learning spatial sequences in unilateral neglect

Psychol Res (1997) 60:42-52 © Springer-Verlag 1997

Asher Cohen" Alon Wasserman. Nachum Soroker

Learning spatial sequences in unilateral neglect

Received: 7 June 1996/Accepted: 22 October 1996

Abstract Brain-damaged patients with unilateral spatial neglect ignore aspects of the world located on the side opposite their lesion. In the present study we examined the performance of unilateral neglect patients (UN) on an SRT task in which a hybrid repeating sequence (21313) was used. We analyzed the patients' performance for each location separately as a function of the target's location in the trial preceding the response. The UN patients were severely limited in their learning of the sequence when compared to normal controls. In particular, they appeared to learn unique associations (21 and 13) but not ambiguous ones (31 and 32). We discuss two possible explanations for this phenomenon. The first is that UN patients show a deficit similar to that of normal subjects in dual task situations. The second is that the learning deficit is unique to spatial processing impairments of UN patients and is not directly related to research with normal population. We outline future research that may distinguish between these two explanations.

Introduction

The neglect syndrome is caused by a neurological lesion. It is a failure of patients to orient and respond to stimuli that appear contralaterally to the side of the lesion (see Halligan and Marshall, 1993; Heilman, Watson, & Valenstein, 1993, for reviews). The present study exam- ines learning of spatial sequences by neurologically impaired patients with neglect. The goal of this study is twofold - to gain insight into the processes of sequence

A. Cohen ([])'A. Wasserman Department of Psychology, The Hebrew University, Jerusalem 91905, Israel; e-mail: [email protected]

N. Soroker Loewenstein Rehabilitation Hospital, Raanana, Israel

learning and to shed light on the nature of the processing deficits responsible for neglect.

This link between neglect patients and sequence learning may appear surprising upon first examination. Although neglect cannot be explained by peripheral perceptual damage, it is typically conceived as a deficit to some high-level perceptual-attentional systems (e.g., Marshall, Halligan, & Robertson, 1993). By contrast, sequence learning is typically categorized as a part of skill acquisition (e.g., Curran, 1995; Keele, Cohen, & Ivry, 1990; Nissen & Bullemer, 1987) and is often studied in the research on processes of motor control. One of the main contentions of the present study is that the gap between these two domains is more apparent than real (see also Curran, 1995; Keele & Curran, in press; Mayr, 1996).

There may be several links between neglect and sequence learning. One key concept that may bridge the two domains is that of attention. The role of attention in both sequence learning and the neglect deficit has been extensively debated in the literature. The pattern of sequence learning shown by neglect patients may reveal the role of attention in this learning process and at the same time provide cues to the nature of the neglect deficit itself. Second, sequence learning is typically studied in the spatial domain. Neglect patients have deficits in spatial processing. Examining the ability of these patients to learn spatial sequences may provide hints for the precise nature of their spatial deficits from a learning perspective.

Sequence learning and attention

Most research on sequence learning has used the Serial Reaction Time task (SRT) introduced by Nissen and Bullemer (1987). Typically, stimuli appear in one of three to five possible locations, each of which requires a different response. Subjects have to respond quickly and accurately to the appearance of a stimulus, and the next stimulus appears on the screen shortly after the response. In some conditions the appearance of the stimuli

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in the various locations follows a repeating sequence, while in other conditions the appearance of the stimuli is random. Learning is assessed by comparing the reaction times for random sequence and repeating sequence conditions. Nissen and Bullemer found that subjects can learn sequences after a relatively short training period.

Nissen and Bullemer (1987) examined the role of attention in this spatial learning paradigm by asking the subjects to perform an auditory tone task concurrent with the SRT task. The assumption underlying this manipulation is that the secondary task demands at least some of the subjects' attention, and consequently less attention remains available for the SRT task. Indeed, subjects in the original study of Nissen and Bullemer did not appear to learn the repeating sequence in the dual task situation. Nissen and Bullemer concluded that sequence learning requires attention.

Cohen, Ivry, and Keele (1990) examined this issue more closely. They used the same dual task methodology of Nissen and Bullemer (1987) but manipulated the type of repeating sequence in the SRT task. Three types of repeating sequences were used. The first sequence type, termed "unique," included repeating sequences in which each action in the sequence was uniquely associated with another action (e.g., action 1 was always followed by action 2). In the hybrid sequence, some actions were uniquely associated with other actions whereas some other actions were not uniquely associated with any action. In the ambiguous sequence, the type of repeating sequence used by Nissen and Bullemer, there were no unique associations between any pair of actions. Cohen et al. (1990), like Nissen and Bullemer, did not observe learning of the ambiguous sequence. Subjects did, however, show learning of the other two types of repeating sequences.

Cohen et al. (1990) suggested that learning ambiguous repeating sequences requires attention. By contrast, learning repeating sequences with unique associations may require only minimal involvement of attention. The notion is that forming associations between pairs of actions requires attention if these associations are not unique. The nature of the attentional system that is required has not been specified, and we shall return to this issue in the General discussion. Note that Cohen et al. never claimed that people learn only unique associations in dual task situations. In fact, several studies (Cohen et al., 1990; Curran & Keele, 1993; Frensch, Buchner, & Lin, 1994) showed that learning hybrid sequences in a dual task situation causes a faster response to all actions in the sequence, including those that are ambiguously predicted by the immediately prior item. These findings suggest that the learning shown in the dual task situation is not just a form of classical conditioning learning in which two actions are linked by a simple association. The claim has been that the presence of a unique association is important in learning the repeating sequences and that some form of a presumably complex associative mechanism is responsible for this learning (see also Keele & Jennings, 1992).

Subsequent research challenged some of the empirical results of Cohen et al. (1990). Several studies found that subjects can learn at least simple kinds of ambiguous sequences in the presence of a concurrent auditory task (Keele, Jennings, Jones, Caulton, & Cohen, 1995; Reed & Johnson, 1994). The theoretical claim of Cohen et al. that the interference in learning observed in the dual task situation is due to the attentional demands of the secondary task has been challenged as well. Other re- searchers suggested that the interference in learning sequences with a concurrent secondary task may have to do with factors other than attention, such as organiza- tion (Stadler, 1995), short term memory (Frensch & Miner, 1994), and interaction between the two concurrent tasks (Schmidtke & Heuer, this issue).

At present, then, there is no agreement in the literature concerning the precise effects of a secondary task on sequence learning, nor is there agreement regarding the cause of the learning interference in this dual task situation. One possible reason for this state of affairs is the inherent limitation of the dual task methodology. The potential pitfalls of such a methodology are well-known (e.g., Duncan, 1980). Subjects in these situations cannot focus on any one task exclusively but have to divide their attention in some manner between the two tasks. Di- viding attention between two tasks is at least in part a matter of strategy that can be influenced by a variety of factors. Thus, differences between experiments may be due to some subtle differences between strategies employed by the subjects in the different experiments. Most studies to date have attempted to control this problem by emphasizing to the subjects the importance of the tone task and by applying performance criteria to verify that the subjects indeed focused their attention primarily on the tone task. The criteria were sometimes rough (e.g., Cohen et al., 1990; Nissen & Bullemer, 1987) and sometimes more strict (e.g., Cnrran & Keele, 1993). Nevertheless, it is clearly not possible to fully control the strategy used by the subjects to divide their attention between the tasks.

Consequently, it is possible that subjects in the study of Reed and Johnson (1994) learned the ambiguous sequence in the presence of the secondary tone task because they did not focus their attention exclusively on the tone task. Furthermore, it is possible that even in the original experiments of Cohen et al. (1990), in which ambiguous sequences were not learned, subjects did not fully focus their attention on the auditory task. Recall that subjects in this study did learn hybrid repeating sequences including the associations between ambiguous pairs of actions within the sequence. This learning may have been due to residual attention that remained focused on the SRT task during the performance of the tone task.

One potential way to overcome this limitation is to examine neurologically impaired patients. Patients that suffer from a relatively focal lesion may sometimes suffer from a selective loss of a cognitive function. In the so- called "pure cases" patients may show a complete lack

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of a specific function. For example, a circumscribed lesion in a particular brain area may lead to complete amnesia of declarative memory (e.g., Squire, 1992). Be- cause the SRT task involves spatial sequence learning, and because of the evidence that attention may be required to learn some such sequences, we chose to test patients with unilateral visual neglect (UN). We shall first review the neglect syndrome and its possible causes.

The neglect syndrome

Neglect includes a number of phenomena, all of them characterized by the patient ignoring aspects of the world positioned on the side contralateral to the lesion. For example, sensory neglect is defined as lack of response to contralesional stimuli, whereas patients with motor neglect do not use contralesional limbs (Heilman et al., 1993). It is not entirely clear to what extent these different forms of neglect are related, as they can be dissociated (e.g., Marshall et al., 1993). In this study we shall focus on sensory neglect.

Damage to a number of different brain regions may lead to neglect, but sensory neglect appears most com- monly as a result of a lesion to the inferior parietal lobe (Vallar, 1993). Sensory neglect may be manifested si- multaneously in different modalities but can also be confined to a single modality (Soroker, Calamaro, & Myslobodsky, 1995). In the present study we are fo- cusing on patients with unilateral visual neglect (UN). There are several standard tests that are used to diag- nose visual neglect (e.g., Soroker et al., 1995). For example, patients are asked to bisect lines of various sizes. U N patients tend to bisect the lines at a point ipsilesional to the middle of the line.

The cause of U N is controversial. Part of the problem stems from the possibility, mentioned earlier, that there may be several different types of U N (Marshall et al., 1993). Early theories (e.g., Bender, 1952) suggested that sensory neglect is due to loss of low-level sensory information. However, a number of studies (e.g., Berti et al., 1992; Cohen, Ivry, Rafal, & Kohn, 1995) have shown that UN can be demonstrated in the absence of any low-level sensory deficit. It is common to divide current theories into two main camps (Marshall et al; Robertson, 1993). Attentional theories assume that U N is caused by damage to some attention systems (e.g., Posner, Walker, Friedrich, & Rafal, 1984; Riddoch & Humphreys, 1987). Representational theories assume that damage to representations of spatial information causes UN (e.g., Bisiach & Luzzatti, 1978).

For a first approximation, the difference between the two classes of theories runs along a static-dynamic continuum. Representational theories generally assume that the damage in UN patients is due to loss of representations of contralesional space. Thus, relatively stable and static representations of space that are intact in the normal population are impaired in UN patients and lead to the symptoms of sensory neglect (e.g., Bisiach &

Luzzatti, 1978). In contrast, attentional theories such as that of Posner et al. (1984) suggest that U N patients are impaired in moving their attention from its current position to more contralesional locations. The focus in these theories is on loss of dynamic on-line aspects of processing rather than on impairment of static spatial representations.

Several lines of evidence support the claim that dynamic processes are important in the manifestation of UN. For example, Riddoch & Humphreys (1983) showed that U N patients can improve in a line-bisection task if they are cued in advance to the contralesional side. Posner et al. (1984) showed that U N is particularly apparent when patients are first cued to a position in the ipsilesional field and are then required to respond to stimuli positioned in the contralesional visual field. Consequently, more recent versions of the spatial representation theories (e.g., Rizzolatti & Berti, 1993) have become more complex and include additional processes that are more dynamic in nature and allow for the fact that on-line events improve patients' performance. In a way, one can think of these additional processes as "attentional".

Because current representational theories include dynamic elements, it has become quite difficult to design studies that can support one class of theory over the other. Given this state of affairs, a more productive approach may be to further investigate the nature of the deficits in the dynamic attentional processes of UN patients. We suggest that testing U N patients on the SRT task may provide insights into this issue. Certain char- acteristics of this task may be especially important in this respect (see also Mayr, 1996). In a typical task, some of the stimuli are positioned in the left visual field and some are positioned in the right visual field. Thus, right UN patients (as in the present study) respond faster to a stimulus positioned on the right side than to a stimulus positioned on the left side.1 The task is spatial in nature, with responses based entirely on the stimulus position. Note that this is the case in both the random and the repeating sequence conditions. Learning in this task can be defined as the difference between a response to a stimulus in a particular position when it is part of a repeating sequence and a response to a stimulus in the same position as part of a random sequence. The important point for our purposes is that the spatial information of the stimuli in the two sequence conditions is identical in any given trial. Learning consists of some form of association between trials.

1Neglect is typically defined as lack of response to contralesional stimuli. Thus, strictly speaking, we may expect right neglect patients to completely ignore stimuli that appear on the left side. However, patients in the post-acute stage (as were the patients in this study) can respond to contralesional stimuli in well-defined situations such as the SRT task, where they know that a stimulus has to appear somewhere. In these situations the deficit is manifested as a much slower response to contralesional stimuli (see Cohen et al., 1995).

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Can U N patients learn the spatial sequence in an SRT task? The patients process stimuli much more efficiently in the ipsilesional field. Would that ability also affect learning associations between stimuli in different positions? It would be particularly interesting to see whether, after practice, the patients' performance in the damaged visual field would become similar to that in the intact visual field. The answer to this question may be affirmative under the assumption that knowledge of the sequence provides valid cues for the patients concerning the next position. As shown by Posner, et al. (1984), a valid cue can improve neglect patients' performance in the neglected visual field to a level similar to that of the intact visual field. On the other hand, learning of relatively permanent spatial associations may be impaired in the damaged visual field.

The experiment

that normal subjects can learn this sequence in the presence of a concurrent auditory task. A hybrid sequence also has the desired property that some of its pairs of actions are uniquely associated (21 and 13 in our sequence) and some pairs are ambiguous (31 and 32 in our sequence). As noted previously, evidence with normal subjects indicates that both types of association can be learned in the presence of a secondary task, and we wished to examine whether the same learning can be observed in U N patients.

Method

Patients

Two right-hemisphere-damaged patients with chronic unilateral neglect manifestations participated in the study. Figure 1 presents a computerized construction of their lesion. Below is a description of this lesion.

The present study examined spatial learning of the SRT task in two U N patients. Each of the patients participated in ten sessions over a period of approximately two weeks. We selected patients with chronic neglect) In addition we examined 12 normal college students on the same SRT task. The college students participated in a single session each.

There were two related goals to this study. First, testing patients may serve the same function as using a secondary task for normal subjects. One possible outcome of the distractor task with normal subjects is that it forces them to allocate attention to it, and the common assumption is that less attention would then be devoted to the SRT task. Analogously, U N patients may allocate less attention to the SRT task (in the neglected visual field) because of their deficit. In fact, patients may show more severe attentional deficits than normal subjects in a dual task situation because the latter may be able to alternate their allocation of attention efficiently between the two tasks. The assumptions underlying the analogy made here between dual task methodology and U N patients are not simple, and we shall expand on this issue in the General discussion. Second, the pattern of spatial learning displayed by U N patients in the SRT task may provide cues to the nature of this deficit.

The stimuli in our experiment appeared in three equidistant locations on the horizontal meridian. The repeating sequence we used was 21313, where 1 is the left position, 2 is the middle position, and 3 is the right position. Thus, in the usual terminology, this is a hybrid sequence of length 5. We chose a hybrid sequence because, as reviewed earlier, it has consistently been found

Patient G. M. This 56-year-old right-handed female, with four years of formal education, had an ischemic infarction in the right middle cerebral artery (MCA) territory involving the superior and middle temporal gyri, the temporo-parietal junction, the inferior parietal lobule, the sensory-motor cortex, the inferior frontal gyrus, and the posterior part of the middle frontal gyrus. The subcortical extension of the lesion reached the lateral aspect of the lentiform nucleus, sparing the internal capsule. The patient's visual fields were intact, but extinction of left-sided stimuli occurred upon bilateral simultaneous stimulation (BSS). Left hemisensory loss and hemiparesis were of moderate severity, with the distal upper limb showing the greatest deficits. Three weeks after the onset of stroke, severe left-sided neglect was evident in her activities of daily life. At that time the patient's total score in the standardized Behavioral- Inattention Test (BIT) battery for assessment of visual neglect was 31 (cut-off score for normality = 130; maximal score = 145, see Wilson, Cockburn, & Halligan, 1987). Neglect was manifested in the cancellation, copying, line-bisection and representational drawing subtests of the battery. About two months later her total BIT score was 84, showing persistence of severe unilateral neglect. G. M. was tested three years after the onset of the stroke.

Patient N. B. This 64-year-old right-handed female, with 12 years of formal education, had an ischemic infarction in right MCA territory involving the inferior parietal lobule, the inferior and middle frontal gyri, the superior temporal gyrus anteriorly, and the anterior capsular-putaminal region. The visual fields were intact, but in BSS there was extinction of left-sided stimuli. As with patient G. M., hemisensory loss and hemiparesis were of moderate severity, with the distal upper limb showing the clearest impairments. Six weeks after the onset of stroke the patient's BIT total score was 120. At that time neglect was manifested in all subtests of the battery. Although three weeks later the BIT total score was 135, N. B. continued to show classical unilateral neglect in representational-drawing tasks. Also, visual extinction was persistently elic- ited in the BSS condition. N. B. was tested a year after the onset of her stroke.

2The behavior of neglect patients in the acute stage is quite variable and can be very different on different days. Because of the multiple sessions in this experiment, we chose to test chronic neglect patients. Note that most neglect patients eventually recover and do not show systematic symptoms of neglect in the post-acute stage. It is relatively rare to find patients with chronic neglect.

Control subjects. Twelve students participated in this experiment as a partial fulfillment of their course requirements.

Apparatus and stimuli The stimuli were presented on an active matrix monochrome screen attached to a notebook computer. Responses were made by pressing one of three keys with the sec-

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Fig. l Lesion reconstructions for patients G. M. and N. B. These lesion reconstructions are the outcome of an algorithm for semiautomatic processing of images obtained from follow-up (3 months post onset) CT scans of the brain. The lesions are depicted on a set of standard templates. The templates are shown corresponding to the CT slices for the patient in whom structural damage was evi- denced. See text for description of the lesioned brain areas in each patient

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ond, third, and fourth fingers of the dominant hand. The keys were mounted on a response board interfaced with the computer. Sub- jects viewed the stimuli from a distance of approximately 60 cm. The stimuli consisted of three horizontal lines, each 7 mm long. The distance between two neighboring lines was 15 ram. The target was an J(, 5 mm high and 4 mm wide, that appeared above one of the lines.

Desert

Each session of the SRT task consisted of two practice blocks of 30 trials each, and ten experimental blocks of 100 trials each. Two types of sequence were used. In the random sequence condition the target appeared randomly above one of the three lines with the constraint that it did not appear in the same position on two consecutive trials. In the repeating sequence condition the target appeared cyclically in a five element sequence, 21313. The two practice blocks and the nineth experimental block consisted of a random sequence. The remaining experimental blocks used the repeating sequence. The target appeared in the central position on the first trial of all the blocks.

As in standard SRT tasks, learning was assessed by comparing the average reaction time (RT) for the eighth and tenth block (in which the repeating cycle was used) to the nineth random sequence block. Typically, RTs are averaged across the different locations. In the present study, however, we were interested in the learning displayed in each of the three positions. Furthermore, we also examined the response for each position as a function of the location of the target in the preceding trial. The five initial sessions for each of the patients were considered as basic training for the repeating sequence. The remaining five sessions were conducted to investigate the nature of the learning.

Because previous studies with the SRT did not analyze learning for each position separately, we also tested 12 normal college students on the same task and conducted the same analyses.

Following the eighth and tenth session, the patients performed a task known as "generate" (Nissen & Bullemer, 1987). Because this task turned out to be uninformative, however, we will not describe it any further in this paper. 3

3 The two patients did not display any knowledge of the sequence as is assessed in the generate task. The reasons for the patients' poor performance is not clear, however. It is possible, for example, that the task may have been too difficult for them. Details of the patients' performance in the generate task can be obtained from the authors upon request.

Procedure

The patients were tested in their home. During the performance of the SRT task they sat in front of the computer with the second, third, and fourth finger of their right hand on the right, middle, and left response keys. They were told to respond to the appearance of the X mark by pressing the corresponding key as fast as they could. Each block started with three warning tones, and then the target appeared above the central position. The target remained on the screen until the patient responded or (if no response was executed) for 5 s. Following the response (or the 5 s) there was an interval of 200 ms in which no target was present, and then the target appeared in its next position.

Results and discussion

The results of the normal subjects in each of the ten blocks are shown in Fig. 2. As is common in analyses of SRT tasks, the RT for all 100 trials of each block were averaged. The typical assessment of sequence learning is by comparing the average RT of block 9 (the random sequence block) with that of the two flanking repeating sequence blocks (blocks 8 and 10). Note that in this

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analysis the responses from the three different locations are combined.

In the present study we were interested in two more refined analyses. The first involves the amount of learning in each of the three locations separately. We term this analysis "the simple location analysis." The upper panel of Fig. 3 depicts, for each location, the average RT in block 9 (random), and the average RT collapsed over blocks 8 and 10 (repeating). We conducted a 2 (Sequence: repeating, random) x 3 (Location: right, middle, left) ANOVA to evaluate the findings. All the effects in this analysis were significant. The main effect of sequence, F(1, 11) = 57.8, p < .01, indicates that there was a clear learning of the sequence. The main effect of location,/7(2, 22) = 17.0,p < .01, is due to the response for location 2 being slower than those for the other locations. This finding may reflect the relative frequency of the three locations. Finally, the sequence x location interaction was significant as well, F(2, 22) = 6.9, p < .01. The interaction indicates that learning was not identical in the three locations (117 ms in location 1,145 ms in location 2, 169 ms in location 3).

Importantly, separate contrasts showed clear learning in each of the three locations. 4

The second analysis, the complex location analysis, involves learning in each location as a function of the target's location in the preceding trial. This analysis is not just a simple partitioning of the previous analysis, because it takes into consideration the target's previous location in the random sequence as well. For example, the response of the subjects in location 2 following location 3 in the repeating sequence condition (the 32- repeating-sequence condition) is compared exclusively to those trials in the random sequence condition where the target appeared in location 2 and was preceded by a target in location 3. In other words, the trials in the random sequence condition in which location 2 was preceded by location 1 (which were included in the previous analysis) are not included in this analysis. There were four conditions in this analysis: 21 (i.e., response to target in location 1 following target in location 2), 13, 31, and 32. Note that the first two are unique associations and the last two are ambiguous associations.

The results are shown in the lower panel of Fig. 3. A 2 (Sequence: random, repeating) x 4 (Location pair) ANOVA revealed that the main effect of sequence was significant, F(1, 11) = 44.2, p < .01. This effect reflects the learning observed in each of the four pairs. The main effect of location was significant as well, F(3, 33) = 9.5, p < .01. This effect is due to the different absolute RTs for the different location conditions. Interestingly, the sequence x location interaction did not approach significance, F(3, 33) = 1.2, p < 0.33, despite some differences in the learning between the four location conditions (123 ms for location 21, 152 ms for location 13, 112 ms for location 31, and 132 ms for location 32).

The results of this experiment generally fit with the extant literature. Subjects were able to learn associations of both unique and ambiguous sequences. In the present experiment, the subjects were able to learn both types of sequences equally well. 5 Frensch et al. (1994), using a different method, found that learning unique associations was easier. The precise conditions in which unique associations may be easier has not yet been determined, but it is not central for the purpose of the present study. Our main focus in this study was to compare the behavior of neglect patients to the normal population. Our main goal in this control experiment, therefore, was to

4We also examined the errors in the various conditions. Because the number of errors was small we could not analyze them statistically. In all cases the trend in the errors paralleled that of the latencies and there was no indication of a speed-accuracy tradeoff. SNote that, as is customary in the SRT literature, we based our estimate of the magnitude of learning on the absolute RT differences between the repeating and random sequence conditions. It is also possible to estimate the magnitude of learning by computing the ratio of the RTs in tile random and repeating sequence conditions. Although this latter estimate may lead to somewhat different estimates of learning (e.g., the relative learning of unique and ambiguous transitions for normal subjects), it does not change the conclusions relevant to the present study.

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demonstrate that subjects can learn both unique and ambiguous associations.

There are two potential problems with the use of the college subjects as a control. First, we examined the results of the group averaged across the individuals. It is possible that a minority of the subjects do not learn the sequence and that the patients may be similar to this minority group. However, every single subject in our group showed learning in every condition. A second potential problem concerns the age of our control group. We used young colleg e students and the patients are relatively old. Recent research by Curran (this volume), however, indicates that elderly can learn ambiguous transitions as well.

We now turn to the findings from the UN patients. To make sure that the patients had sufficient training for learning the sequence, we considered the first five sessions of each patient as training and examined their learning in the subsequent five sessions. Thus, for the remainder of this section we will focus on the learning displayed in sessions 6-10.

Figure 4 presents the simple location analysis averaged across the two patients. Note again that in this comparison there is no consideration of the target's location in the trial preceding the response. Two separate effects can be seen in this figure. First, there was a clear effect of location. The response to the right location was faster than that to the other two locations. We expected a difference between the right and left locations. We did not expect the RTs for the central location to be as slow as those for the left location. We return to this issue shortly. Second, there was a clear effect of learning. The RTs to the repeating sequence blocks were shorter. Importantly, the magnitude of learning appears to be similar in all three locations.

A 2 (Patient: G.M, N. B..) x 2 (Sequence: random, repeating) x 3 (Location: right, middle, left) mixed-design ANOVA was performed to evaluate the findings. Note that the patient factor functions as a between- subjects variable and the other two factors function as within-subject variables (to which each patient contrib-

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Fig. 4 The simple location analysis collapsed for the two neglect patients

uted five observations). The two main effects of particular interest in this analysis were significant, F(1, 8) = 40.3, p < .01 for the sequence factor, and F(2, 16) = 60.2, p < .01 for the location factor. No interaction was observed between these two factors, F(2, 16) < 1. In other words, the patients displayed similar learning in the three different locations.

Two additional effects were related to differences between the patients. First, the main effect of the patient was significant, F(1, 8) = 27.8, p < .01, reflecting the fact that patient N. B. was much slower than patient G. M. There was also a significant interaction between the patient and location factors, /:(2, 16)= 17.9, p < .01. This interaction reflects the different pattern of the two patients for the central and left locations. G. M., as is typical of neglect patients, was slowest in responding to stimuli in the left location. N. B. was slowest in responding to targets in the central location. Impor- tantly, the patient factor did not interact with the sequence factor, F(1, 8) < 1, and there was no interaction between the three factors, F (2, 16) = 1.7, p > 0.21. In other words, the learning displayed by the two patients was similar.

Because of the difference between the patients, it is of interest to evaluate the results of each patient separately. Figure 5 presents the results of the simple location analysis for each patient. The upper panel presents the findings from G. M., and the lower panel presents the results of N. B. The results of G. M. are typical of neglect patients. Her RTs were fastest for the target in the right ipsilateral location, slowest for the left contralesional location, and intermediate for the central location. The results of N. B. are different. Like patient G. M., N. B. was fastest for the target in the right location, but unlike G. M., N. B. was slower for the target in the central location than for the one in the left location. We do not know the reason for this pattern of response. A complex pattern of responses for different locations is occasionally observed with neglect patients (Werth, 1993). In addition, the target appeared less frequently in the central location. It is possible that N. B. (given that her neglect is less severe than that of G. M.) was more affected by the relative frequency of the targets. It is clear, though, that N.B. has a deficit in responding to the central and left locations in comparison with her response to the right location. More importantly for the present purposes, both patients showed similar learning patterns in all three locations.

These findings seem to suggest that learning is similar in all locations, independently of the neglect deficit. The data, however, do not take into consideration the location of the target in the trial preceding the response. Figure 6 presents the complex location analysis - that is, the RTs at each location as a function of the preceding location. As mentioned earlier, there were four conditions in this analysis: 21, 13, 31, and 32. The figure depicts, for each condition, the average RTs in the repeating sequence blocks and in the random sequence block. As can be seen in the figure, the simple learning

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pattern found in the previous figure is no longer present. Instead, it appears that learning is clearly present in the unique association conditions (21 and 13) and is much less present in the ambiguous sequence conditions (31 and 32).

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400 2-1 1-3 3-1 3-2

Location

Fig. 6 The complex location analysis collapsed for the two patients

A 2 (Patient: G. M., N. B.) × 2 (Sequence: random, repeating) × 4 (Location: 21, 13, 31, 32) ANOVA was performed. The two main effects of sequence and location were significant, sequence: F(1, 8) = 24.6, p < .01; location: F(3, 2 4 ) = 13.6, p < .01. Most importantly for the present study, and unlike the results of previous analysis, there was a significant sequence x location interaction, F(3, 24) = 7.3, p < .01. Put differently, learning was not similar in the four location conditions. To assess the nature of this interaction better we performed planned contrasts of the learning in each of the location conditions. In the two unique association conditions there was a significant difference between the repeating sequence and random sequence conditions: for 21, F(1, 8) = 17.0, p < .01; fo r 13, F(1, 8) = 7.0, p < .02. The difference between the sequence conditions did not approach significance in the two ambiguous conditions: for 32, F(1, 8) = 1.6, p > .26; for 31, F(1, 8) < 1. I t should be noted, however, that there was a trend of learning for the ambiguous pair 32 and, as we will see shortly, this trend was present with both patients. The results of this analysis suggest that descriptions of learning in neglect patients should be qualified. Whereas

5O

Table 1 Possible classifications of the four pairs of actions Location Frequency in Direction of

a cycle attention movement Gap Association

21 1 left 13 2 right 31 1 left 32 1 left

Learning magnitude

* statistically significant

half unique 258* full unique 123" full ambiguous -21 half ambiguous 90

the patients clearly appear to learn unique associations between spatial locations, they seem to learn very few if any ambiguous ones.

The patient factor in this analysis was similar to that of the simple location analysis. The main effect of patient was significant, F(1, 8) = 21.0, p < .01, reflecting the slower responses of patient N. B. In addition there was a significant patient-by-location interaction, F(3, 24) = 6.3, p < .01, due to the relative slowness revealed by patient N. B. in responding to the central location. As before, no other interaction with the patient factor approached significance, F(1, 8) < l for the patient x sequence interaction; F(3, 24) = 1.07, p > .38 for the patient × sequence x location interaction.

Because of the difference between the two patients, we shall also present the complex location analysis for each one separately. The upper panel of Fig. 7 depicts the complex location analysis for patient G. M., and the lower panel for N. B. As can be seen in the figure, although there are differences in the patients' relative speed in the different locations, the pattern of learning is fairly similar for both and is in accord with the sugges- tion that the unique associations were clearly learned, whereas much less learning was displayed for the ambiguous associations. 6

General discussion

The results of this study demonstrate that there is a clear difference between the learning pattern of a hybrid sequence in an SRT task for a normal-subjects population and for UN patients. The main difference is seen in the complex location analysis. Whereas normal subjects showed a robust learning of the association between all

6We also performed separate contrasts for the two patients to evaluate the learning in each of the four associations. These analyses should be taken with caution because their statistical power is fairly weak, given that each patient contributed only five samples. For patient G. M. there was a significant difference between the repeating and the random sequence for the pair 21, F(1, 4) = 17.5, p < .02. The difference between the repeating and random sequences for the pair 13, although in the right direction, was not significant. The difference was not significant for the two ambiguous associations, as well. For patient N. B. the difference between the repeating and the random sequence was significant for pairs 21 and 13, F(1, 4) = 16.2, p < .02, and F(1, 4) = 12.5, p < .03, respectively. The difference between the two sequence conditions was not significant for the ambiguous pairs.

pairs of actions, the U N patients displayed this learning for two of the pairs and a weak or no learning at all for the other two pairs.

What is the difference between the pairs of actions that were learned well by the U N patients and those that were learned less well? Table 1 presents four possible ways of classifying pairs of actions. One factor is frequency, the number of repetitions of the pairs within a sequence. A second factor is the direction of spatial movement from the first action to the second. A third factor is the spatial distance between the two actions of the pair ( ful l = the distance from right to left location; half = the distance from the central location to a peripheral location or vice versa). A final factor is whether the association is unique or ambiguous. These classifications were singled out because there were previous reports that they may have had a cognitive effect, at least in some situations. Only one of these classifications, the type of association, distinguish the two pairs that were learned well from those in which learning was less apparent.

One qualification, however, is in order. Although the difference between the repeating and random transitions reached significance only for the unique pairs, there was a trend toward learning one of the ambiguous pairs (32) as well. It is possible, therefore, that other factors (e.g., spatial distance) also contribute to the learning ability of the patients. More research is required to clarify this issue.

Why do U N patients have this type of learning deficit? This is the central question posed by our study. As pointed out in the introduction, the spatial demands of the SRT task are similar for the repeating sequence and the random sequence conditions. Learning consists of associations between spatial properties of two trials or more and is dynamic in nature. Thus, the deficit in learning displayed by the U N patients cannot be at- tributed to a deficit in relatively stable non-dynamic representations of space. A deficit in a stable representation of space should impair both random and repeating sequence blocks. We suggest that the learning problems are due to an impairment in the dynamic attentional processes of space.

What may this deficit be? There are at least two types of explanations for this phenomenon. First, it is possible that U N patients display similar deficits to those displayed by normal subjects in the dual task methodology. Alternatively, the learning deficit may be specific to the

51

spatial processing impairments of UN patients and is not directly related to the SRT findings obtained with normal subjects. In the remainder of the discussion we shall elaborate on these two types of explanations and suggest possible lines of research that may distinguish between them.

Both explanations are based on the classical study of Posner et al. (t984) concerning the attentional deficits of UN patients. As shown by Posner et al., UN patients can shift their attention relatively freely to both sides of space if they are cued in advance to the target location. In other words, when patients get a valid cue they do not have a deficit in shifting their attention to the cued location even if it is positioned in the neglected hemifield. Neglect patients are specifically impaired when they plan to move their attention to their normal side (the side of the lesion) and the target appears unexpectedly on the contralesional side. That is, the patients show a clear deficit when the cue points to the normal side but is invalid, and the target appears in the contralesional side. Importantly, both valid and invalid cues are defined in such situations within a span of a single trial. A repeating sequence in the SRT task can be defined as a sequence of valid cues in which the locations of the target in the preceding trials provide valid cues to the appearance of the target in the present trial.

The first explanation focuses on the observation that the nature of the valid cue in the SRT task is different for unique and for ambiguous associations. The cue for unique associations is provided exclusively by the preceding trial. By contrast, the last trial is not sufficient to provide a valid cue for an ambiguous association, and it is necessary to use two or more trials as cues. Our findings indicate that UN patients cannot take advan- tage of such a complex cue.

This explanation may also account for the findings obtained in the dual-task studies, with one added assumption. Subjects in dual-task situations do not learn as well as subjects in single task situations. In a way, the subjects in the dual-task situation have a learning "deficit." We need to assume, quite reasonably, that the learning deficit in dual task situations is less severe than that of neglect patients. Put differently, subjects may be able to use their attention in a limited fashion while performing concurrent tasks. As a result, subjects in these situations may be able to learn hybrid sequences. Furthermore, the less demanding the concurrent secondary task is (or the less strict the performance crite- rion of the secondary task is), the more learning is displayed by the subjects. This may be the reason that subjects in some studies learn ambiguous sequences in the dual task situations.

This explanation assumes that there is a relation between the type of attention deficit displayed by UN patients and the attentional load caused by performing concurrent tasks. This assumption may appear prema- ture. There is strong evidence that UN patients suffer from spatial attention deficits (e.g., Posner et al., 1984) that are anatomically localized in the posterior part of

the brain. By contrast, studies suggest that the attention system most affected by concurrent tasks is different and is localized in the anterior part of the brain (e.g., Posner, Petersen, Fox, & Raichle, 1988). Thus, it appears that the attentional system impaired in UN patients is different from that affected by concurrent tasks. However, there is clear evidence of interaction between the two attentional systems (see Posner & Petersen, 1990, for a review), and it is likely that disturbance of the anterior attentional system by a secondary task would also affect the operation of the posterior attention system.

Note that this explanation assumes that UN patients are impaired in learning all types of ambiguous transitions. Our study, however, employed a single hybrid sequence in which both ambiguous transitions involved shifting attention from an ipsilesional location to a more contralesional location (i.e., from location 3 to either location 2 or location 1). The second explanation is that UN patients are specifically impaired in these types of transitions because of their general spatial processing deficits. For example, when UN patients focus their attention on an ipsilesional location (e.g., location 3), they may not be able to shift their attention to a particular location. Put differently, when planning to shift their attention to the contralesional field, UN patients may be able to do it normally when only a single location is relevant (as in typical studies such as that of Posner et al., 1984). However, they may not be able to discriminate between two contralesional location (e.g., location 1 or location 2) for their attentional shift. According to this explanation, UN patients will not be impaired in learning ambiguous transitions in which such a discrimina- tion is not required (e.g., 21 and 23, or 12 and 13). Importantly, this explanation does not assume a general deficit in learning ambiguous transitions and therefore does not have direct implications for SRT studies with normal subjects.

The present study cannot distinguish between the two explanations because only a single hybrid sequence was used. To separate the two explanations, it is necessary to use hybrid sequences in which the nature of the ambiguous transitions is different. For example, the sequence 23131 contains ambiguous transitions from left to right (12 and 13). The first explanation predicts that UN patients will be impaired in this sequence, whereas the second explanation predicts that no deficit will be observed by UN patients in this sequence. Another strong prediction of the first explanation is that UN patients will not be able to learn ambiguous sequences (i.e., sequences in which all the associations are ambiguous) at all. The second explanation, in contrast, predicts that learning will be impaired only for the transitions 31 and 32. More research is needed to examine these predictions and differentiate between the two explanations.

Acknowledgements This article was supported by NIH grant RO1MH51400, and by a grant from the Israeli Foundations Trustees. We thank Axel Buchner, Tim Curran, Peter Frensch, and Mike Stadler for helpful comments.

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References

Bender, M. B. (1952). Disorders in perception. Springfield, IL: C. C. Thomas.

Berti, A., Allport A., Driver, J., Dieners, Z., Oxbury, J., & Oxbury, S. (1992). Levels of processing for visual stimuli in an "extin- guished" field. Neuropsychologia, 30, 403-415.

Bisiach, E., & Luzzatti, C. (1978). Unilateral neglect of representational space. Cortex, 14, 129-133.

Cohen, A., Ivry, R. I., & Keele, S. W. (1990). Attention and structure in sequence learning. Journal of Experimental Psy- chology: Learning, Memory, and Cognition, 16, 17-30.

Cohen, A., Ivry, R. B., Rafal, R. D., & Kohn, C. (1995). Activating response codes by stimuli in the neglected visual field. Neuro- psychology, 2, 165-173.

Curran, T. (1995). On the neural mechanisms of sequence learning. Psyche, 2(12), URL: http://psyche.cs.monash.edu.au/volume2- 1/psyche-95-2-12-sequence- 1-curran. html

Curran, T. (this volume). Effects of aging on implicit sequence learning: Accounting for sequence structure and explicit knowledge. Psychological Research.

Curran, T., & Keele, S. W. (1993) Attentional and nonattentional forms of sequence learning. Journal of Experimental Psycholo- gy: Learning, Memory, and Cognition, 19, 189-202.

Duncan, J. (1980). The demonstration of capacity limitation. Cognitive Psychology, 12, 75-96.

Frensch, P. A., & Miner, C. S. (1994). Effects of presentation rate and individual differences in short term memory capacity on an indirect measure of serial learning. Memory and Cognition. 22, 95-110.

Frensch, P. A., Buchner, A., & Lin, J. (1994). Implicit learning of unique and ambiguous serial transactions in the presence and absence of a distractor task. Journal of Experimental Psychol- ogy: Learning, Memory, and Cognition, 20, 567-584.

Halligan, P. W., & Marshall, J. C. (1993). The history and clinical presentation of neglect. In I. H. Robertson and J. C. Marshall (Eds.), Unilateral neglect." Clinical and experimental studies (pp. 3-25). Hove, U.K.: LEA.

Heilman, K. M., Watson, R. T., & Valenstein, E. (1993). Neglect and related disorders. In K. M. Heilman and E. Valenstein (Eds.), Clinical neuropsychology (pp. 279-336). New York: Oxford University Press.

Keele, S. W., Cohen, A. & Ivry, R. I. (1990) Motor programs: Concepts and issues. M. H. Jeannerod (Ed.), Attention and Performance XIII (pp. 3-18). New York: Evlbaum.

Keele, S. W., & Curran, T. (in press). On the modularity of sequence learning systems in humans. In E. Covey (Ed.), Neural representation of temporal patterns. New York: Plenum.

Keele, S. W., & Jennings, P. J. (1992). Attention in the representation of sequence: Experiment and theory. Human Movement Studies, 11, 125-138.

Keele, S. W., Jennings, P. J., Jones, S., Caulton, D., & Cohen, A. (1995). On the modularity of sequence representations. Journal of Motor Behavior, 27, 17-30.

Kinsbourne, M. (1993). Orientational bias model of unilateral neglect: Evidence from attentional gradients within hemispace. In I. H. Robertson and J. C. Marshall (Eds.), Unilateral neglect: Clinical and experimental studies (pp. 63-86). Hove, U.K.: LEA.

Marshall, J. C., Halligan, P. W., & Robertson, I. H. (1993). Con- temporary theories of unilateral neglect: A critical review. In I. H. Robertson, J. C. Marshall (Eds) Unilateral neglect: Clinical and experimental studies (pp. 311-329). Hove, U.K.: LEA.

Mayr, U. (1996). Spatial attention and implicit sequence learning: Evidence for independent learning of spatial nonspatial sequences. Journal of Experimental Psychology." Learning, Mem- ory, & Cognition, 22, 350-365.

Nissen, M. J., & Bullemer, P. (1987). Attentional requirements of learning: Evidence from performance measures. Cognitive Psychology, 19, 1-32.

Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25-42.

Posner, M. I., & Petersen, S. E., Fox, P. T., & Raichle, M. E. (1988). Localization of cognitive operations in the human brain. Science. 240, 1627-1631.

Posner, M. I., Walker, J. A., Friedrich, F. J., & Rafal, R. D. (1984). Effects of parietal lobe injury on covert orienting of visual attention. Journal of Neuroscience, 4, 1863-1874.

Reed, J., & Johnson, P. (1994). Assessing implicit learning with indirect tests: Determining what is learned about sequence structure. Journal of Experimental Psychology: Learning, Memory, & Cognition, 20, 585-594.

Riddoch, M. J., & Humphreys, G. W. (1983). The effect of cueing on unilateral neglect. Neuropsychologia, 21, 589-599.

Riddoch, M. J., & Humphreys, G. W. (1987). Perceptual and action systems in unilateral visual neglect. In M. Jeannerod (Ed.), Neurophysiological and Neuropsychological aspects of spatial neglect (pp. 151-181). Holland: Elsevier.

Rizzolatti, G., & Berti, A. (1993). Neural mechanisms of spatial neglect. In I. H. Robertson and J. C. Marshall (Eds.), Unilateral neglect: Clinical and experimental studies (pp. 87-105). Hove, U.K.: LEA.

Robertson, I. H. (1993). The relationship between tateralized and non-lateralized attentional deficits in unilateral neglect. In I. H. Robertson and J. C. Marshall (Eds.), Unilateral neglect. Clinical and experimental studies (pp. 257-278). Hove, U.K.: LEA.

Schmidtke, V., & Heuer, H. (this volume). Task integration as a factor in secondary-task effects on sequence learning. Psycho- logical Research.

Soroker, N., Calamaro, N., & Myslobodsky, S. (1995). McGurk illusions to bilateral administration of sensory stimuli in patients with hemispatial neglect. Neuropsychologia, 33, 461-470.

Squire, L. R. (1992). Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99, 195-231.

Stadler, M. A. (1995). Role of attention in implicit learning. Journal of Experimental Psychology." Learning, Memory, & Cognition 21, 674-685.

Vallar, G. (1993). The anatomical basis of spatial hemineglect in humans. In I. H. Robertson and J. C. Marshall (Eds.), Uni- lateral neglect: Clinical and experimental studies (pp. 27-59). Hove, U.K.: LEA.

Werth, R. (1993). Shifts and omissions in spatial reference in unilateral neglect. In I. H. Robertson and J. C. Marshall (Eds.), Unilateral neglect: Clinical and experimental studies (pp. 211- 231). Hove, U.K.: LEA.

Wilson, B., Cockburn, J., & Halligan, P. (1987). Development of a behavioral test of visual-spatial neglect. Arch. Phys. Med. Re- hab., 68, 98-102.

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