Working memory (WM), the ability to briefly retain and manipulateinformation in mind, is central to intelligent behavior. Here we takeadvantage of the high temporal resolution of electrophysiologicalmeasures to obtain a millisecond timescale view of the activityinduced in distributed cortical networks by tasks that imposesignificant WM demands. We examined how these networks areaffected by the type and amount of information to be remembered,and by the amount of task practice. Evoked potentials (EPs)were obtained from eight subjects performing spatial and verbalversions of a visual n-back WM task (n = 1, 2, 3) on each of threetesting days. In well-trained subjects, WM tasks elicited transientresponses reflecting different subcomponents of task processing,including transient (lasting 0.02–0.3 s) task-sensitive and load-sensitive EPs, as well as sustained responses (lasting 1–1.5 s),including the prestimulus Contingent Negative Variation (CNV), andpost-stimulus frontal and parietal Slow Waves. The transientresponses, with the exception of the P300, differed between theverbal and spatial task versions, and between trials with differentresponse requirements. The P300 and the Slow Waves were notaffected by task version but were affected by increased WM load.These results suggest that WM emerges from the formation of adynamic cortical network linking task-specific processes withnon-specific, capacity-limited, higher-order attentional processes.Practice effects on the EPs suggested that practice led to thedevelopment of a more effective cognitive strategy for dealing withlower-order aspects of task processing, but did not diminishdemands made on higher order processes. Thus a simple WM task isshown to be composed of numerous elementary subsecond neuralprocesses whose characteristics vary with type and amount ofinformation being remembered, and amount of practice.
IntroductionWorking memory (WM) refers to the limited, attention-
demanding capacity to hold and manipulate information in mind
for several seconds in the context of cognitive activity (Baddeley
and Hitch, 1974). This faculty is intimately involved in language
comprehension, reasoning and learning (Baddeley, 1992), and it
appears to be a central component of intelligent behavior in
general (cf. Kyllonen and Christal, 1990). Once thought of as a
single, unitary system, WM has come to be regarded as a
multicomponent process. Based on behavioral and lesion data,
Baddeley and Hitch (1974) proposed a trivariate model of WM,
in which WM is composed of a central executive and two
distinct storage buffers: the visuospatial sketch pad and the
articulatory loop. Others, however, have argued for a less
structured view of WM. For example, Just and Carpenter (1987,
1992) describe WM as a limited pool of nonspecific neural
activation that is necessary for task-related manipulation of
information and for the maintenance of that information in an
accessible state. Alternatively, Schneider and Detweiler (1988)
picture WM as a shifting coalition of interacting but
independent process- specific subsystems.
Much progress has been made in the past two decades in
characterizing the neural substrate of WM. Evidence from
human lesions studies has suggested that WM depends on the
activity of a number of cortical regions, primarily the prefrontal
cortex (Petrides and Milner, 1982; Frisk and Milner, 1990; Owen
et al., 1996). Neuroimaging studies have also shown that the
prefrontal cortex, as well as other areas of association cortex, are
active during WM tasks (Jonides et al., 1993; Paulesu et al., 1993;
McCarthy et al., 1994; Smith et al., 1995; Courtney et al., 1996;
Owen et al., 1996; Smith et al., 1996; Braver et al., 1997; Cohen
et al., 1997; Jonides et al., 1997; Manoach et al., 1997; Courtney
et al., 1998). These studies demonstrate that WM relies on
distributed activity in a number of cortical areas. However, the
relatively poor temporal resolution of neuroimaging methods
makes it difficult to track the time course of activation in dif-
ferent cortical areas as attention is allocated to each successive
stage of task processing.
This information can be provided by the high temporal
resolution of electrophysiological measures. In nonhuman
primates, invasive electrophysiological recordings have shown
that the neural representation of information retained over short
delays is associated with transient activation of neurons in
widespread association areas. This neuronal activation is
sensitive to momentary within-task demands, and is modulated
by the allocation of attention to different stimulus attributes and
task requirements (Fuster and Jervey, 1981; Fuster and Jervey,
1982; Miyashita and Chang, 1988; Funahashi et al., 1989; Koch
and Fuster, 1989; Chelazzi et al., 1993; Wilson et al., 1993; Miller
and Desimone, 1994; Vaadia et al., 1995; Rao et al., 1997). These
data are consistent with the notion that WM emerges when
distributed activity is recruited into a functional network by the
effortful attention required to meet task demands (cf. Gevins et
al., 1983; Crick, 1984; Gevins et al., 1987; Schneider and
Detweiler, 1988; Bressler et al., 1993; Gevins and Cutillo, 1993;
Kimberg and Farah, 1993).
In humans, noninvasive electrophysiological measures have
been used to track the subsecond timecourse and distribution of
WM processes in a variety of paradigms (e.g. Starr and Barrett,
1987; Gevins et al., 1990; Ruchkin et al., 1990, 1992, 1995; Lang
et al., 1992; Gevins and Cutillo, 1993; Raney, 1993; King and
Kutas, 1995). In a recent study, Gevins et al. (1996) compared
the evoked potentials (EPs) elicited in tasks that imposed a high
WM demand with those elicited in tasks that had the same
stimulus and response requirements, but that placed minimal
demands on WM. Both verbal and spatial versions of the WM task
were associated with subsecond changes in electrical signals
over frontal and parietal cortex. Although there were some
differences in the EPs between the spatial and verbal versions,
the similarity in both waveshape and topography between the
EPs elicited by the two task versions was even more notable. This
suggested that WM is a function of a distributed system with
Cerebral Cortex Oct/Nov 1998;8:563–574; 1047–3211/98/$4.00
Dynamic Cortical Networks of Verbal andSpatial Working Memory: Effects ofMemory Load and Task Practice
Linda K. McEvoy, Michael E. Smith and Alan Gevins
EEG Systems Laboratory and SAM Technology, 101 Spear
Street, Suite 204, San Francisco, CA 94105, USA
both task-specific and task-independent components, and led to
the suggestion that the functional networks that arise during the
performance of specific WM tasks interact with a system which
may be common to all attention demanding tasks.
The current study aims to replicate and extend these findings
in two ways. The first goal of this study is to further investigate
the subsecond dynamics of WM networks by incrementally
increasing WM load in verbal and spatial versions of a WM task.
Task-specific increases in activation with increased WM load
could indicate that an area is involved in maintaining internal
representations of the task relevant stimulus features. Non-
specific increases in activation with increased WM load would
be expected from areas involved more with the higher order
attentional demands of the task than with task-specific
processing.
A second purpose of this study is to investigate the effects of
practice on the dynamic networks underlying WM. If WM is a
complex process, some of the subsecond neural processes of a
WM task should change with practice while others remain
constant. In related studies (Gevins et al., 1997; Smith et al.,
1998), we have found that the ongoing EEG is sensitive to
practice effects in WM tasks. For example, practice resulted in a
relative increase in activation of right parietal areas in spatial
tasks and a relative decrease in activation of these areas in verbal
tasks, indicating the formation of task-specific neurocognitive
strategies. Practice also resulted in increased power of the
frontal midline theta component, which was interpreted as
ref lecting increased activation of the anterior cingulate, an
important node in the anterior attentional network.
The presence of practice effects in the ongoing EEG suggests
that practice is also likely to affect the EPs. EPs and ongoing EEG
ref lect different, but related aspects of neurophysiological
function. The ongoing EEG ref lects the state of functional
networks underlying task performance (cf. Lopes da Silva,
1991), whereas EPs index specific operations being performed
on internal representations and provide a more temporally
fine-grained view of cortical function. Thus, while the task- and
practice-related effects show that the EEG is sensitive to both
changes in attentional state and to the consolidation of
task-specific skills, changes in the EPs could demonstrate which
of the many subprocesses involved in task performance change
as a function of practice. Therefore, in addition to examining
how load and content manipulations affect the functional neural
networks involved with WM task performance, this study also
seeks to characterize the changes in such networks that occur
with task practice.
Materials and Methods
Subjects
Eight healthy young adults (22–28 years, mean age 24 years; three
women) participated as subjects. All participation was fully informed and
voluntary. Subjects received an honorarium at the end of the experiment,
a portion of which depended on the accuracy of their task performance.
Cognitive Tasks
Subjects performed a continuous matching task that required them to
indicate whether the current stimulus matched that presented on a
previous trial. Full details of the task can be found in Gevins et al. (1996).
Brief ly, task stimuli consisted of single capital letters, drawn randomly
from a set of 12. At the beginning of each trial, a warning cue appeared in
the center of the screen for 0.2 s. The stimulus occurred 1.3 s after the
onset of the warning cue in one of 12 possible locations. Stimuli were
presented for 0.2 s once every 4.5 s. The identity of the letter and its
spatial position varied randomly from trial to trial. A small fixation dot was
continuously present at the center of the screen.
Subjects performed two versions of the task at each of three difficulty
levels. In a verbal version, subjects were required to remember the
identity of the visual stimulus presented; in a spatial version, they were
required to remember its position on the screen (see Fig. 1). In the low
load (LL) difficulty level, subjects were required to compare the current
stimulus with that presented on the previous trial and to respond by
pressing a microswitch with their right index finger if the current
stimulus matched that presented on the previous trial (i.e. if, in the verbal
version, it was the same letter as that presented on the previous trial
regardless of its position on the screen, or, in the spatial version, if it
occurred in the same position as on the previous trial, regardless of what
the letter was). A ‘non-match’ decision was indicated by a right middle
finger response. In the moderate load (ML) difficulty level, subjects were
required to compare the current stimulus with that presented two trials
ago, and in the high load (HL) difficulty level, to compare the current
stimulus with that presented three trials ago. Match stimuli occurred
randomly on 50% of the trials. Since trials were 4.5 s long, subjects were
required to remember the identity or location of each stimulus, as well as
its sequential order, for 9 s in the ML level and for 13.5 s in the HL level.
Subjects participated in three sessions, each spanning a 6–8 h period.
The first two sessions occurred on two consecutive days. Subjects then
had one day off before the final session. On the first day, subjects began
by performing one block (23 trials) of each of the six task conditions in
order of increasing difficulty. Subjects then performed seven blocks of
each condition. Task conditions were presented in groups of six, with
each condition occurring once within the group. Condition order within
each group was randomized to eliminate any order effects. Subjects were
given a lunch break and rest periods as needed. During the second and
third sessions, subjects performed eight blocks of 23 trials of each task
condition. The six test conditions were presented randomly within each
block. The first block on each day served as warm-up exercises and was
omitted from further analyses.
To maintain motivation, subjects were rewarded 5 cents for each
correctly detected ‘match’ stimulus, and lost 10 cents for each incorrect
match response. Subjects were instructed to respond as quickly and
accurately as possible.
Recordings
EEG was recorded continuously from 27 scalp locations (Fp1, Fp2, AF3,
AF4, FT9, F7, F3, FZ, F4, F8, FT10, T7, C3, CZ, C4, T8, P9, P7, P3, PZ, P4,
P8, P10, O1, OZ, O2, Iz) during task performance, using electrically
linked mastoids as reference. Electrooculographic (EOG) activity was
recorded from electrodes located in the center of the supraorbital ridge
Figure 1. Spatial and verbal versions of the high load (HL) level of the WM task. Inseparate blocks subjects were required to compare either the location (Spatial task) orthe identity (Verbal task) of the current stimulus with that presented one (low load, LL),two (medium load, ML) or three trials ago (high load, HL). Match decisions (50%) wereindicated by pressing a switch with the middle finger of the right hand; nonmatchdecisions were indicated by pressing a switch with the index finger of the right hand.
564 Evoked Potentials and Working Memory • McEvoy et al.
above each eye, referenced to an electrode at the outer canthus of each
eye. Physiological signals were band-pass filtered at 0.01–100 Hz and
sampled at 256 Hz. Automated artifact detection was followed by
application of adaptive eye movement artifact decontamination filters (cf.
Du et al., 1994). The data were then visually inspected and segments
containing possible residual artifacts were eliminated from subsequent
analyses. In one subject, excessive frontal low-frequency artifact
necessitated high-pass filtering the data at 2 Hz. The data from this subject
were excluded from all analyses involving EP components with
significant low-frequency contributions.
Analysis
After artifact removal, data from trials with correct responses were
averaged into 12 separate categories based on Task Version (Spatial and
Verbal), Load Level (LL, ML, HL), and Stimulus Type (Match or Nonmatch
stimuli). EPs were calculated over the period 1.7 s prior to the onset of the
stimulus (0.4 s prior to the warning cue) to 2.0 s after stimulus onset.
Amplitude measurements were made relative to the average value in the
pre-cue interval. To isolate components of interest, the EPs were digitally
filtered with a zero phase-shift digital filter. Low-frequency EPs were
examined after low-pass filtering the data at 7 Hz. To measure the
post-stimulus transient EPs, the data were digitally filtered with a
band-pass from 2 to 20 Hz to attenuate overlapping low-frequency activity
and higher-frequency muscle noise. An exception to this was the parietal
P300 response, which has significant energy in the low-frequency band.
Prior to measuring this component, the data were band-pass filtered from
0.5 to 20 Hz.
EP component overlap was further minimized by spatially enhancing
the data. After temporal filtering, a nearest-neighbor, planar current
source density derivation (CSD) was computed using realistic head-shape
information based on the measured electrode positions and an optimal,
least-squares estimate of the CSD operator using 5–10 surrounding
electrodes (Le et al., 1994). The CSD reduces the high degree of spatial
overlap of the EPs that would otherwise be observed in the scalp data,
and removes the effect of the reference electrode. Thus, the CSD
produces a waveform topography that emphasizes local changes in EP
amplitude and is relatively insensitive to contributions from remote
generators. Peripheral sites for which the CSD cannot be accurately
calculated were eliminated from analysis.
Statistical analyses were performed using repeated measures analyses
of variance (ANOVAs), with Greenhouse–Geisser corrections for
violations of the assumption of sphericity. Prior to statistical analyses, data
were standardized within subjects by converting the data to z-scores
across all conditions. When significant effects were observed as a
function of electrode site, the data were standardized separately at each
site to remove the possibly confounding effects of overall amplitude
difference between sites (cf. McCarthy and Wood, 1985).
To differentiate brain areas specifically involved in WM tasks from
those activated by novel or difficult tasks in general, it is important to
examine the EPs in subjects who have practiced the tasks to the level that
behavioral variables have stabilized (cf. Gevins et al., 1997). Therefore,
the effects of type of information held in WM, verbal or spatial, and the
effect of increasing WM load were examined in EPs obtained in the third
session, after subjects had practiced the tasks sufficiently that the
behavioral responses had stabilized. To examine the effects of practice on
the EPs, data recorded in the first and third session were compared. Since
the behavioral data showed that the greatest practice-related changes
occurred in the HL level, analysis of the practice effects was restricted to
this subset of the data.
Results
Effect of Task Type and WM Load on Behavioral and
Electrophysiological Measures
Behavior
Behavioral performance in the third session systematically
differed between the three WM load levels but not between the
two task versions (Table 1). Separate Task Version (Verbal,
Spatial) by Load Level (LL, ML, HL) repeated-measures ANOVAs
were performed on accuracy (assessed using d ′ scores) and
reaction time (RT) measures. No effects of Task Version for
either RT or accuracy were obtained, indicating that the spatial
and verbal versions of the task were well matched for difficulty.
There were highly significant effects of Load for both accuracy
[F(2,14) = 23.27; P < 0.001] and RT [F(2,14) = 12.78; P < 0.001].
Accuracy decreased and RT increased with increasing load level.
Neither accuracy nor RT differed across the seven test blocks
within the session, indicating that the asymptotic level of
performance achieved during the two prior sessions was
maintained throughout this session.
To determine whether selectively rewarding correct match
responses resulted in a response bias, we examined β values in
each of the three load levels. β values ranged from 2.0 (±1.2) in
the HL level to 2.5 (±3.0) in the LL level, suggesting a small
tendency towards a conservative response bias (i.e. subjects
were less likely to make false ‘match’ responses). However, βvalues did not significantly differ from 1.0 (indicating no
significant response bias) at any load level.
Electrophysiology
Figure 2 shows CSD EPs, averaged across subjects, from a subset
of the channels for each of the three load levels in the verbal and
spatial WM tasks. Both tasks elicited a series of topographically
distinct responses beginning with the EP peaks over parieto-
occipital regions elicited by the visual warning cue. This was
followed by the low-frequency contingent negative variation
(CNV) over the central midline region associated with
anticipation of the stimulus. The onset of the stimulus elicited a
series of EP peaks over parietal, central and frontal regions,
labeled P250, P280, P300 and P390 on the figure. (EP def lections
are commonly named according to their polarity and latency.
This convention is followed here, where current emerging from
the scalp is represented as positive polarity, and current entering
the scalp is represented as negative polarity.) Sustained
responses (‘Slow Waves’), lasting several hundred milliseconds,
were elicited over the midline central region in the prestimulus
period (the CNV), and over the left frontal (frontal slow wave,
FSW) and right parietal (parietal slow wave, PSW) regions in the
post-stimulus period. The sustained responses showed long-
lasting amplitude differences as a function of WM load. Some of
the transient responses (e.g. P250, P300) were also affected by
WM load.
Figure 2 shows that the EP waveforms and topography in the
two tasks are very similar. There are, however, some task-
specific effects. For example, a central positive-negative series of
peaks in the interval between ∼200 and ∼450 ms (which is
largest at Cz but can also be seen at Fz) is more prominent in the
spatial than the verbal task. In contrast, a peak occurring at ∼390
Table 1Average accuracy (d ′) and reaction time scores in the low (LL), moderate (ML) and high (HL)working memory load conditions for the Verbal and Spatial tasks. Both accuracy and reaction timesignificantly differed as a function of working memory load, but not as a function of task type
Accuracy (d′) Reaction time (ms)
Verbal Spatial Verbal Spatial
LL 4.12 4.10 589 559ML 3.97 3.96 733 674HL 3.06 3.15 796 781
Cerebral Cortex Oct/Nov 1998, V 8 N 7 565
ms is larger in the verbal task than in the spatial task (this effect
is less visible in Fig. 2 due to the overlapping low-frequency
activity, but see Fig. 3). A Slow Wave difference between verbal
and spatial tasks is apparent in Figure 2 at electrode site C3;
however, this difference was not significant. Since this
waveform does not show any significant effects of task or load
(F‘s < 1), it will not be considered further. The Slow Waves and
EP peaks that were significantly affected by the task and/or load
manipulations will be discussed in turn.
Slow Waves
CNV. Following the warning cue, a CNV developed over the
midline central region reaching maximum amplitude at stimulus
onset. Associated def lections were also observed over left (F3),
central (Fz) and, with opposite polarity, right (F4) frontal areas
(Fig. 2). The amplitude of this response was measured at
electrode site Cz, where the response was largest. The CNV was
measured in a 100 ms band, beginning 100 ms prior to stimulus
onset. CNV amplitude decreased as load level increased
[F(2,12) = 17.45; P < 0.001; Fig. 5]. It was also significantly larger
in the verbal task than in the spatial task [F(1,6) = 9.7; P < 0.05;
Fig. 4]. The Task Version by Load Level interaction was not sig-
nificant (F < 1).
Frontal Slow Wave. Responses over the left frontal region
(electrode site F3) differentiated between load level from ∼800
ms prior to stimulus onset until ~1300 ms post-stimulus (Fig. 2).
This sustained activity appears to ref lect at least two spatially
overlapping components. Based on the similarity in waveshape
and task effects, the prestimulus negativity is likely associated
with the CNV. Following the overlapping transient response at
∼400 ms, a slow positive wave emerged in the higher load
conditions and lasted until ∼1300 ms. The amplitude of this
positive slow wave (called the Frontal Slow Wave or FSW) was
measured in subject-specific 100 ms bands at electrode site F3.
The center latency of these bands ranged from 650 to 950 ms,
with an average center latency of 760 ms. The FSW increased
significantly with increasing WM load [F(2,12) = 5.5; P < 0.05;
Fig. 5] but did not differ as a function of Task Version [F(1,6) =
1.88; P > 0.05; average amplitude of –0.08 (±0.17) versus –0.01
(±0.18) µV/cm2 in Verbal and Spatial tasks respectively].
Parietal Slow Wave (PSW). A low-frequency negative wave
emerged over the right parieto-temporo-occipital (PTO) region,
at electrode site P8, beginning at ∼400 ms post-stimulus and
lasting until ∼1400 ms post-stimulus (Fig. 2). This response was
also measured in subject-specific 100 ms bands, at electrode site
P8. The center latency of these bands ranged from 850 to 1150
ms, with an average center latency of 950 ms. The PSW showed
a significant increase in amplitude as load level increased
[F(2,12) = 7.2; P < 0.02; Fig. 5] but did not differ as a function of
Task Version [F(1,6) = 1.2; P > .05; average amplitude of –0.05
(±1.0) versus –0.03 (±0.09) µV/cm2 in Verbal and Spatial tasks
respectively].
EP Peaks
PTO P280. Over the PTO regions, at electrode sites P7 and P8,
a positive def lection with an average latency of ∼280 ms discrim-
inated between verbal and spatial tasks. This response was
significantly larger over the right hemisphere than over the left
Figure 2. Spatiotemporal distribution of CSD EPs in the three load levels of the verbal (left) and spatial (right) WM task. Grand mean EPs over subjects are shown for the epochextending 0.4 s prior to the warning cue to 2.0 s after stimulus onset. The stimulus occurred at time 0. Data are averaged across match and nonmatch stimulus types. A similar patternof EP peaks and Slow Waves were elicited in both tasks. Three Slow Waves (FSW, CNV and PSW) varied as a function of load, as did the P300 response. The EP peaks, including theP280, the P250 and the frontal P390 differed between spatial and verbal task versions.
566 Evoked Potentials and Working Memory • McEvoy et al.
[F(1,7) = 7.43; P < 0.05], and was significantly larger in the verbal
than in the spatial task [F(1,7) = 14.41; P < .01; Fig. 4]. The
significant Hemisphere by Task version interaction [F(1,7) = 7.0;
P < 0.05] indicated that the amplitude difference between the
verbal and spatial tasks was significant over the right hemisphere
only. A significant Task Version by Stimulus Type interaction
[F(1,7) = 22.01; P < 0.01] indicated that for the verbal task,
responses to Nonmatch stimuli were significantly larger than
those to Match stimuli, whereas for the spatial task, responses to
Match and Nonmatch stimuli did not differ (Fig. 3).
Central P250. A biphasic response developed over the
midline central region with a positive def lection occurring at
∼250 ms, and a negative def lection at ~400 ms (Fig. 2). Both
aspects of this response showed the same topography and were
affected in the same way by the experimental manipulations.
Therefore, for simplicity, this complex of responses will be
referred to simply as the P250. The P250 was larger in the spatial
than in the verbal task [F(1,7) = 13.44; P < 0.01; Figs 3 and 4] and
larger to Nonmatch than to Match stimuli [F(1,7) = 13.74; P <
0.01; Fig. 6]. The Stimulus effect interacted with Task Version
[F(1,7) = 45.5; P < 0.001], in that the difference between Match
and Nonmatch responses was significant in the spatial task only
(Fig. 3). The Load Level by Stimulus Type interaction [F(2,14) =
4.82; P < 0.05] showed that responses to Nonmatch stimuli only
were affected by load level: response amplitude decreased as
load level increased.
Parietal P300. The WM tasks elicited a broad positive parietal
complex, or P300 response, between 300 and 500ms. This
response was measured in a 100 ms band centered at the
response peak (353 ms, on average) at electrode sites P3 and P4.
The P300 was significantly larger over right parietal cortex
(electrode site P4) than over the left (electrode site P3) [F(1,6) =
10.18; P < 0.02]. Response amplitude did not differ as a function
of Task Version, but was significantly attenuated by increased
WM load [F(2,12) = 10.25; P < 0.01; Fig. 5]. The Hemisphere by
Stimulus Type interaction was significant [F(1,6) = 9.12; P <
0.05], with larger responses to Match stimuli than to Nonmatch
stimuli over the left hemisphere (P3; Figs 3 and 6).
Frontal P390. A bilateral transient response over the frontal
regions was superposed on the low-frequency activity at these
sites. After filtering out the overlapping low frequency response
with a band-pass filter of 2–20 Hz, this response was larger over
the left hemisphere than over the right, and peaked at ~390 ms.
The P390 was significantly later in the verbal task than in the
spatial task [by an average of 18 ms; F(1,7) = 9.29; P < 0.02]. It
was also significantly later to Nonmatch than to Match stimuli
[by an average of 8 ms, F(1,7) = 9.4; P < 0.02]. The P390 was
significantly larger over the left hemisphere than over the right
[F(1,7) = 11.88; P < 0.02], and significantly larger in the verbal
than in the spatial tasks [F(1,7) = 11.31; P < 0.02; Fig. 4]. There
was a significant Hemisphere by Stimulus Type interaction
[F(1,7) = 12.82; P < 0.01]: over the left hemisphere, responses
were significantly larger to Nonmatch than to Match stimuli (Fig.
3); over the right hemisphere, responses to Nonmatch and
Match stimuli did not differ.
Summary: Well-practiced Tasks
In summary, the analysis of the EP data obtained after subjects
had extensively practiced the tasks showed that WM tasks
elicited both sustained Slow Waves and more transient EP peaks
over widespread cortical areas. Figures 4–6 summarize the
effects of Task Version, WM Load and Stimulus Type on these
responses. Since the functional implications of the task effects
on these potentials can be further understood by considering the
effects of practice, we will defer discussion of the task correlates
of these findings until we have considered the effects of task
practice.
Practice Effects on Behavioral and Electrophysiological
Responses in Difficult Verbal and Spatial WM Tasks
The analysis of practice effects focuses on the EPs in the HL
Spatial and Verbal WM tasks since the behavioral data indicated
that performance in this load level changed most dramatically as
a function of practice. Thus, EPs in the HL level were compared
between the first and third sessions.
Behavior
For the HL tasks, accuracy significantly increased [F(1,7) = 23; P
< 0.01] and RT significantly decreased between the first and
third sessions (F(1,7) = 11.2; P < 0.05; Table 2). Response
accuracy did not differ as a function of Task Version, but RT
showed a significant Task Version by Test Session interaction
Figure 3. Differences in CSD EPs to match and nonmatch stimuli. Data are shownaveraged across load level in the verbal (left) and spatial (right) tasks, for the channelshowing the largest effect for each component. (A) Responses to nonmatch stimuliwere larger than those to match stimuli for the P390, P250, P280 responses. Data havebeen band-pass filtered at 2–20Hz. (B) Responses to match stimuli were larger thanthose to nonmatch stimuli for the P300. Data are filtered at 0.5–20Hz.
Cerebral Cortex Oct/Nov 1998, V 8 N 7 567
[F(1,7) = 6.4; P < 0.05]: responses were significantly faster in the
Spatial task than in the Verbal task in the first session; in the third
session, there were no significant differences in RT between the
two task versions. Analysis of β values from data in the high load
level of the first session showed no significant response bias (β =
0.91 ± 0.16).
Electrophysiology
Slow Waves. The CNV increased significantly as a function of
practice [F(1,6) = 16.1; P < 0.01; Fig. 7], but did not differ as a
function of Task version. Neither the FSW nor the PSW were
significantly affected by practice [FSW: F(1,6) = 0.38; P > 0.05;
PSW: F(1,6) = 0.45, P > 0.05].
EP Peaks. The P280 over the PTO regions was not signi-
ficantly affected by task practice. The central P250 showed a
significant three-way interaction involving Task Version, Stimu-
lus Type and Practice [F(1,7) = 10.0 ; P < 0.02]. The Stimulus
Type by Task Version interaction, caused by larger responses to
Nonmatch than to Match stimuli in the Spatial task only, was
significant in the third session but not in the first. Both the
parietal P300 and the frontal P390 showed significant Practice by
Stimulus Type interactions [Parietal P300: F(1,6) = 12.7; P < 0.02;
Frontal P390: F(1,7) = 14.45; P < 0.01]. Response amplitude did
not differ as a function of Stimulus Type in the first session for
either response, but did in the third. For the parietal P300,
responses to Match stimuli were significantly larger than those to
Nonmatch stimuli, whereas for the P390 responses to Nonmatch
stimuli were significantly larger than those to Match stimuli (Fig.
7). The parietal P300 also showed a Practice by Hemisphere
interaction [F(1,6) = 11.28; P < 0.02]. Response amplitude did
not change over the left hemisphere across sessions, but
significantly increased from the first to third session over the
right hemisphere.
Figure 7 summarizes the effects of task practice on the EPs in
the WM tasks. Practice increased CNV amplitude and increased
the difference between responses to Match and Nonmatch
stimuli for the P250, P300 and P390 responses. Practice did not
have any significant effects on the frontal or parietal slow waves.
DiscussionThis study was designed to characterize the subsecond dynamics
of cortical networks involved in WM task performance. This was
accomplished by examining activity elicited while subjects
performed verbal and spatial versions of a continuous perfor-
mance WM task, each of which was expected to activate
somewhat different WM processes. An important aspect of the
experimental design is that the stimulus and response
requirements were the same for both task versions. This allows
us to attribute any differences in the EPs between the two task
versions to attentional strategy (i.e. focusing on either the verbal
or spatial attributes of the stimulus) rather than to differences in
stimulus properties. A potential drawback of this design is that
some differences between spatial and verbal WM processes may
be masked if subjects are unable to ignore the irrelevant task
attribute. While it is probable that subjects encoded both verbal
and spatial attributes of the stimuli in all task versions, it is
unlikely that subjects performed the memory comparison on
both attributes simultaneously. Both subjective reports and
task-related differences in the EPs suggest that subjects were able
to selectively focus on the relevant task attribute. The lack of any
task version by load level interactions also supports this view,
since an attempt to perform the memory comparison on both
attributes simultaneously might be expected to produce smaller
between-task differences in the low load levels, in which such a
dual-attribute comparison would be easier. Taken together, these
findings suggest that subjects were able to selectively focus on
the relevant stimulus attribute.
In addition to exploring differences between spatial and
verbal WM processes, this experiment was designed to
determine which aspects of task processing are affected by
increasing the WM demands of the task, and to determine which
aspects of task processing change as subjects become more
expert in task performance. The results showed that the verbal
and spatial versions of the WM task elicited both sustained and
transient EPs over widespread cortical areas. These responses
can be broken down into four broad categories: prestimulus
preparatory Slow Wave (CNV), task-sensitive EP peaks (P280,
P390, P250), task-insensitive EP peaks (P300), and task-
insensitive Slow Waves (FSW, PSW).
Pre-stimulus Activity: The CNV
The WM task elicited a slow negative wave, the CNV, in the
period between the warning cue and the stimulus. The
topography of the CNV, and its inverse relationship with RT and
WM load, suggests that it ref lects response preparatory
processes (cf. Rohrbaugh et al., 1976). CNV amplitude
decreased and RT increased as WM load increased. This is
consistent with the results from our prior EP study (Gevins et al.,
1996) in which CNV amplitude was significantly attenuated in
high load WM tasks as compared with control tasks with
minimal WM requirements. The CNV has long been known to
decrease in amplitude when subjects are distracted in the S1–S2
interval, either by intervening stimuli (Teece, 1972), or by the
demands of a secondary task (Teece and Hamilton, 1973). In the
WM tasks, rehearsal of the order and contents of the information
being remembered may have interfered with subjects’ ability to
focus attention on the upcoming stimulus, and thus may have
suppressed the response preparatory processes.
The practice effects on CNV amplitude are in agreement with
this interpretation. Practice served to increase CNV amplitude,
as well as to decrease RT and increase response accuracy. This
suggests that with practice, subjects become better able to
attend and prepare for the upcoming stimulus and required
Figure 4. EPs showing a main effect of task version. Grand average topographs in the verbal and spatial tasks are shown for each EP component affected by Task Version. Data areshown averaged across load level. For the prestimulus Contingent Negative Variation (CNV), responses to matching and nonmatching stimuli are averaged together. For the remainingcomponents, responses to nonmatching stimuli are shown. The CNV was larger in Verbal than Spatial tasks, as was the P280 and P390. The P250 response was larger in Spatial thanin Verbal tasks. The same scale is used for responses in the Verbal and Spatial task for each component. Scales differ across the different components. All topographs in this paperare based on values derived from the 18 electrode sites that remain after performing CSD analysis.
Figure 5. EP components showing a main effect of WM load. Data are collapsed across task version and stimulus type. Grand mean topographs in the low load and high load levelsare shown for each component affected by increased WM load. The CNV, P250 and P300 were all attenuated by increased WM load. The parietal (PSW) and frontal (FSW) SlowWaves increased as function of increased WM load. The same scale is used for the Low and High Load levels for each component. Scales differ across the different components.
568 Evoked Potentials and Working Memory • McEvoy et al.
Cerebral Cortex Oct/Nov 1998, V 8 N 7 569
response, while simultaneously maintaining the necessary
information in WM.
The CNV also showed amplitude differences between the
verbal and spatial versions of the task. It was larger in the verbal
tasks despite the lack of difference in RT or accuracy scores
between the two task versions. This difference was unexpected
and is in need of replication.
Task-sensitive EP Peaks
Three brief EP peaks were recorded which varied as a function
of task version: the P280, the P250 and the P390. The P280 and
P390 were both larger in verbal than in spatial tasks, whereas the
P250 was larger in the spatial tasks. All these responses were
sensitive to the match–nonmatch stimulus distinction, with
larger responses to nonmatching than to matching stimuli.
The P280 recorded bilaterally over the PTO region was larger
in the verbal task than in the spatial task, and was larger to
nonmatching than to matching stimuli in the verbal task only.
This response is similar in latency and topography to the ‘visual
memory potential’ described by Begleiter et al. (1993). The
visual memory potential is a right predominant response over
the PTO regions which is larger to figures that do not match
previously presented pictures than to those that do. This
potential was interpreted as ref lecting visual short-term memory
for objects (Begleiter et al., 1993). It is possible that the P280
observed in this study also ref lects activation of a visual object
short-term memory system.
The P390, recorded bilaterally over the frontal areas, but with
larger amplitude over the left hemisphere, was larger in the
verbal than in the spatial task. Over the left hemisphere, this
response was larger to nonmatching than to matching stimuli.
Practice increased this difference. The finding that the P390 was
larger in verbal than spatial tasks and larger over the left
hemisphere than the right may indicate that left frontal cortex is
more strongly engaged in verbal than in spatial WM tasks. Similar
conclusions have been drawn from functional neuroimaging
studies (e.g. Smith et al., 1996).
Functional imaging studies have indicated an important role
for the left frontal cortex in subvocal articulation (Sergent et al.,
1992; Paulesu et al., 1993; Awh et al., 1996; Fiez et al., 1996) and
in sequencing operations (Petrides and Milner, 1982; Shallice,
1982; Shimamura et al., 1990; Petrides et al., 1993). Both of
these processes are likely to be more involved in verbal than in
spatial WM rehearsal strategies. Introspective reports indicated
that subjects used a sequential, subvocal rehearsal strategy to
perform the verbal WM task, whereas most subjects reported
using some type of analog, or moving spatial image strategy in
the spatial task.
However, the transient nature of the P390, and the lack of any
load-related effects, suggests that this response does not index
WM maintenance operations. Rather, the sensitivity of this
response to the matching dimension of the stimulus suggests
that it may be involved with a memory comparison process or
with WM updating. When a nonmatching stimulus is presented,
the subject is required to add a new stimulus to the list of those
currently held in memory and to delete from memory the
stimulus that is no longer required. In the case of matching
stimuli, WM updating can be performed by rearranging the
order of which the stimuli currently held in memory are to be
compared to future stimuli. The larger EPs to nonmatching than
to matching stimuli may indicate that more resources are
required for WM updating when new content must be added.
The larger response in the verbal than spatial task suggests that
the process ref lected in the P390, whether a comparison process
or an updating process, is more active in response to verbal than
to spatial information. The practice-related increase in P390
sensitivity to the matching/nonmatching dimension shows that
this process becomes more efficient with task practice.
The biphasic midline central response, the P250, which was
apparent over approximately the same interval as the P280 and
P390 responses, may ref lect activity in areas involved with
processing spatial stimulus attributes. The P250 was larger in the
spatial than in the verbal task and was larger to nonmatching
than to matching stimuli in the spatial task. Like the P390, the
difference between responses to matching and nonmatching
stimuli was enhanced with task practice. These task correlates
suggest that this response ref lects activity in areas involved with
the comparison of spatial attributes of a stimulus with those
represented in WM, and/or with activity related to spatial WM
updating. Like the P390, this response also showed a practice-
related increase in the difference between matching and
nonmatching stimuli.
Figure 6. EP components modulated by match versus nonmatch decision requirements. Grand mean topographs are shown for responses to matching and nonmatching stimuli, forthe task version showing the largest stimulus differences. Data are averaged across load level. For the P250 grand mean responses in the spatial task are shown. For the P280 grandmean responses in the verbal task are shown. Both the P250 and P280 were larger to nonmatching than to matching stimuli. For the P300, grand mean responses averaged over bothverbal and spatial task are shown since this response was larger to matching than to nonmatching stimuli in both task versions. For the P390, responses in the verbal task are shown.Responses were larger to nonmatching than to matching stimuli. The same scale is used for the responses to Match and Nonmatch stimuli for each component. Scales differ acrossthe different components.
Figure 7. EP components affected by task practice. Grand mean topographs for each component differing between the first and third sessions are shown. Data from the high loadlevel only are shown. The CNV is averaged across verbal and spatial tasks, since it increased with practice for both task versions. The P250, P300 and P390 showed increaseddifferences between responses to matching and nonmatching stimuli with practice, thus for these responses, the topography of the difference waveforms are shown. The P250 waslarger to nonmatching than to matching stimuli in the spatial task only. Thus for this response, responses to matching stimuli were subtracted from those to nonmatching stimuli inthe spatial task. The P300 was larger to matching than to nonmatching stimuli so responses to nonmatching stimuli were subtracted from those to matching stimuli. The P390 waslarger to nonmatching than to matching stimuli, so responses to matching stimuli were subtracted from those to nonmatching stimuli. Since the practice effects for the P300 andP390 did not differ as a function of task version, these responses are shown averaged across spatial and verbal conditions. The same scale is used for the responses in the First andThird session for each component. Scales differ across the different components.
Table 2Average accuracy (d′) and reaction time scores in the Verbal and Spatial tasks in the first andthird testing session. Accuracy increased and reaction time decreased between the first and thirdsession. There were no differences in response accuracy as a function of verbal and spatial tasktype. Responses were significantly faster in the Spatial than in the Verbal task in the first sessiononly
Accuracy (d′) Reaction time (ms)
Verbal Spatial Verbal Spatial
Session 1 2.17 2.05 1111 1006Session 3 3.06 3.15 796 781
570 Evoked Potentials and Working Memory • McEvoy et al.
Cerebral Cortex Oct/Nov 1998, V 8 N 7 571
Load-sensitive but Task-insensitive P300 Response
In the latency range of 0.3–0.5s, a load-sensitive but task-
insensitive response (P300) occurred over parietal cortex. The
parietal P300 response observed in this study is one of a broad
category of positive parietal def lections occurring to task-
relevant stimulus, collectively referred to as the P3 or P300 (for a
review, see Picton, 1992). Although the P300 is one of the most
studied of all EP def lections, the cognitive significance of this
potential is not fully understood. Since the P300 is typically
elicited by task stimuli requiring a decision, and since its
amplitude increases with subjective confidence in the response
choice, it appears to be related to an aspect of cognitive proces-
sing involved with stimulus classification. The insensitivity of
this response to task version suggests that it represents a
higher-order cognitive component than that ref lected in the
P390 and P250 responses. Whereas the latter responses may
ref lect task-specific comparison or updating processes, the P300
may ref lect a decision-making component common to both
tasks.
The results of both our current and prior study (Gevins et al.,
1996) indicated that increasing the WM demands of the task
attenuated P300 amplitude. Similar results have been observed
in numerous memory studies using versions of the Sternberg
paradigm (Sternberg, 1969): as memory set size increases, the
P300 to probe stimuli decreases (e.g. Okita et al., 1985; Kramer
et al., 1986; Strayer and Kramer, 1990; Mecklinger et al., 1992).
This effect can be interpreted in terms of a resource allocation
theory of P300 amplitude. That is, the P300 has been concep-
tualized as indexing a pool of processing resources that can be
allocated among tasks. The P300 amplitude in a given task will be
attenuated to the extent that additional tasks utilize the same
resources (Natani and Gomer, 1981; Isreal et al., 1980; Kramer et
al., 1986). Thus the inverse relationship of P300 amplitude to
WM load suggests that the demand to retain information in WM
requires the reallocation of resources from the stimulus
classification and response decision-making component of the
task to the WM maintenance, or rehearsal, component (cf.
Mecklinger et al., 1992).
P300 amplitude in this task was also found to vary according
to whether the current stimulus matched or did not match the
target stimulus being remembered, being larger in the match
trials. This is consistent with results from other studies showing
that P300 amplitude is larger to probes that match a stimulus in
the memory set than to those that do not (e.g. Kramer et al.,
1986; Mecklinger et al., 1992). The difference in response
amplitude to matching and nonmatching stimuli increased with
practice, suggesting that with practice subjects became more
skilled in the stimulus classification and response decision-
making component of the task.
Late Post-stimulus Activity: Frontal and Parietal Slow
Waves
The requirements to maintain focused concentration on the task
and to constantly remember and manipulate information can be
expected to elicit sustained activation over various cortical areas
(Lang et al., 1992; Mecklinger and Pfeifer, 1996; Ruchkin et al.,
1990, 1992, 1998). For example, the analysis of the ongoing EEG
in both verbal and spatial WM tasks showed that frontal midline
theta increased as load level increased (Gevins et al., 1997,
1998). This was interpreted as ref lecting increased activation in
the anterior cingulate, an important node in the anterior
attentional network (Posner and Peterson, 1990; Posner and
Rothbart, 1992). The EP results in both this and our prior study
(Gevins et al. 1996) provide evidence of sustained activation of
left frontal and right parietal cortex, in the form of load-sensitive
but task-insensitive Slow Waves.
These frontal and parietal Slow Waves occurred after stimulus
evaluation and response preparation, in an interval in which
verbal or spatial information was being maintained in WM
between successive stimulus presentations. Both responses
systematically increased as a function of WM load but did not
differ between spatial or verbal versions of the tasks. This
suggests that these responses do not ref lect modality-specific
WM maintenance, but may instead be related to the higher-order
attentional demands of the task.
Support for the notion that the FSW is involved in nonspecific,
higher-order aspects of task performance comes from a recent
electrophysiological investigation of WM in the monkey (Rao et
al., 1997). In monkey frontal cortex neuronal firing in the delay
interval of a delayed matching-to-sample task was alternately
associated with the maintenance of either stimulus location or
object identity based upon the changing demands of the task.
Neuroimaging studies have also supported the role of the
prefrontal cortex in general executive and higher-order control
functions (eg. D’Esposito et al., 1995). Similarly, WM for any
form of information requires sustained attention, which has
been shown to asymmetrically activate right parietal regions
(Roland, 1982; Gevins et al., 1983, 1985; Deutsch et al., 1988;
Pardo et al., 1991). Modality nonspecific activation of inferior
right parietal cortex has also been reported in a recent PET
investigation of WM (Klingberg et al., 1996).
Thus the load-sensitivity and task-insensitivity of the frontal
and parietal Slow Waves suggest that these responses ref lect
higher-order aspects of task processing that are common to both
versions of the WM task employed here. These Slow Waves may
be related to the functional association between frontal and
parietal cortices necessary for performance of WM tasks. Studies
of lesion patients have indicated that electrical fields generated
in posterior cortex are modulated by inputs from frontal regions
(e.g. Knight et al., 1989; Yamaguchi and Knight, 1990). Studies
of nonhuman primates have also demonstrated the importance
of information transmission between frontal cortex and
posterior parietal regions for performance of WM tasks (e.g.
Friedman and Goldman-Rakic, 1994).
Activity in this frontal-parietal network did not change with
practice. This suggests that although subjects became more
skilled in task performance, and developed more efficient
preparatory and task-specific processing strategies, the higher-
order demands of the task were not diminished by practice.
Conclusions
This study has demonstrated that the mental operations engaged
by simple WM tasks are composed of numerous elementary
subsecond neural processes. Some of these processes, especially
those ref lected in the brief EP peaks, varied with type of
information (verbal or spatial) being retained. Other responses,
especially those ref lected in the frontal and parietal Slow Waves,
were affected by the amount of information being retained but
not by the type of information. This suggests that, in addition to
task-specific activation related to perceptual processes and to
task-specific WM processes, the functional neural networks that
arise during the performance of different types of WM tasks also
draw upon a limited-capacity system common to all
attention-demanding tasks (cf. Kahneman, 1973). Increasing
WM load not only systematically increased the sustained
activation of frontal and parietal regions involved in higher-order
572 Evoked Potentials and Working Memory • McEvoy et al.
attentional processes, but also suppressed response-related
processes (CNV and P300). Thus, as the WM demands of the task
increased, fewer resources were available for trial-specific
stimulus evaluation and response processing.
The results further showed that practice increased the
efficiency of stimulus evaluation and response preparatory
processes, although it did not decrease the higher-order
attentional demands of the task. The practice-related increase in
the prestimulus CNV suggests that response preparatory
processes became more efficient with practice, while the
practice effects on the P250, P300 and P390 potentials show that
stimulus evaluation and comparison processes also improved
with practice. In contrast, the absence of practice effects on the
frontal and parietal Slow Waves indicates that practice did not
globally decrease the attentional demands of the task. Rather,
these results indicate that practice-related improvements in
performance were primarily due to an increased efficiency in
preparing for and responding to stimuli on a trial-by-trial basis
while concurrently maintaining information in WM.
NotesWe thank Sue Whitfield and Georgia Rush for assistance with data
acquisition and preprocessing. This research was supported by grants
from the National Institute of Mental Health and the Air Force Office of
Scientific Research. Parts of this research were presented at the Annual
Meeting of the Society for Neurosciences, New Orleans, 1997.
Address correspondence to Linda McEvoy, EEG Systems Laboratory
and SAM Technology, 101 Spear Street Suite 203, San Francisco, CA
94105, USA.
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