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The Journal of Neuroscience, July 1, 1998, 18(13):5026-5034
The Role of Parietal Cortex in Verbal Working Memory
John
Jonides1,
Eric H.
Schumacher1,
Edward E.
Smith1,
Robert A.
Koeppe2,
Edward
Awh3,
Patricia A.
Reuter-Lorenz1,
Christy
Marshuetz1, and
Christopher R.
Willis1
1 Department of Psychology and 2 Division
of Nuclear Medicine, Department of Internal Medicine, University of
Michigan, Ann Arbor, Michigan, 48109-1109, and 3 Department
of Psychology, University of California, San Diego, California
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ABSTRACT |
Neuroimaging studies of normal subjects and studies of patients
with focal lesions implicate regions of parietal cortex in verbal
working memory (VWM), yet the precise role of parietal cortex in VWM
remains unclear. Some evidence (Paulesu et al., 1993 ; Awh et al., 1996)
suggests that the parietal cortex mediates the storage of verbal
information, but these studies and most previous ones included encoding
and retrieval processes as well as storage and rehearsal of verbal
information. A recent positron emission tomography (PET) study by Fiez
et al. (1996) isolated storage and rehearsal from other VWM processes
and did not find reliable activation in parietal cortex. This result
suggests that parietal cortex may not be involved in VWM storage,
contrary to previous proposals. However, we report two behavioral
studies indicating that some of the verbal material used by Fiez et al. (1996) may not have required phonological representations in VWM. In
addition, we report a PET study that isolated VWM encoding, retrieval,
and storage and rehearsal processes in different PET scans and used
material likely to require phonological codes in VWM. After subtraction
of appropriate controls, the encoding condition revealed no reliable
activations; the retrieval condition revealed reliable activations in
dorsolateral prefrontal, anterior cingulate, posterior parietal, and
extrastriate cortices, and the storage condition revealed reliable
activations in dorsolateral prefrontal, inferior frontal, premotor, and
posterior parietal cortices, as well as cerebellum. These results
suggest that parietal regions are part of a network of brain areas that
mediate the short-term storage and retrieval of phonologically coded
verbal material.
Key words:
neuroimaging; parietal cortex; positron emission
tomography; retrieval processes; speech; verbal working memory
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INTRODUCTION |
Working memory involves the
storage and manipulation of limited information for a brief time. A
particularly human form of working memory that appears to play a
significant role in language comprehension and problem-solving is
verbal working memory (Jonides, 1995). According to at least one
influential model, verbal working memory has three components: a buffer
to store phonological codes, a rehearsal process to refresh those
codes, and a set of executive processes to manipulate the contents of
the buffer in the service of higher cognitive demands (Baddeley,
1992).
Neuroimaging techniques indicate that brain activations
accompanying verbal working memory are found in dorsolateral
prefrontal, inferior frontal, supplementary motor, premotor, and
parietal cortices. Figure 1 summarizes
these studies by showing superimposed coordinates of activation from
published studies of verbal working memory. One area of activation that
is seen repeatedly in these studies is parietal cortex, in the regions
labeled by Brodmann as 7 and 40. This area is characteristic of studies
of working memory, but not long-term memory, as shown by the analysis
of Cabeza and Nyberg (1997). What is the function of this parietal region of activation? Some have argued that it is the seat of storage
processes (Paulesu et al., 1993; Awh et al., 1996). However, two
experiments that recruited storage processes did not find any evidence
of parietal activation at all. How is this to be reconciled?
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Figure 1.
Peak activation pixels reported in neuroimaging
studies of verbal working memory (Grasby et al., 1993; Paulesu et al.,
1993; Petrides et al., 1993; Andreasen et al., 1995; Awh et al., 1996;
Fiez et al., 1996; Schumacher et al., 1996; Smith et al., 1996; Cohen
et al., 1997; Jonides et al., 1997). Shown are four parasagittal slices
(Tailarach and Tournoux, 1988) in the left (x =  33 and x = 17) and right (x = +17 and x = +33) hemispheres to provide
approximate hemispheric localization of the identified areas. In each
slice, reliable areas of activation from the cited reports are
localized in proper y and z coordinates,
with a range of x coordinates being included in each
depicted slice, as indicated at the bottom of each
schematic. The different symbols represent different areas of
activation, as indicated in the legend. The areas of activation that
are taken from each report are not uniquely identified.
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One experiment by Grasby et al. (1993) suffered from a comparison of
memory and control conditions tested on different subjects. This may
have resulted (as the authors themselves recognized) in insufficient
statistical reliability to reveal underlying activations that may have
been revealed by within-subject comparisons. The second exception to
the finding of parietal involvement in working memory is an experiment
that was conducted to isolate the storage processes of verbal working
memory (Fiez et al., 1996). Subjects encoded five word or nonword items
and were scanned using positron emission tomography (PET) during a 40 sec retention interval only; they recalled the items after scanning was
complete. Fiez et al. (1996) reported activations in dorsolateral
prefrontal cortex, supplementary motor cortex, and left cerebellum,
consistent with other studies represented in Figure 1. Also, they
reported activations, although not statistically reliable, in Broca's
area and right cerebellum that are also consistent with previous
reports. Importantly, however, they reported no reliable activation in
parietal cortex even with a region-of-interest analysis designed to
focus on this area. This failure to find parietal activation has two
possible implications for the nature of processing in verbal working
memory tasks: parietal mechanisms are not involved in storage; rather, they are involved in encoding or retrieval processes. We investigated both implications.
First, we sought behavioral evidence that the failure to find parietal
activation in the experiment by Fiez et al. (1996) may have been a
function of their experimental procedure. Second, we conducted a
neuroimaging experiment that replicated and extended the design of the
study by Fiez et al. (1996) but also included conditions to assess the
contribution of parietal activation to encoding and retrieval
processes.
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BEHAVIORAL EXPERIMENTS |
The experiment by Fiez et al. (1996) included three scans in which
retention was required: one for semantically related words, one for
unrelated words, and one for nonwords. Words can be coded in terms of
some combination of semantic, phonological, or visual codes. However,
verbal working memory is typically identified with a phonological
coding strategy, a strategy that extends not only to meaningful words
but also to other verbal material that is not semantically codable
(e.g., syllables). For example, many studies have shown selective
interference on material in verbal working memory by phonologically
interfering tasks, and others have shown that phonologically similar
items are more difficult to store in verbal working memory than
dissimilar items (Conrad, 1964; Murray, 1968). Also, patients who have
deficits in verbal working memory can be quite normal in their storage
of semantic and visual codes (Warrington et al., 1971; Saffran and
Marin, 1975). All of this evidence implicates a phonological code in many verbal working memory tasks, a code that may be responsible for
parietal activations. If, however, subjects in the experiment by Fiez
et al. (1996) relied on semantic codes in part to retain the word
stimuli, then the impact of a phonological working memory would be
mitigated, leaving only one scan (that with nonwords) to show the full
activation pattern that might be characteristic of phonological
processing. One scan might not be sufficiently sensitive to reveal this
pattern. To test the possibility that subjects rely more on
phonological working memory for nonwords than words, we first conducted
two behavioral experiments, both of which were intended to reveal the
use of a phonological coding strategy if one was in play.
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EXPERIMENT 1 |
Materials and methods
In the first experiment, we tested subjects on working memory
for words and nonwords using a presentation and storage procedure similar to that of Fiez et al. (1996) but with retrieval assessed by a
recognition rather than a recall test. A recognition test allowed us to
present distractors that varied in their similarity to the target items
so that we could assess which kinds of distractors were likely to cause
errors. From this, we could make inferences about the kinds of internal
codes used to store words and nonwords.
Subjects. Twelve right-handed subjects (six males and six
females) were paid for participation in an experimental session of ~1
hr. All were informed of the experimental procedure and consented to
participate.
Stimuli. The experiment consisted of 22 trials, 11 using
words as the target stimuli and 11 using nonwords. The words were selected from the list by Paivio et al. (1968), with some additional words that had fewer than seven letters and were of two or three syllables in length; the criterion for selection was words with high
frequency of occurrence in English and low concreteness (to mitigate
the use of a mnemonic strategy based on imagery). Words in a list were
semantically unrelated to one another. The semantically related
distractors for the words were chosen from the same categories as the
target words. The phonologically similar distractors were chosen so
that they either rhymed with one of the targets or were otherwise
phonologically similar (e.g., loss-cost). The nonwords were
constructed so as not to approximate English words. Phonologically similar nonword distractors were constructed by changing some of the
consonants and/or vowels of the target nonwords; they either rhymed
with a target or were otherwise phonologically similar, as with the
words.
Experimental procedure. Subjects were seated ~46 cm from a
computer monitor. Each trial began with a fixation dot that appeared in
the center of the monitor controlled by a Macintosh IIC computer running Psyscope control software (Cohen et al., 1993). The fixation dot remained on the screen throughout the trial. At the beginning of
each trial, five targets (either all words or all nonwords) were
presented sequentially just below the fixation dot for 3 sec each with
500 msec intervening between successive stimuli, replicating the
presentation conditions of Fiez et al., (1996). After presentation of
all targets, a tone sounded signaling the beginning of a 55 sec
retention interval. The termination of this interval was signaled by a
pair of tones after which 22 probe items were presented consecutively
just below fixation, each for 500 msec with an interprobe interval of
1500 msec. Subjects were to respond with one of two key presses to
indicate whether each probe matched one of the five target items. Of
these 22 probes, 10 matched the targets (two matches of each target),
and 12 were distractor items. When words were the targets, four of the
distractors were phonologically similar to one of the targets, four
were semantically similar, and four were dissimilar from all targets.
When nonwords were the targets, six of the distractors were
phonologically similar to one of the targets, and six were dissimilar
(of course, there could be no semantically similar distractors for
nonwords). The order in which probes of these various types were
presented was randomly determined. Half of the subjects received all of
the trials with words before any trials with nonwords; the other half were given the trials in the reverse order.
Results and discussion
When words were the memorized targets, the accuracies of
recognition responses to dissimilar distractors, semantically similar distractors, and phonologically similar distractors were 99.2, 98.1, and 99.6%, respectively; the corresponding response times for these
three types of distractors were 618, 635, and 665 msec, respectively.
Even as high and uniform as the accuracies appear, there is an overall
effect of distractor type on accuracy as assessed by ANOVA
(p < 0.002). This overall effect is accounted
for by the fact that the semantically similar distractors produced
responses less accurate than either the dissimilar
(p < 0.001) or the phonologically similar
distractors (p < 0.001). The response times are
also different from one another (p < 0.0005),
and this difference is a result of a reliable difference between the
dissimilar distractors and the phonologically similar ones
(p < 0.0005) as well as a marginally reliable
difference between the dissimilar distractors and the semantically
similar ones (p = 0.07).
When nonwords were the targets, there was a large difference in both
accuracy and response time between dissimilar distractors and
phonologically similar distractors (96.9 vs 83.8% and 670 vs 798 msec,
respectively). The differences between these types of distractors in
both accuracy (p < 0.0001) and response time (p < 0.0001) were highly reliable.
Overall, the word targets showed evidence of both semantic and
phonological coding, in that there were effects of semantically similar
distractors on accuracy, and of both semantically similar and
phonologically similar distractors on response time. For the nonwords,
there was a large effect of phonological similarity on both accuracy
and response time, an effect that was much larger than the effect of
phonologically similar distractors on accuracy or response time for
words. This was supported by two ANOVAs (one for accuracy and one for
response time) that included words versus nonwords as stimuli and
phonologically similar versus dissimilar distractors; these analyses
showed that the effect of phonological similarity was decidedly larger
for nonwords than for words (p < 0.0005 for
each of the dependent measures). These data suggest three things about
the use of words and nonwords in a paradigm such as that used
by Fiez et al. (1996): (1) words are coded and stored using some
combination of phonological and semantic representations; (2) nonwords
are coded and stored using a phonological representation; and (3)
nonwords rely much more on a phonological representation than words.
There are two interpretations of the greater effect of phonological
similarity on nonwords than words: there is more phonological coding
for nonwords than there is for words, and nonwords are not subject to
other types of coding that are available for words (e.g., semantic), so
the phonological coding effect is more prominent for nonwords.
Whichever of these is correct, our results led us to hypothesize that
Fiez et al. (1996) may not have found evidence of posterior parietal
activation, because their imaging data were heavily influenced by the
processes responsible for storing words, and these may have relied more
on a semantic than a phonological code. If posterior parietal
mechanisms are specific to phonological coding and storage, then this
would mitigate activations in this area for word stimuli in their
study. To provide converging evidence about this hypothesis, we
conducted a second behavioral experiment. This experiment assessed the
use of a phonological code by attempting to interfere with its
operation.
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EXPERIMENT 2 |
Materials and methods
The second experiment was also intended to probe for the use of
a phonological working memory strategy when words versus nonwords were
used as stimuli. In all respects, the present experiment replicated the
presentation and recall parameters of Fiez et al. (1996), with two
exceptions. During the retention interval (55 vs 40 sec), used by Fiez
et al. (1996) for technical reasons), we had subjects either engage in
articulatory suppression by repeatedly saying "one, two, three,
four" aloud at a rate of ~1.5 digits/sec, or we had them trace a
figure eight repeatedly with their left index finger around a block
outline figure eight. Articulatory suppression is known to suppress the
ability of subjects to engage in verbal rehearsal, and thus it should
interfere with storage and rehearsal of a phonological code if one is
in use (Murray, 1968). Thus, we examined whether storage of words
versus nonwords was impaired by articulatory suppression, and we
compared this effect with any generally interfering effect caused by a
secondary task (tracing) that should result in only nonspecific
interference with verbal memory.
Subjects. Six subjects participated for payment; all
consented to volunteer for an experimental session of 1 hr.
Stimuli. The words and nonwords that were used as target
stimuli were selected and constructed as described for experiment 1. In
experiment 2, however, the words that were targets could either be
related to one another or unrelated. When related, the words were
chosen from the same semantic category; when unrelated, they had no
obvious semantic relationship to one another.
Experimental procedure. Subjects were tested on their memory
for nonwords, related words, and unrelated words. The order in which
these three types of stimuli were tested was varied across subjects in
a counterbalanced manner. For each type of material, subjects were
sequentially presented five items of the appropriate type (3 sec each
with 500 msec intervening between successive items), and they retained
those items in memory during a 55 sec retention interval that was
filled with one of the two types of interfering task. After this
interval, subjects were required to free recall the items orally (as in
Fiez et al., 1996), and their responses were recorded for later
transcription.
Subjects completed all types of trials with one interfering task and
one type of stimulus material (e.g., articulatory suppression interfering with nonword stimuli) before moving on to the other type of
interfering task with the same type of stimulus material (e.g., tracing
interfering with nonword stimuli). For each interfering task, subjects
were given one trial of practice before being given four trials of
testing with that interfering task, after which they switched to the
other interfering task with the same type of stimulus material. The
order in which they were given the two types of interfering tasks was
the same for each of the types of stimulus materials they memorized,
and the order of interfering tasks was counterbalanced across
subjects.
Results and discussion
The mean recall accuracies for related words, unrelated words, and
nonwords were 98, 83, and 51%, respectively. Overall accuracy was 84%
with the interfering tracing task but only 69% with the articulatory
suppression task. An ANOVA that included type of material (related
words, unrelated words, and nonwords) and type of interfering task
(tracing and suppression) indicated that both of these main effects
were reliable (p < 0.0005 and 0.02, respectively). The interaction between these factors was also
significant (p < 0.02), so we examined the
individual effects to locate the source of the reliable interaction.
This analysis revealed that articulatory suppression interfered more
than tracing for both nonwords and unrelated words (41 vs 61% for
nonwords, p < 0.01; 71 vs 94% for unrelated words,
p < 0.0005).
It is surprising that this interference is not greater for nonwords in
view of the results of experiment 1 that nonwords showed a greater
phonological similarity effect than words. However, in that the
performance levels with words and nonwords are quite different overall,
it is difficult to conclude much about the apparently equivalent
magnitudes of the effects of articulatory suppression. The issue is one
of scaling. At a high accuracy level, a 23% difference may not be
psychologically equivalent to a 20% difference at a lower accuracy
level. Consider, for example, rescaling the results into a percentage
score for the effect of articulatory suppression. For unrelated words,
articulatory suppression produces a decrement in performance of 24%
(94 71/94%), whereas for nonwords, it produces a decrement of
33%. Looked at in this way, nonwords do show a greater effect with
articulatory suppression. Overall, without a theory of what the proper
scale of comparison is, it is difficult to evaluate this issue.
For the related words the type of interfering task had no reliable
effect (97 vs 98%; p = 0.73). We conclude from this
that a phonologically interfering task has a pronounced effect on
memory for nonwords and for unrelated words, suggesting that a
phonological code is used at least in part to retain these stimuli in
memory. For related words, the fact that performance is so good overall and that it is not differentially affected by phonological versus nonphonological interfering tasks is consistent with the conclusion that the storage of these materials in memory may rely largely, or
perhaps exclusively, on a semantic, rather than a phonological, code.
Taken together, experiments 1 and 2 make the case that the storage of
nonwords relies unequivocally on the use of a phonological code. For
words, by contrast, storage may rely on both a phonological code and a
semantic code. Thus, the use of words in an experiment that
investigates phonological working memory may not provide the best
evidence of the circuitry that accompanies phonological coding and
storage, although it may be entirely suitable to provide evidence of
circuitry involved in semantic working memory. For two of its three
scans, the experiment by Fiez et al. (1996) relied on words as stimuli;
therefore, that experiment may not have had an adequate opportunity to
observe brain activations that depended on phonological coding and
rehearsal. It should be noted that in a separate analysis, Fiez et al.
(1996) did find evidence of greater activation of a frontal opercular
region in their nonword than in their word conditions, suggesting that
even in their experiment, subjects may have engaged in rehearsal more
with nonword than with word stimuli. For this reason, we replicated and
extended the experiment by Fiez et al. (1996) using nonwords as
stimuli.
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NEUROIMAGING EXPERIMENT |
Materials and methods
Rationale
The neuroimaging experiment was designed to replicate the
conditions of Fiez et al. (1996) with sufficient statistical power to
discover parietal activation in a storage condition and to add
conditions that would assess the role of parietal activation in
encoding and retrieval processes as well. We restricted our stimuli to
the class of nonwords in this experiment for three reasons: (1) the
behavioral data reported above make the case that nonwords evoke a
phonological coding and storage strategy, whereas words are subject to
semantic coding (in addition to phonological coding); (2) the
introspections of subjects in the behavioral experiments indicated that
nonwords required much more intensive rehearsal than did words, again
suggesting the use of a phonological code for nonwords; and (3) the
poorer performance in retrieval of nonwords than words indicates that
processing of the former items is more demanding, suggesting that
storage and rehearsal might be more effortful with nonwords, thereby
leading to greater brain activation in the areas mediating the storage
and rehearsal processes. Thus, we were encouraged in the belief
that nonwords provided the best opportunity to discover evidence
of parietal involvement in verbal working memory using a phonological
code.
Subjects
The participants were six males and six females, all of whom
were right-handed. They were paid for their participation, and they
consented to participate for two sessions, one that provided practice
on the tasks and one during which the PET scans were conducted.
Conditions
There were three memory and two control conditions in the
experiment, each tested twice during the PET session for a total of 10 scans. Each condition was also tested during a practice session that
preceded the day of PET testing. The three memory conditions all
included nonwords as stimuli, with scanning directed at storage,
encoding, or retrieval phases of processing, respectively. The two
control conditions were designed to remove effects of perceptual and
motor processes.
Storage condition. This condition was designed to be similar
to that of Fiez et al. (1996). A trial began with the presentation of
five nonwords for 3 sec each, with 500 msec intervening between successive nonwords, for a total presentation interval of 17.5 sec.
Immediately after this interval, a tone sounded and a fixation cross
appeared on the computer screen, which signaled a retention interval
that lasted 65 sec. After this, a retrieval phase began with the
presentation of a pair of tones, which indicated to subjects that they
were to recall the five nonwords in any order they chose. PET scanning
began 5 sec after the onset of the retention interval and terminated
before the beginning of retrieval. Thus, there was no encoding of
stimuli during the period of scanning; the scanning interval was
occupied largely by processes of storage and possibly some processes of
covert retrieval before the explicit retrieval task.
Encoding condition. In the encoding condition, seven
nonwords were presented for 2 sec each with 500 msec intervening
between presentation of successive stimuli (seven items were used
rather than five, as in the storage condition, to occupy encoding
processes more fully in this task). Each nonword was presented twice
for a total of 35 sec devoted to presentation of stimuli. After this interval, a tone sounded and a fixation cross appeared on the screen
for 65 sec, during which time subjects were to store the nonwords in
memory (just as they did in the storage condition). After this
retention interval, a pair of tones sounded, and subjects engaged in
retrieval, which consisted of a recognition task (recognition was used
to collect data about whether the phonological similarity of mismatches
affected responses, as it should if subjects were engaged in
phonological encoding). During the retrieval interval, 21 nonwords
appeared one at a time, and subjects responded with one of two key
presses to indicate whether each presented nonword matched one of the
studied items. Seven of these stimuli matched the original nonwords;
seven mismatches were phonologically dissimilar; and seven mismatches
were phonologically similar to the original nonwords. Each of these
test stimuli was presented for 2 sec, with 500 msec intervening between
successive stimuli. Thus, the retrieval phase as a whole lasted 52.5 sec. Scanning was initiated 5 sec before the beginning of the study
phase of the experiment and during the first 25 sec of the retention
interval when the fixation cross was on the screen (i.e., the scans
included encoding processes of interest and then switched to a neutral
condition after 35 sec; this paradigm has been shown to be effective in revealing activating effects of the task of interest) (Koeppe et al.,
1994; Cherry et al., 1995). Thus, the PET data include activations that
were largely a function of processes used to encode the stimuli into
memory and to store them, with little or no contribution of retrieval
processes.
Retrieval condition. We began each trial with the
presentation of five nonwords for 3 sec each with 500 msec between
successive nonwords (as in the storage condition). This presentation
phase was followed by a single tone that signaled a retention interval of 65 sec, during a which a fixation cross was presented on the screen
(as in the encoding and storage conditions). After the retention
interval, a pair of tones was sounded signaling the beginning of
retrieval. During the retrieval phase, 14 nonwords were presented for 2 sec each with 500 msec between successive nonwords for a total of 35 sec. Of these 14 nonwords, five were identical to the nonwords that
subjects stored in memory, five were phonologically similar
distractors, and four were phonologically dissimilar distractors. After
the last of these nonwords was presented, a fixation dot appeared on
the screen and remained for 30 sec. Scanning was initiated 5 sec before
the beginning of the retrieval phase and continued through the duration
when the dot appeared on the screen, for a total of 65 sec (again,
making use of a switching paradigm during scanning) (Koeppe et al.,
1994; Cherry et al., 1995). In this way, we designed this condition to
concentrate on activations that were a function of retrieval processes,
but, of course, encoding and storage processes were also involved, in
that subjects had to encode the probes and had to continue storing the
five target items until the end of the retrieval period.
Fixation control. This condition was designed to match the
perceptual and response characteristics of the storage condition and to
be similar to the control condition of Fiez et al. (1996). Accordingly,
it included just a fixation cross that remained on the screen with no
response requirement on the part of subjects. The fixation cross was
presented before the beginning of the scan and remained for a total of
105 sec, lasting well past the end of the scan.
Nonword control. This condition was designed as a control
for the encoding and the retrieval conditions. The condition began with
14 nonwords, each presented for 2 sec with 500 msec between successive
nonwords. Subjects were required to push a response button at the onset
of each nonword. After the last nonword was presented, a fixation cross
appeared on the screen and remained for the duration of the scanning
interval. Thus, this condition included presentation of exactly the
same number of nonwords as the encoding and retrieval conditions, and
it also included a switch to a fixation cross after the 14 nonwords
appeared, matching the presentation parameters of the encoding and
retrieval conditions. We had subjects make a manual response with the
presentation of each nonword to match the responses that they made in
the retrieval condition (although this made the control not completely
comparable to the encoding condition in which no manual responses were
made during the scanning interval).
Conditions were counterbalanced for presentation in the experiment
according to the following scheme: each condition was tested once
before any condition was tested a second time. The order of
presentation of conditions during the first five scans was repeated for
the next five. For the first five scans, either the fixation control or
the nonword control was presented first, with the other control
condition presented fifth in order. Half of the subjects had the
fixation control presented first, and half had the nonword control. The
middle three scans of the first five were the encoding, storage, and
retrieval conditions, with the order among these three counterbalanced
completely within each set of three subjects. Below, we describe the
events for a scan of each of the three memory conditions and the two
controls.
PET protocol
A Siemens (Erlangen, Germany) ECAT EXACT-47 PET scanner was used.
It produced 47 contiguous slices that were 3.375 mm (center to center)
apart. The reconstructed in-plane resolution was 10 mm full-width,
half-maximum. Subjects were positioned in the scanner, and their head
positions were recorded. Head position was verified before each scan.
Each subject had an intravenous catheter inserted into his or her right
arm.
The experimenter administered an intravenous bolus of 40 mCi of
[15O]water at the beginning of each scan as the
subject began the sequence of trials. PET scanning began 5 sec after
the count rate increased above the background level and continued for
60 sec. Twelve minutes separated each scan to allow the background
radiation to reach an ~1% level caused by clearance and decay.
Results and discussion
Behavioral data
Accuracy for the storage condition, in which free recall was the
required retrieval task, was 64% during the PET session, somewhat
lower than that of Fiez et al. (1996), in which a response had to match
one of the encoded items perfectly to be scored correct. For the
encoding and retrieval conditions, for which the retrieval task was
recognition, average accuracies were 93 and 92%, respectively, during
the PET session and 88 and 94% during the practice session. For these
tasks also, we recorded response times, which averaged 889 and 880 msec
for the encoding and retrieval conditions, respectively, during the PET
session and 886 and 870 msec during the practice session.
Of interest is a comparison of responses when a probe item on the
recognition test in the encoding and retrieval conditions did not match
one of the target nonwords. A mismatch could be either phonologically
similar to a target or dissimilar from all targets in the set for that
trial. When a probe was similar to the target, accuracy and response
times were reliably worse than when the probe and target were not
similar in both the PET and practice sessions. Participants were 13%
less accurate when the probe was similar to the target than when it was
not similar during the PET session (99% for dissimilar and 86% for
similar probes; p < 0.0001) and 15% less accurate
during the practice session (99% for dissimilar and 84% for similar
probes; p < 0.002) (the data from one participant
during the practice scan were not analyzed because of a technical
error). Participants were 172 msec slower when the probe was similar to
the target than when it was not during the PET session (805 msec for
dissimilar and 977 msec for similar probes; p < 0.0001) and 138 msec slower during the practice session (809 msec for
dissimilar and 947 msec for similar probes; p < 0.0001). These effects, for both response time and accuracy, were not
reliably different for the encoding and retrieval conditions. Thus,
there is a pattern of phonological similarity effects in these data
that mimics that in experiment 1, suggesting, once again, that subjects
encode and store phonological representations for nonwords in this
task.
PET data
We conducted omnibus analyses of each of the memory conditions
compared with its appropriate control as well as specific analyses that
asked whether there was activation in posterior parietal and other
regions. For the omnibus analyses, regional cerebral blood flow changes
between two different conditions were assessed by subtraction analysis
of PET image sets (Friston et al., 1991; Worsley et al., 1992). First,
intrasubject registration by an automated algorithm corrected motion
between scans within a subject's PET session (Minoshima et al.,
1993a). PET image sets for each subject were then transformed to a
standard bicommissural stereotactic system (Talairach and Tournoux,
1988). The transformation procedure consisted of three steps: (1)
detection of the midsagittal plane of the brain (Minoshima et al.,
1992), (2) detection of the bicommissural (anterior
commissural-posterior commissural) line of the midsagittal plane
(Minoshima et al., 1993b), and (3) linear scaling followed by nonlinear
warping of the brain to remove anatomic differences among subjects
(Minoshima et al., 1994). Next, a subtraction image set was created for
each subject between the averaged images for memory task minus its
control condition. The subtraction image sets were then averaged across
subjects, producing a group average subtraction image set consisting of
mean and SD of cerebral blood flow (CBF) changes for each brain voxel.
SDs for the voxels were averaged within the brain to create a pooled
estimate of variance, and t statistical values were
calculated for each voxel using a pooled variance estimate and
correcting for multiple nonindependent comparisons (Friston et al.,
1991; Worsley et al., 1992). Significant CBF changes were localized
using stereotactic coordinates and are displayed in the figures on a
standard nonlinearly warped magnetic resonance image (to Talairach
coordinate space) for visual interpretation.
The areas of reliable activations and deactivations are reported in
Table 1 for each of the memory conditions
minus its respective control (i.e., when the control condition produced
lower activation than the experimental condition or when it produced
higher activation than the experimental condition). For each reliable
area, we report the stereotactic coordinate, the Z score of
the peak pixel, and the Brodmann label for the area.
Storage-fixation control. Consider first the activations
and deactivations for the storage-fixation subtraction reported in Table 1. This condition closely approximates the condition used by Fiez
et al. (1996). We find activation in left inferior frontal gyrus
(Broca's area), left premotor cortex, supplementary motor cortex, and
right cerebellum, all of which are characteristic of a circuit for
verbal working memory (Fig. 1). We also find activation in dorsolateral
prefrontal cortex in both left and right hemispheres, a pattern that
has also often been associated with some verbal working memory tasks
(Smith et al., 1996; Cohen et al., 1997). In addition, there is
reliable activation in left cerebellum and in right inferior frontal
gyrus, both of which are approximately homologous to activations found
in the opposite hemisphere (homologous bilateral activation is often
found in studies using working memory tasks; Smith et al., 1996).
In addition to these sites, note also that there is reliable activation
in lateral posterior parietal cortex in Brodmann's area 40, an area
not found by Fiez et al. (1996). This site of activation is reliably
activated by post hoc analysis in the right hemisphere only,
but inspection of the activation images suggests that there is also
activation of a homologous site in the left hemisphere. Because
posterior parietal sites of activation are often found in studies of
verbal working memory, we constructed regions of interest (ROIs) based
on data from previous verbal working memory experiments to interrogate
the present data to determine whether there was statistically reliable
activation in both left and right parietal sites. For all of these ROI
analyses, we took peak voxels of activation from previous experiments
and constructed spherical ROIs with a diameter of 10.8 mm and placed these on the data of individual subjects from the present experiment. We then averaged the activation of all voxels within the ROI for each
subject and compared this mean to zero to determine whether there was
significant activation present.
The first such analysis was based on a verbal working memory task from
Awh et al. (1996) in which subjects had to match each of a series of
letters to the letter that had occurred two items back in the series (a
"two-back" task). In this experiment, there were two left and two
right parietal sites of activation with coordinates (33, 46, 38),
(17, 60, 45), (12, 64, 47), and (26, 55, and 50). Applying
these ROIs to the data of the storage-fixation subtraction revealed
two reliable activations (p < 0.05), one in
each hemisphere (33, 46, 38; 12, 64, 47). We next created ROIs
from a set of experiments that had used a three-back verbal working
memory task (matching each letter against the one that was three items
back in the series) (Smith et al., 1996; Schumacher et al., 1996,
Jonides et al., 1997). Collapsing across these three experiments, two
reliable parietal ROIs were chosen, one in the left (35, 49, 38)
and the other in the right (37, 49, 40) hemisphere. Applying these
ROIs to the present data revealed reliable activation in both areas
(p = 0.053 in the left and p < 0.002 in the right hemispheres). Taken together, these analyses reveal
that there are sites of reliable activation in posterior parietal
cortex, in both the left and right hemispheres. These sites are located either in Brodmann's area 7 or 40, sites that have previously been
implicated in working memory tasks.
We compared the activations in the left and right posterior sites to
determine whether one was reliably larger than the other by using the
ROIs from the three-back tasks, cited above. Although the magnitude of
the activation was larger on the right than on the left, these
activations did not differ reliably (p = 0.2351). Nonetheless, we are cautious in accepting a null hypothesis
about this difference. In part this is because we entertain the
hypothesis that some of the parietal activation we obtained may be a
function of attentional processes that are required to change focus
from one item to another as they are rehearsed. This might be expected to be a function of processes more of right than left parietal cortex,
based on imaging studies of selective attention (Corbetta et al., 1993,
Heinze et al., 1994). So, the greater magnitude of right than left
parietal activation that we have documented, although not reliable, may
indicate an involvement of parietal mechanisms in shifting attention
from internal representations of one item to another as they are
rehearsed. At this point, this issue is not resolved. We do note,
however, that our previous studies of verbal working memory have also
found substantial right as well as left parietal activation, so our
data are not inconsistent with these past results (Awh et al., 1996;
Schumacher et al., 1996; Smith et al., 1996; Jonides et al., 1997).
Another focus of interest in the storage-fixation subtraction is the
activation in dorsolateral prefrontal areas. Table 1 shows that there
was one site of reliable activation in left dorsolateral prefrontal
cortex and three sites in right. These regions may be involved in the
executive control of processes required for storage and rehearsal of
the nonwords in our study. For example, there may be processes
necessary to tag the memoranda with relevant context so that they can
be retrieved later. Another possibility is that the long retention
interval used in our study, and that of Fiez et al. (1996) as well,
resulted in the recruitment of long-term memory processes in addition
to processes of working memory. If this were the case, we might expect
that there would be some overlap between the dorsolateral prefrontal
areas that we observed and those frequently found in other long-term
memory studies. Of course, areas involved in the encoding of
information for long-term memory are not relevant to this issue in that
the storage condition of the present experiment did not involve any encoding at all. However, regions of activation in long-term memory experiments that may be involved in either storage or retrieval may be
relevant (assuming that the storage condition of the present experiment
may have involved some covert, internal retrieval as well). With this
in mind, we used the 10 sites of activation that Cabeza and Nyberg
(1997) identified as sites from long-term memory studies that may have
been involved in storage or retrieval (coordinates: 32, 7, 55; 30, 32, 33; 27, 47, 1; 48, 8, 32; 26, 27, 8; 32, 42, 15; 28, 21, 2; 29, 53, 1; 23, 25, 3; and 36, 50, 10). We then created spherical regions of
interest from the peak voxels of these sites with a diameter of 10.8 mm
and applied these to the present data. Eight of the 10 sites had
reliable activations (p < 0.05), and the other
two approached reliability (p < 0.11).
Overall, then, the pattern of activation we find in the subtraction of
the fixation control from the storage condition is consistent with past
studies of verbal working memory, including, importantly, activation in
posterior parietal cortex. In addition, we find some evidence that
there may be some long-term memory involvement in the storage
condition, which we attribute to the long retention intervals involved
in the experiment. We conclude that there continues to be reason to
suspect involvement of the posterior parietal cortex in storage
processes. The involvement may be as part of a circuit controlling
shifts of attention involved in rehearsing the verbal material, or it
may be as part of a circuit involving storage itself.
Retrieval-nonword control. The activations found in a
subtraction of the nonword control from the retrieval condition are also listed in Table 1. Note that by post hoc analysis there is reliable activation in right posterior parietal cortex in a region
almost identical to that found in the storage-fixation control
subtraction. In addition, there is activation in right dorsolateral
prefrontal cortex, overlapping the activation site found in the
storage-fixation subtraction. This is confirmed by placing ROIs from
the parietal and frontal areas of the storage-fixation subtraction on
the data of the retrieval-nonword subtraction. In that these two
subtractions represent completely independent scans, the fact that
there is overlap in the parietal and frontal activations suggests that
the storage and retrieval conditions share some circuitry in common. A
strong candidate for the function that is mediated by this common
circuitry is storage: this is the defining feature of the storage
condition, and storage of the target nonwords is required in the
retrieval conditions while subjects are matching these targets against
the probes that they encounter. It seems reasonable, therefore, to
argue that a combination of frontal and parietal mechanisms is involved
in storage processes. This argument is consistent with previous
research that has also implicated parietal (Paulesu et al., 1993; Smith
et al., 1996; Jonides et al., 1997) and frontal (Cohen et al., 1997)
mechanisms in the storage of information in working memory.
For the same reason that we suspected that long-term memory processes
may have played some role in the storage condition, we also suspected
that they may have been involved in the retrieval condition.
Consequently, we applied a region-of-interest analysis to the
retrieval-nonword activations using the same 10 ROIs identified from
the report of Cabeza and Nyberg (1997) that mark long-term memory
regions playing a role in storage. Of these 10 regions, eight were
reliably activated (p < 0.05) in the
retrieval-nonword subtraction; the remaining two were suggestively
close (p = 0.08 and 0.14). Thus, we suspect that
the long retention interval used in the retrieval condition may, as
with the storage condition, have permitted long-term memory processes
to play some role.
We also note that the retrieval condition shows evidence of activation
in left and right extrastriate regions of occipital cortex. Perhaps the
control condition did not engage perceptual mechanisms for encoding the
nonwords to the same extent as did the retrieval condition. This may
have been a result of subjects having to attend to the identity of each
nonword that was presented in the retrieval condition but having to
attend only to the fact that an item was presented in the control
condition, regardless of its identity.
Encoding-nonword control. As Table 1 reports, this
subtraction yielded no areas of activation that were statistically
significant, but one area of activation in left extrastriate occipital
cortex was nearly significant. This site of activation is nearly
identical to one of the extrastriate sites found for the
retrieval-nonword subtraction, and so we attribute it to the same
hypothesized cause, greater encoding processes recruited by the
encoding condition than by the control condition.
It is of interest to note that the encoding condition did not show any
evidence of posterior parietal activations. This was confirmed by
applying ROIs for left and right posterior parietal sites (identified
in the same way as in the analysis of the storage-fixation subtraction) to the encoding-nonword subtraction. None of these ROIs
revealed significant sites of activation (p > 0.20 in both cases).
Of course, one might argue that the present paradigm involves not only
working memory but also long-term memory processes, as we suggested
above. So, perhaps mechanisms that are involved in the encoding of
verbal information for long-term storage are also appropriate
candidates to reveal themselves in this condition. To examine this, we
identified five areas that Cabeza and Nyberg (1997) identified as
associated with long-term encoding, and we applied ROIs based on these
areas to the present data. Only one area (2, 28, 28) approached
reliability (p = 0.056).
It is possible that the amount of encoding that was necessary in the
encoding condition was relatively light, and so the brain mechanisms
that mediated this encoding were not sufficiently taxed to reveal
themselves in our study. This possibility is somewhat contradicted by
the fact that we did find a site of nearly reliable activation in
extrastriate cortex. Nevertheless, we remain cautious in interpreting
the null findings of encoding-related activations in either posterior
parietal cortex or in areas associated with encoding for long-term
memory. Exercising this caution, however, we offer the hypothesis that
posterior parietal cortex is not a primary site of mechanisms involved
in the encoding of material for working memory.
Deactivations. We have included in Table 1 regions in which
the control conditions produced higher relative cerebral blood flow
than their respective experimental conditions. There is little general
agreement from previous research about the proper interpretation of
"deactivations" such as these. As Shulman et al. (1997) discuss, there are two classes of hypothesis to account for them: decreased activation in the memory conditions as a function of inhibitory task
processes or suspension of processes in the memory conditions that are
normally active in the control conditions. Shulman et al. (1997) point
out that task-related deactivations caused by processes of the
experimental conditions should be idiosyncratic; that is, they should
reflect the specific processes that are needed by these conditions. By
contrast, there may be more commonality among the deactivated areas
across experiments if these areas represent suspension of processes
that are normally active in the passive control conditions (e.g.,
unconstrained thought processes and monitoring of the external
environment). Comparison of the areas of deactivation shown in Table 1
with those documented by Shulman et al. (1997) for nine visual tasks
that do not involve working memory explicitly reveals some
commonalities and some differences. Broadly speaking, there are
similarities in deactivations in areas of medial frontal cortex,
posterior cingulate, sections of posterior parietal cortex, and
anterior temporal areas. At a finer grain of analysis, though, the
match between the deactivations shown in Table 1 and those reported by
Shulman et al. (1997) is sporadic. So, it is difficult to conclude
whether there is a consistent pattern of deactivations across studies
regardless of task or whether the deactivations are task-specific. We
do note that many of the regions of deactivation in our experiment 3 are ones that have been cited in previous studies of working memory
(Jonides et al., 1997). These include regions of inferior temporal
cortex, angular gyrus, precuneus, and frontal pole. Certainly, the
issue of whether there is common or distinct deactivation across tasks
deserves much further study.
| |
CONCLUSIONS |
Overall, the results of the present study confirm what is by now a
growing literature on the circuitry of verbal working memory. This
literature has documented the involvement of a network of sites
concentrated in dorsolateral prefrontal, premotor, supplementary motor,
inferior prefrontal, cerebellar, and posterior parietal areas. The
storage condition of the present experiment reveals activations in all
of these sites, including the posterior parietal site that was not
activated in two previous reports (Grasby et al., 1993, Fiez et al.,
1996). We conclude that the pattern of activations we and others have
found for parietal cortex implicates it in mechanisms involved in the
storage of verbal material. Corroborating these observations are
several cases in which deficits in verbal working memory can be
attributed to lesions in the region of posterior parietal cortex and
surrounding tissues, although these lesions are uniformly in left
hemisphere, whereas we find activations in both hemispheres (Warrington
et al., 1971; Saffran and Marin, 1975; Shallice and Vallar, 1990). The
neuroimaging and neuropsychological evidence thus appears to converge
on the conclusion that posterior parietal cortex plays a role in the
storage of verbal information in working memory. In addition, perhaps,
there may also be posterior parietal involvement in attentional
mechanisms used in working memory, mechanisms that may be necessary as
part of rehearsal processes.
These conclusions expand on the report by Fiez et al. (1996) in an
important way. The circuitry for verbal working memory that was
documented by these authors, we surmise, was largely a function of the
storage of semantically rich words, unlike the nonwords that we used
exclusively in our experiment 3. With such materials, a phonological
storage strategy may not play a particularly prominent role; rather,
subjects may rely more on semantic codes for the words to store them in
working memory. Perhaps then, this implicates posterior parietal
mechanisms in the storage of phonological codes in verbal working
memory, with nonphonological codes for verbal materials relying on
other brain structures. Although there is not a great deal of
behavioral evidence to support the use of semantic codes in verbal
working memory, there is some evidence (Shulman, 1971) suggesting at
least that such codes are possible. Thus, we are left with the
conclusion that verbal working memory may be mediated by either
phonological or semantic storage and that the role of posterior
parietal cortex may hinge on the use of phonological coding.
| |
FOOTNOTES |
Received Oct. 17, 1997; revised April 8, 1998; accepted April 9, 1998.
This work was supported in part by a grant from the Office of Naval
Research and by a grant from the National Institute on Aging, both to
the University of Michigan. We thank David Badre, Anna Cianciolo, and
Leon Gmeindl for their help in data collection and data analysis.
Correspondence should be addressed to Dr. John Jonides, Department of
Psychology, University of Michigan, 525 East University Avenue, Ann
Arbor, MI 48109-1109.
| |
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Top
Abstract
Introduction
