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REPORT
1Cognition and Action Group, Department of Neurology and 2Department of Psychiatry, National University of Athens, Eginition Hospital, Athens, Greece; 3Department of Cognitive Sciences, Università Vita e Salute San Raffaele, Milano, Italy; and 4Department of Radiology, Washington University School of Medicine, St. Louis, Missouri
Submitted 17 September 2004; accepted in final form 22 December 2004
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ABSTRACT |
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INTRODUCTION |
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, 1996, 2003). This supervisory system is viewed as a bottleneck for information processing that regulates the flow and content of information.
Although the capacity of visual working memory is limited (Luck and Vogel 1997), behavioral data on change-detection tasks suggested that several features can be simultaneously retained in separate, capacity-limited stores among which there is little or no competition (Wheeler and Treisman 2002). Furthermore, the processing of multiple as compared with processing of a single feature imposes no additional cost on feature-specific capacity when these features can be integrated into objects (Luck and Vogel 1997; Wheeler and Treisman 2002).
Lesion, neurophysiological, and neuroimaging studies suggest that anatomically distinct neural systems process different object features in working memory (Goldman-Rakic et al. 2000), indicating a structural correlate of the functional independence of feature processing. It is also known that neurons in cortical areas such as parietal (Chafee and Goldman-Rakic 1998; Gnad and Andersen 1988), motor (Carpenter et al. 1999; Smyrnis et al. 1992), premotor (Carpenter et al. 1998), and prefrontal areas (Chafee and Goldman-Rakic 1998; Funahashi et al. 1989) show sustained neural activity during memory delays preceding a movement.
However, it is still not known whether neural systems supporting working memory are also endowed with separate components for the storage and retrieval of spatial and serial order information, 2 basic features that need to be computed so that complex motor acts can be carried out. We hypothesized that in such tasks serial order and spatial information would be processed hierarchically, rather than in parallel, because spatial direction is a property of single elements of a sequence, whereas serial order is a property of the temporal relations between the elements in the sequence set.
We previously studied how accurately subjects move to the remembered direction of a visual target cued on the basis of its serial order within a sequence of visually presented targets (Theleritis et al. 2004) using a version of the motor memory scanning task first studied by Georgopoulos and Lurito (1991). We found that the accuracy of the recalled serial order and direction decreased with increasing number of targets. In this study, we investigate how accuracy and response latency of a movement to a remembered target depend on the number of features (serial order and direction) and the number of targets (memory load) in a sequence.
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METHODS |
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Eleven right-handed healthy volunteers (3 women, 8 men) participated in the study. The mean age was 36.8 yr (range 25–54 yr). Participants gave informed consent, the experimental protocol having been approved by the Eginition Hospital Human Studies Committee.
Apparatus
The experimental apparatus was previously described in detail (Theleritis et al. 2004). Subjects sat in a darkened room and faced a computer monitor (17 in.; Hitachi CM630ET) placed at a distance of 60 cm from their eyes. Subjects held, with the right hand, a pencil-type manipulandum on a horizontal digitizing tablet (Calcomp Inc. 2000) placed in front of them. The manipulandum's position was sampled at 100 Hz and its position displayed on the monitor as a 2.5-mm-diameter round white cursor. The ratio of manipulandum to cursor movement was 1.
Procedure
In the Spatial Task (Fig. 1A) each trial began when the subject moved the cursor into a 10-mm-diameter red circle displayed at the center of the monitor. A sequence of 2, 3, or 4 targets (5-mm-diameter white filled disks) was presented at pseudorandomly chosen locations placed along a 10-cm-radius circumference. There were 16 possible target locations, regularly spaced at 22.5° intervals. Each target was presented for 1 s and was extinguished at the appearance of the following target. After all the targets had been presented, a delay of 2 s followed and then one of the target positions was highlighted for 300 ms (probe). As soon as possible the subject moved to the target whose location was nearest to the probe and maintained the position until the end of a 3-s period (Response period).
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In the Conjunction Task (Fig. 1C) target presentation proceeded exactly as for the location task. After the retention period one of the targets was presented again (probe) and the subjects had to move to the recalled location of the target following in the sequence.
Each subject performed 3 separate blocks of 64 trials for each task. In each block a sequence of 2, 3, and 4 targets was presented (a total of 64 x 3 x 3 = 576 trials). The order of task and subsequent block presentation was randomized from subject to subject.
The instantaneous velocity of the manipulandum was computed by numerically differentiating the position data. This trace was used to estimate the movement onset and the end of the movement. The response latency (RL) was the time in milliseconds from the appearance of the probe target to movement onset (Fig. 1D). The position of the cursor was expressed in a polar coordinate system (direction and amplitude) with the origin at the center target (Fig. 2).
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Because there is a single performance measure, i.e., the angular difference between the target direction and the movement endpoint direction (Fig. 2) and because this difference could be attributable to either an error in recollecting the serial order of the target (in the serial order and conjunction task) or its direction (in the spatial and conjunction task), we used a stochastic model to estimate the uncertainty associated with the target's serial order and direction. This was done by a maximum likelihood estimation procedure. Probability distributions of the directional data were computed using a model with 2 parameters: 1) the width of a Gaussian distribution of movement directions, that is, the SD of the variable directional error (
); and 2) the probability of making a serial order error, p(Eserial). The conditional probability of a given trial's movement endpoint direction, p[DM|p(Eserial), ], is given by
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), an unconstrained search procedure.
In a first analysis the directional data for each task and each memory set size were pooled across subjects. Bootstrapped estimates of p(Eserial) and and the relative 95% confidence intervals were obtained by resampling the data 4,000 times.
In the second analysis separate estimates of p(Eserial) and were obtained for each subject and each memory set size. Estimates of p(Eserial) were arcsine transformed and analyzed using a 2-factor, repeated-measures ANOVA with independent factors the memory load and the task (serial order and conjunction tasks). A 2-factor, repeated-measures ANOVA was also performed to assess the effects on of memory load and task (spatial and conjunction tasks).
Median response latencies were estimated for each subject, task, and memory load. A 2-factor, repeated-measures ANOVA was used to ascertain the effects of load and task on response latencies.
Furthermore, the response latency in the conjunction task was modeled using the data from the spatial and serial order tasks. In the first model it was assumed that the retrieval of direction and serial order in the conjunction task proceed serially and therefore that the latency in the conjunction task would be equal to the sum of the latencies in the component tasks. The second model assumed that the retrieval of direction and serial order information proceed in parallel and that movement latency in the conjunction task depends on the time both processes are completed.
The latency for the conjunction task predicted by the serial model is
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RESULTS |
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We first consider the data on the probability of serial order errors in the serial order and the conjunction tasks. As shown in Fig. 3A the probability of serial order errors increased with memory load in both tasks [F(2,9) = 21.53, P < 0.0001], but there was no overall difference in serial order error probability between the 2 tasks [F(1,10) = 0.08, P > 0.7] and, more important, the memory load effect on serial order error probability was not different in the 2 tasks [load x task interaction, F(2,9) = 0.21, P > 0.8]. We conclude that the capacity for serial order information was the same in the serial order and the conjunction task. Interestingly, Fig. 3A suggests that subjects occasionally moved to a target different from the one also cued in the spatial task and that the probability of such errors increased with memory load [F(2,9) = 13.3, P < 0.03]. There are at least 2 possible explanations for these errors: either subjects used the wrong strategy in choosing the target, such as basing their choice on the serial order of the cue and target, or the spatial location of target was retained inaccurately. To distinguish between these alternative interpretations, we analyzed the directional error for trials with a memory load of 4 targets in which the probability that the subjects had moved to a wrong target was greater than the probability that they had moved to the correct one. The SD of the directional difference between the movement endpoint and the correct target was significantly smaller in the spatial task (79 deg) than in the conjunction task (114 deg) (one-tailed bootstrapped t-test, P < 0.05). This result suggests that choosing the wrong target in the spatial task was more likely to depend on inaccurate spatial information than a faulty strategy, such as using the serial order of the cue.
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In summary, the results showed that the simultaneous storage in working memory of both features in the conjunction task does not affect the capacity to store serial order and spatial information compared with the feature tasks.
Retrieval from memory
We measured response latencies in the 3 tasks to infer the time taken to retrieve serial order and spatial information from memory. Although response latencies increased with memory load overall [F(2,9) = 49.44, P < 0.0001], a significant task effect [F(2,9) = 9.01, P < 0.01] and a memory load by task interaction [F(4,7) = 8, P < 0.01] indicated that response latency and its modulation by memory load differed among tasks. Figure 3C shows pooled response latencies as a function of memory load in the 3 tasks. These data indicate that response latencies in the serial order and conjunction tasks were greater and that they increased at a faster rate with memory load than response latencies in the spatial task.
To gain better insight into the relation between retrieval times in the different tasks, we modeled the response latency in the conjunction task using the data from the 2 feature tasks. In the first model we assumed that the retrieval of serial order and spatial information take place sequentially (serial model) and therefore the retrieval time in the conjunction task is the sum of the retrieval times in the feature tasks. In the second model we assumed that the retrieval of direction and serial order information proceed simultaneously (parallel model) and therefore the retrieval time in the conjunction task is equal to the time taken by the slower of the 2 retrieval processes. Figure 3D shows the latencies predicted by the serial and parallel models and the RL in the conjunction task as a function of memory load. The latencies in the conjunction task and those predicted by the parallel model were not different [F(1,10) = 0.48, P > 0.5] nor were they affected differently by memory load [interaction F(2,9) = 2.34, P > 0.1]. In contrast the latencies predicted by the serial model were significantly greater than those found in the conjunction task [F(1,10) = 13.66, P < 0.01]. These results are not consistent with the hypothesis that serial order and directional information are retrieved sequentially, but rather indicate that spatial and serial order information retrieval proceed simultaneously and independently.
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DISCUSSION |
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) and even more (5–6 items) for spatial information (Wheeler and Treisman 2002). However, a recent study that manipulated the complexity of the memorized feature information found that the capacity of the visual component of working memory can vary from 3.2 to 7.5 items according to the feature retained: the smaller the capacity, the larger the complexity of the feature (Alvarez and Cavanagh 2004). The conclusion of that study that the effective memory load depends both on the complexity of the feature memorized and on the number of objects is consistent with our data that indicate a gradual decrease of accuracy with target number. The second finding was that the directional and serial order accuracy did not change when memorizing either feature in isolation or both features simultaneously. In addition, the response latencies in the conjunction task were consistent with a model that assumed that they were determined on each trial by the slower of the 2 retrieval processes. These results were not entirely expected. Although spatial direction is a property of each individual target, determining the serial order of a target in the sequence also implies being able to distinguish it by some means other than its serial order (i.e., its direction) from the other targets. Therefore we hypothesized that knowledge of the serial order of a target should also encompass knowledge of its distinguishing feature. Thus we predicted that in the conjunction task, when both directional and serial order information need to be jointly stored, we would observe a loss in the amount of retrieved feature information compared with the single-feature tasks. However, this prediction was not confirmed by our results.
On the contrary, our results suggest that the targets' serial order and direction information are stored in separate feature-specific, limited-capacity systems. This hypothesis, previously promoted by Wheeler and Treisman (2002) in the context of storage in working memory of simple visual features, would explain why the storage of serial order does not interact with the storage of direction information. Clearly, this account does not address how information is combined to form a single movement plan. If binding takes place after, rather than before, the appearance of the probe then one would expect that serial order information would be retrieved before selecting the appropriate direction information. This serial retrieval would yield retrieval times in the conjunction task equal to the sum of the retrieval times in the feature tasks. However, our data showed that the retrieval of both features occurs in parallel, rather than serially, in the conjunction task. Thus we must conclude, somewhat paradoxically, that serial order and spatial information are stored as bound features, but in separate stores. How this could be accomplished computationally remains unknown. Nevertheless, neural recordings in the motor cortex during a version of the motor memory-scanning task have demonstrated the existence of signals related to both independent and bound representations of serial order and spatial information during the delay period of a working memory scanning task. More specifically some neurons were found to be responsive only to serial order information, whereas others were responsive only to direction information and still others were responsive to a combination of the 2 features (Carpenter et al. 1999).
A potential confound in this study is that subjects may have used the same strategy in all 3 tasks. It should be noted that during retrieval subjects must have used different strategies. In fact, using the same strategy would have resulted in chance performance in one or more of the tasks with respect to the criteria used by us to define the target and the distractors. Second, the response latency in the serial order and conjunction tasks was significantly higher than that in the spatial task and increased linearly with memory load as shown by previous studies (Sternberg 1969), clearly indicating that subjects used different retrieval strategies in the different tasks. Third, in the spatial task the direction of the movement in trials in which the subject had probably moved to a target different from the one cued were closer to the probe location than the direction of the movements in the conjunction task (see RESULTS), thus suggesting that errors in the spatial task were attributed to faulty spatial information rather than to a faulty strategy. Whether it is possible that during the delay period subjects maintained both types of information is a thornier issue. Blocking of task conditions and randomization of the order of task presentation across subjects minimized this possibility. Furthermore, in the serial order task, where targets were continuously visible, the idea that subjects would have used working memory to store spatial information is not consistent with the finding that the internal representation of the environment relies on a short-lived, unlimited-capacity memory system (Sperling 1960). Nevertheless, we cannot definitely rule out that serial order information may have been retained in all 3 tasks, even though there would be no obvious advantage in doing so and the data indicate that this information was not used when it was task irrelevant.
In conclusion we showed that separate stores hold targets' direction and serial order information in working memory. Nonetheless, direction and serial order are probably also maintained in bound representations because there is no time cost when retrieving both features beyond that taken to retrieve each feature in isolation.
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FOOTNOTES |
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Address for reprint requests and other correspondence: N. Smyrnis, Department of Psychiatry, National University of Athens, Eginition Hospital, 74 Vas. Sofias Ave, 11528, Athens, Greece (E-mail: smyrnis{at}med.uoa.gr)
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REFERENCES |
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ABSTRACT
INTRODUCTION
