that implicit semantic processing can occur in the neglected field for neglect patients and
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with subliminal presentation for controls. This further supports the theoretical claim that visual perceptual input has direct access to semantic memory without the need to involve working memory.
GENERAL DISCUSSION The results from these three experiments indicate that representations of familiar proverbs in semantic LTM can be activated by visually presented material of which the participant is unaware, either because of a cognitive deficit arising from brain damage, or because of experimentally manipulated presentation time. The phenomenon appeared only for verbal material with which participants were familiar. This substantially extends previous findings by suggesting that activation is at the semantic level for complex visual stimuli rather than based on simple association between individual features in the display and individual words in the proverbs. Following from the theoretical considerations in the introduction, the difference in matching performance for familiar and unfamiliar proverbs can be explained by a model in which there is direct activation of semantic LTM from perception and such activation of traces in LTM operates independently of a working memory system. That is, the activation of LTM occurs without recourse to an intermediate stage of processing that then transfers information into LTM. In the latter case, visual information that was not consciously processed would be lost at the intermediate stage before that transfer could occur. The former case requires no such intermediate stage and allows for activation of existing semantic networks that influences choice of semantically related verbal material. In the healthy brain, the products of this activation would then be transferred to working memory (Logie, 2003; Logie & van der Meulen, 2009). In neglect patients, the inability to transfer the activated representations into working memory could result from an impairment of the transfer process or from damage to the working memory system itself (Della Sala, Logie, Beschin, & Denis, 2004). The above view is of a perceptually driven, or bottom-up process in which the contents of the stimulus in the neglected field activates stored representations. These activated representations would then overlap with the representations activated by explicit processing of one of the familiar proverbs. Activation of representations of the foil or other familiar proverbs would be less likely to overlap with the semantic content of the neglected field in the picture. There would be no existing representations of the unfamiliar proverbs as multiple features combined in a semantic context. This would make it much less likely that reading an unfamiliar proverb would activate exisiting semantic representations that overlap with the semantic content of the depicted materials in the neglected field. An alternative view is that instructions to the neglect patients can influence the implicit processing through top-down control. Danckert, Maruff, Kinsella, de Graaff, and Currie (1999) showed that a patient with neglect could make categorical judgments about items in their neglected field, and this could be manipulated systematically by changing their instructed goal in the task. However, in that previous study, the patients were given a single goal for their categorical judgment on each trial. In the experiments we report here, the task is not to determine whether a single presented proverb matches an aspect of the presented stimulus. Rather, the participants are given several proverbs and do not know which of these is relevant to
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the stimulus. As such, the semantic judgment is ill defined. Nevertheless, it is possible that the participants in our task undertook a top-down search as each of the four proverbs was presented. In the case of the patients, this might have led to a reexamination of the picture as each proverb was presented. It is possible that the patients then became aware of materials on the left of the picture, even although they had not been aware during their initial inspection. However, none of the patients had any difficulty with comprehension, and so they would have been aware of the contents of not only the target proverb but also of the foil proverb (in which a keyword was linked to the material on the neglected side), and the other non-target proverbs. If this form of top-down, directed search had led to awareness of the depicted materials, then we might have expected that the foil proverbs would have been chosen more than the distracters. The data in Table 1 show that this clearly was not the case. It remains possible that the target proverb in Expt 1 was selected more frequently than the foil because the latter contained a single reference to the main (coloured) target item in the picture, but the target proverb contained references to the semantic binding of the target and background. This account would fit with a finding reported by Van Fleet and Robertson (2009) in which they found that neglect patients appeared more likely to be aware of conjunctions of features on the neglected side whereas they showed effects of implicit priming from single features. However, the patients would have been as likely to undertake top-down reexamination of the picture for the unfamiliar as for the familiar proverbs, and in both cases, performance was dependent on matching the binding between target item and background in the picture with the semantic content of the target proverb. Yet, the patients did not select an unfamiliar proverb which offered a semantic match to the depicted material. This only occurred for the familiar proverbs. The familiarity manipulation in our experiments occurs for the explicit material (the proverbs), suggesting that a familiar, but not an unfamiliar, proverb activates a network of existing associations. However, a correct response can only come from a match between the activation of semantic associations linked with the target proverb and the implicit, stimulus-driven semantic activations from the material in the neglected (patients) or subliminal (controls) field. That is, performance would be both goal driven by the proverbs (top-down) and stimulus driven by implicit processing of the target material in the picture (bottom-up).
Acknowledgements We are grateful to Dr Stephen Darling for assistance with the collection of data for the young control participants in Expt 2. The study was funded by grant number CZB/4/346 from the Chief Scientist Office (CSO) of the Scottish Government to Della Sala and Logie, for which Dr Stephen Darling and Dr Patricia Bestelmeyer were research fellows.
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