 |
 Previous Article | Next Article 
The Journal of Neuroscience, October 1, 2002, 22(19):8720-8725
Transient Storage of a Tactile Memory Trace in Primary
Somatosensory Cortex
Justin A.
Harris1,
Carlo
Miniussi2,
Irina M.
Harris1, and
Mathew E.
Diamond1
1 Cognitive Neuroscience Sector, International School
for Advanced Studies (SISSA), Trieste 34014, Italy, and
2 Clinical Neurophysiology Laboratory, Istituto di Ricovero
e Cura a Carattere Scientifico San Giovanni di Dio, 25125 Brescia, Italy
 |
ABSTRACT |
Working memory is known to involve prefrontal cortex and posterior
regions of association cortex (e.g., the inferior temporal lobes).
Here, we investigate the potential role of primary somatosensory cortex
(SI) in a working memory task with tactile stimuli. Subjects were
required to compare the frequencies of two vibrations separated by a
retention interval of 1500 msec. Their performance was significantly disrupted when we delivered a pulse of transcranial magnetic
stimulation (TMS) to the contralateral SI early (300 or 600 msec) in
the retention interval. TMS did not affect tactile working memory if
delivered to contralateral SI late in the retention interval (at 900 or 1200 msec), nor did TMS affect performance if delivered to the ipsilateral SI at any time point. Primary sensory cortex thus seems to
act not only as a center for on-line sensory processing but also as a
transient storage site for information that contributes to working memory.
Key words:
somatosensory cortex; working memory; flutter vibration; transcranial magnetic stimulation; immediate memory; somatotopic
| |
INTRODUCTION |
Working memory refers to the ability
to hold and manipulate information for short periods (on the order of
seconds) and to update the information as required by moment-to-moment
demands. As such, it plays an important role in many cognitive
processes, functioning as an interface between perception, attention,
memory, and action (Baddeley, 1996 ). Studies investigating the neural basis of working memory have uncovered an important role for prefrontal cortex in the executive monitoring of mnemonic information. For example, brain imaging studies in humans and electrophysiological recordings in monkeys have shown that populations of neurons in the
prefrontal cortex become active while subjects perform working memory
tasks (for review, see Goldman-Rakic, 1996; Ungerleider et al., 1998;
Fuster, 2001), and lesions to areas of prefrontal cortex disrupt
working memory function (for review, see Petrides, 2000b). Similar
experimental approaches have provided evidence that posterior regions
of cortex, such as the inferior temporal lobe, also contribute to
working memory, possibly as one location where information is
maintained during the retention period (Fuster and Jervey, 1981;
Miyashita and Chang, 1988; Postle et al., 1999; Petrides, 2000a).
Working memory for perceptual information has thus come to be viewed as
a process in which multiple, widely distributed cortical regions
interact to hold a memory trace across short delays (Fuster, 2001).
Recent findings suggest that primary sensory cortex may also be part of
this network when the task requires retention of information of a
sensory rather than semantic or categorical quality. Specifically,
several studies with monkeys have observed neuronal activity in primary
somatosensory (SI) or visual (VI) cortex that is correlated with
working memory for tactile or visual information (Zhou and Fuster,
1996, 2000; Super et al., 2001). We have obtained psychophysical
evidence consistent with a role for SI in tactile working memory in
humans (Harris et al., 2001b). Here, we describe two experiments that
test the proposal that neuronal activity in primary sensory cortex can constitute an essential part of the short-term memory trace.
In both experiments, human subjects were required to perform a working
memory task in which they compared two vibrotactile stimuli. Experiment
1 examined whether subjects were more accurate when the two stimuli
were presented to the same finger versus when they were presented to
fingers on different hands. This would imply a role for SI, because
neurons in SI have receptive fields confined to the contralateral side
of the body (Penfield and Rasmussen, 1950; Maldjian et al., 1999;
Francis et al., 2000; Shoham and Grinvald, 2001), and the hand
representation in area 3b of SI is acallosal (Jones and Powell,
1969; Killackey et al., 1983) and therefore could not support
comparisons across the body midline. To test directly whether SI
contributes to the vibrotactile working memory task, experiment 2 examined the effect of applying transcranial magnetic stimulation (TMS)
to SI. TMS disrupts ongoing neuronal activity in a localized area of
cortex by briefly inducing an electrical field in the tissue below the
magnetic coil. The timing of stimulation can be varied during the
execution of a task to demonstrate the time course of the involvement
of a specific cortical area in that cognitive process (Hallett, 2000;
Pascual-Leone et al., 2000). Because we were interested to know when SI
contributes to tactile working memory, we applied TMS at different
times across the retention interval (Fig.
1).
View larger version (40K):
[in this window]
[in a new window]
|
Figure 1.
Summary of the procedure for experiments using
TMS. Subjects felt two 1000-msec-long vibrations, separated by a 1500 msec retention interval during which they received a single pulse of
TMS. TMS was delivered either 300, 600, 900, or 1200 msec after the end
of the first vibration (1200, 900, 600, or 300 msec before the start of
the second vibration). TMS was applied to the left or right SI, and the
vibrations were presented to the left or right index finger. Thus, on
half the trials TMS was applied to the SI contralateral to the
vibrations, and on the remaining trials, TMS was applied ipsilateral to
the vibrations.
|
|
| |
MATERIALS AND METHODS |
Experiment 1. We asked eight right-handed subjects
(five men and three women) between 23 and 34 years of age (mean, 27 years) to compare the frequency of two vibrations delivered to a
fingertip. The vibrations were produced using piezoelectric wafers
(Morgan Matroc, Bedford, OH) individually driven by 80 V pulses from
custom-built amplifiers controlled by a computer running LabVIEW
(National Instruments, Austin, TX). For a detailed description of the
apparatus, see Harris et al. (2001b). Each vibration was 1000 msec long
and consisted of a square wave of fixed amplitude (250 µm) and rise time (5 msec). The frequency, measured as the number of deflections per
second, was always an even number in the range of 16-24 Hz. The
frequency of the two vibrations to be evaluated always differed by 2 Hz, but the specific frequencies varied across trials, forcing subjects
to compare the two vibrations rather than make a categorical judgment
about one of them (Hernández et al., 1997).
The two vibrations were separated by an interval of 300, 600, 900, or
1200 msec. There were 80 trials for each retention interval (a total of
320 trials in the experiment). On half of these trials (40 per
interval), the two vibrations were presented to the same index finger
(both on the left or both on the right, counterbalanced), and on the
remaining trials they were presented to opposite index fingers (left
followed by right or right followed by left, counterbalanced). In each
trial, the subjects had to decide whether the second vibration was of
higher or lower frequency than the first. Trials from each of the eight
conditions (four intervals times two locations) were randomly
intermixed, and subjects did not know in advance what the next trial
would be. Because neurons in SI have unilateral receptive fields
(Penfield and Rasmussen, 1950; Maldjian et al., 1999; Francis et al.,
2000; Shoham and Grinvald, 2001), a role for SI can be inferred if
subjects are more accurate with same-finger comparisons than
opposite-finger comparisons. In contrast, equivalent performance would
imply an exclusive role for cortical areas, such as the secondary
somatosensory cortex (SII), that possess bilateral receptive fields and
strong callosal connections and thus can support comparisons across the
body midline (Whitsel et al., 1969; Robinson and Burton, 1980;
Killackey et al., 1983; Francis et al., 2000; Disbrow et al., 2001;
Ruben et al., 2001).
Experiment 2. We tested 14 right-handed subjects (11 men and
3 women) between 23 and 38 years of age (mean, 31 years). They compared
the frequency of two vibrations presented to the same finger, either
both on the left index finger or both on the right index finger (for
summary of the experimental design, see Fig. 1). The vibrations were
separated by 1500 msec. During this retention interval, a single 0.25 msec pulse of TMS was delivered to the hand area of SI. Because we were
interested to know when SI contributes to holding the tactile working
memory trace, we used TMS to track its involvement at different times
(for a summary of the experiment, see Fig. 1). To this end, we
delivered single TMS pulses at discrete time points (300, 600, 900, and
1200 msec) after the end of the first vibration. We chose not to use
repetitive TMS (which consists of a train of magnetic pulses) because a
single pulse affords much more precise temporal resolution. TMS was
delivered using a Magstim (Whitland, UK) rapid magnetic
stimulator with a figure-eight (double 70 mm) coil, which can
induce a maximum magnetic field of 2.2 tesla at the scalp site.
Individual resting excitability thresholds of stimulation were
previously determined by stimulating the left motor cortex and
measuring the amplitude of contractions evoked in the contralateral
first interosseus dorsalis muscle by a single TMS pulse. During all
subsequent experimental trials, the stimulation intensity was set at
110% of this threshold for each subject. The mean intensity used
during the experiments was 69% of maximal output, well within safety
guidelines issued by the National Institute of Neurological Disorders
and Stroke (Wassermann, 1998).
The appropriate location for stimulating the hand area of SI was
identified for each subject as the site at which tactile extinction
could be most readily obtained. Thus, before beginning the experimental
trials, the subject performed a tactile detection task while single TMS
pulses were delivered at different positions ~5 mm posterior to the
position at which the motor excitability threshold was obtained. The
subject sat with each index finger resting on a piezoelectric wafer,
and in each trial, a single 4 msec deflection was presented at one or
both wafers (the amplitude of the deflection was set just above the
subject's detection threshold, determined earlier). The subject stated
whether he or she felt a deflection on the left finger, right finger,
or both fingers. On each trial, a single TMS pulse was presented
exactly 20 msec after the deflection, at which time it should disrupt
tactile detection (Cohen et al., 1991). By moving the coil between
trials, we were able to determine the position and orientation of the coil at which the TMS most reliably interfered with the detection task.
The typical position of the virtual cathode of the coil was
approximately over C3/C4 in the International 10/20 EEG system, with
the handle pointing toward the posterior midline. Once SI was located,
the coil was held fixed in this position by an articulated mechanical
arm for the 80 trials of the experimental block.
To reduce the number of TMS pulses delivered to each individual, the
experiment was split across two equal groups of subjects: for seven
subjects, TMS was delivered either 300 or 1200 msec after the end of
the first vibration; for the other seven subjects, TMS was delivered
600 or 900 msec after the first vibration. In one block of 80 trials,
the TMS coil was positioned over the left SI, and the vibrations were
presented to the contralateral or ipsilateral index finger (40 trials
of each, randomly intermixed within each block). In a separate block of
80 trials, the coil was positioned over the right SI, and again
vibrations were presented to the contralateral or ipsilateral finger.
The order of the two blocks was counterbalanced between subjects. Thus,
each subject was tested with 80 trials in which TMS was delivered
contralateral to the vibration and 80 trials in which TMS was
ipsilateral to the vibration. In half of these trials, TMS was
delivered early in the retention interval (either 300 or 600 msec), and
in the other half of the trials, TMS was delivered late in the interval (900 or 1200 msec); again, trials of each type were randomly
intermixed. Therefore, each subject received 40 trials in each of the
four experimental conditions (early versus late times contralateral versus ipsilateral).
Those subjects tested with TMS at 300 versus 1200 msec were given an
additional block of 80 trials with "sham" stimulation in which the
coil was positioned over the posterior midline, 10 cm from the
stimulation sites over SI, corresponding to Pz in the
International 10/20 EEG system. The coil was held at a 45° angle to
the skull so that most of the magnetic field would miss the brain but
still produce a scalp sensation, and TMS was delivered at 300 or 1200 msec into the retention interval. The order of this block relative to
the other two was counterbalanced across subjects.
In both experiments, the recruitment of subjects and all experimental
protocols were conducted in accordance with the Declaration of Helsinki
and were approved by the institutional Bioethics Committee.
| |
RESULTS |
Experiment 1
As shown in Figure 2, the subjects'
accuracy was above chance for all conditions (p < 0.0001, two-tailed Z test). However, for the shorter
retention intervals (300 and 600 msec), their accuracy was
significantly higher when the two vibrations were presented to the same
finger than when they were presented to opposite fingers
(p = 0.014 and 0.002 for 300 and 600 msec
intervals, respectively, by two-tailed paired Student's t
test). Indeed, whereas accuracy with same-finger comparisons was
~30% above the level expected by chance (50% correct), accuracy for
opposite-finger comparisons was only ~20% above chance. This 10%
difference in accuracy represents a 33% drop in performance (as a
proportion of the accuracy level for single-finger comparisons). We
interpret this to mean that at the 300 and 600 msec time points, the
memory trace was distributed across both SII (which would allow
opposite-finger comparisons) and SI (which would favor same-finger
comparisons). In contrast, when the retention interval was 900 or 1200 msec, the subjects were equally accurate when comparing vibrations
delivered to opposite fingers and when comparing vibrations delivered
to the same finger (p = 0.73 and 0.69 for 900 and 1200 msec intervals, respectively, by two-tailed paired Student's
t test). The fact that the initial advantage in making
same-finger comparisons disappeared suggests that by 900 msec into the
retention interval, no part of the memory trace remained in SI but
rather was still held in a cortical area (e.g., SII), where neurons
represent tactile stimuli bilaterally. To directly test the hypothesis
that tactile information is transiently stored in SI, experiment 2 examined the effect of applying TMS to SI while subjects performed the
vibrotactile working memory task.
View larger version (17K):
[in this window]
[in a new window]
|
Figure 2.
Results of experiment 1, in which subjects
compared two vibrations separated by a retention interval of 300, 600, 900, or 1200 msec. At all intervals, performance was above chance for
vibrations presented both on the same side and on opposite sides.
However, at the shorter intervals, the subjects were significantly more
accurate when the two vibrations were presented on the same side than
on different sides (p < 0.05). There
was no such laterality effect at the longer intervals. Error bars
indicate SEM.
|
|
Experiment 2
Because tactile stimuli are processed by the contralateral, but
not ipsilateral, SI (Penfield and Rasmussen, 1950; Cohen et al., 1991;
Maldjian et al., 1999; Francis et al., 2000; Shoham and Grinvald,
2001), we hypothesized that the working memory trace would likewise be
held in contralateral SI only. TMS therefore would be expected to
affect tactile working memory only when applied contralateral to the
stimulus site. Consistent with this model, we found that subjects'
accuracy was high during ipsilateral SI stimulation at all time points
(between 77 and 81% correct). Indeed, performance with ipsilateral TMS
was no different (p > 0.75) from performance
with a sham TMS procedure in which the pulse was delivered, at either
300 or 1200 msec into the retention interval, to a site on the midline
posterior to SI (here, performance ranged from 76 to 80% correct).
Thus, as predicted, disrupting ongoing neuronal activity in the
ipsilateral SI did not affect the working memory trace of a tactile stimulus.
In contrast, TMS applied to the contralateral SI did disrupt working
memory (accuracy ranged from 70 to 78% correct). To illustrate the
time course of this effect, we calculated for each subject the
difference in accuracy between trials on which TMS was applied to the
contralateral versus the ipsilateral SI. As shown in Figure 3, these difference scores make it clear
that the subjects' accuracy was significantly reduced when TMS was
applied to the contralateral SI early in the retention interval
(z = 4.56, p < 0.00001, for TMS at 300 msec; z = 2.34, p < 0.01, for TMS at
600 msec). The effect was primarily confined to this time
window, because it was no longer statistically reliable when TMS was
delivered 900 msec into the retention interval (z = 1.01; p = 0.16), and there was no effect at all when
TMS was applied late in the interval (at 1200 msec, z =  0.22, p = 0.59). Thus, tactile working memory was
susceptible to disturbance of the contralateral SI across the same
interval during which an SI contribution to the task had been inferred
from the preceding psychophysical experiment.
View larger version (17K):
[in this window]
[in a new window]
|
Figure 3.
Effects of TMS on vibration discrimination in
experiment 2. The plot shows the mean difference in accuracy between
trials in which TMS was applied to the contralateral SI and trials in
which TMS was applied to the ipsilateral SI. This difference score is
significantly below zero when TMS was delivered 300 or 600 msec into
the 1500 msec retention interval, but not when TMS was delivered 900 or
1200 msec into the interval. Therefore, TMS disrupted performance when
applied to the contralateral SI in the first half of the retention
interval. Error bars indicate SEM.
|
|
The size of effect of TMS on performance is best illustrated by
considering accuracy relative to the chance level (50% correct). When
TMS was delivered at 300 msec, the subjects' accuracy was 29% above
chance with ipsilateral TMS ("baseline" performance), but it was
only 20% above chance with contralateral TMS. This difference in
accuracy represents an effective drop in performance of 30% (a 9%
decrease relative to the baseline score of 29% above chance).
Similarly, when TMS was presented at 600 msec, accuracy was 31% above
chance with ipsilateral stimulation but 24% above chance
with contralateral stimulation (a drop of 23%).
To what extent are the results from the two experiments comparable? If
we speculate that the TMS pulse used in experiment 2 eliminated the
contribution of SI to working memory, then the resulting performance
level should be similar to that in experiment 1 for comparison of
opposite-finger stimuli, because SI neurons would be unable to
contribute to comparisons across the body midline. In agreement with
this reasoning, we note that in experiment 1 at delay intervals of 300 and 600 msec, opposite-finger comparisons were ~33% less accurate
than same-finger comparisons, a drop in performance equivalent to that
produced by TMS to the contralateral SI in experiment 2.
| |
DISCUSSION |
We performed two experiments to explore which cortical regions
might participate in tactile working memory. Experiment 1 showed that,
for short delay intervals (300 or 600 msec), the subjects' performance
in comparing two vibrations was ~33% better when both stimuli were
delivered to the same fingertip than to opposite fingers, indicating
that some component of the comparison depended on an area with strictly
unilateral receptive fields, such as SI. Experiment 2 showed that
disruption of SI functioning early in the delay period (at 300 or 600 msec) interfered with subsequent working memory performance by ~30%.
Therefore, experiments using topography and direct interference by TMS
independently lead to the same estimate of when, and by how much, SI
contributes to the working memory task.
Neurons in SI respond to low-frequency vibrations by firing in phase
with each cycle of the stimulus (Mountcastle et al., 1969, 1990;
Hernández et al., 2000; Salinas et al., 2000). Electrical stimulation of SI neurons at a particular frequency produces sensations that monkeys treat as identical to a mechanical vibration of that frequency (Romo et al., 1998, 2000), indicating that SI activity composes an important part of the explicit representation of the vibration. Furthermore, some recent studies have reported that in
working memory tasks, neuronal activity in primary sensory cortex can
be maintained during the retention interval between two stimuli (Zhou
and Fuster, 1996, 2000; Super et al., 2001). The observed correlations
between neuronal activity and working memory have led to the inference
that maintained neuronal responses may constitute the neural substrate
of the working memory trace itself. Here, we have strengthened this
proposal by showing that neuronal activity in sensory cortex not only
accompanies working memory but also is essential to optimal tactile
working memory performance.
Although the results of experiment 1 are consistent with the argument
that SI initially contributes to the tactile memory, they could also be
interpreted as reflecting a time lag in the shift of attention between
hands. Specifically, difficulty in disengaging attention from the
finger at which the first vibration was applied could be put forward to
explain the subjects' poorer performance on short-interval trials when
the two vibrations were presented to opposite fingers. However, recent
research indicates that this is not a satisfactory explanation. In
light of the effect known as "inhibition of return," whereby people
are faster in detecting a tactile cue if it has been preceded by a
contralateral cue than if preceded by an ipsilateral one (Röder
et al., 2002), the results obtained in experiment 1 would appear to be
in spite of attentional effects, rather than because of them.
The effects of TMS reported here cannot be attributed to a direct
disruption of SI sensory processing, because TMS applied to the
contralateral SI is known to affect processing of tactile stimuli only
if delivered within 200 msec of the onset or offset of the stimulus
(Cohen et al., 1991). We found diminished working memory performance
when TMS was delivered 300 or 600 msec after the end of the first
vibration, well outside the time window in which TMS can affect ongoing
sensory processing by SI. Indeed, to argue that sensory processing of
the vibration in SI was still taking place >300 msec after the first
vibration would imply difficulty in comparing vibrations separated by
such short retention intervals. The results of experiment 1 show that
this is not the case, meaning that the representation of a vibration is
fully established within 300 msec.
There are numerous reports suggesting that TMS can have long-range
actions, affecting neuronal activity in areas that receive projections
from the stimulated zone (Paus et al., 1997; Civardi et al., 2001;
Strafella et al., 2001; Münchau et al., 2002). In our experiment,
was the effect of TMS on tactile working memory the result of a
disruption of neuronal activity in SII, the principal downstream target
of SI? Although we cannot completely rule out this possibility, there
are several arguments against it. First, if SI TMS affected the SII
targets of the stimulated site, we would expect to find diminished
performance for stimulation of SI ipsilateral to the tactile stimulus
site, given that SI projects to both ipsilateral and contralateral SII
(Manzoni, 1984). Instead, our experiment showed that the effect of TMS
was unilateral, confined to SI contralateral to the tactile stimulus.
Second, the effect of TMS was limited to the first 600 msec of the
retention interval, corresponding to the time at which subjects were
more accurate at comparing vibrations delivered to the same hand than
different hands. Indeed, the degree to which TMS affected accuracy
matched the difference in accuracy observed for same hand versus
different hand comparisons. Thus, the tactile working memory was
susceptible to SI TMS during the same interval, and to the same extent,
that a separate measure, the topographic distribution, points toward an
SI role. Thus, the most parsimonious interpretation of both sets of
data is in terms of a role for SI in the task.
We believe that the results are best explained as a disruption of
working memory: TMS interfered with the neural mechanisms that support
the memory trace of the first vibration. The results thus provide
direct support for the claim that a component of the working memory
trace for tactile events resides in contralateral SI. Moreover, they
show that SI contributed to maintenance of the memory trace for only a
limited time (<1 sec), after which the perceptual record appears to
have been held beyond this area. Although the present data cannot
specify the storage sites outside SI, we emphasize that even across
longer delays (1-2 sec), tactile working memory was topographically
organized: performance in comparing two vibrations was better when the
stimuli were delivered to the same finger, opposite fingers, or
neighboring fingers than to fingers separated by greater distances
(Harris et al., 2001b). For this reason, we propose that under our
experimental conditions the tactile memory trace is initially
distributed across both SI and SII but is subsequently limited to SII.
This model is illustrated in Figure
4.
View larger version (36K):
[in this window]
[in a new window]
|
Figure 4.
Diagrams showing possible neuronal mechanisms
involved in working memory for vibrotactile stimuli. During delivery of
the first vibration to a fingertip (phase i), the
frequency of the vibration is encoded by the firing rate or firing
pattern of populations of neurons in primary and secondary
somatosensory cortex (SI and SII).
SI neurons fire in phase with the indentation cycle of the vibration,
whereas the firing rate of neurons in SII is a monotonic (increasing or
decreasing) function of the vibration frequency. Both patterns are
depicted here by peristimulus time histograms of neuronal activity, as
reported by Salinas et al. (2000). Across the retention interval,
subjects must remember the frequency of the first vibration to compare
it with the second vibration. We propose that this memory trace is
supported initially by ongoing neuronal activity in both SI and SII
(phase ii), but by 900 msec into the interval
(phase iii), the memory is no longer held in SI.
Populations of neurons in distinct areas of the premotor and prefrontal
cortex (PFC) also contribute to sustaining the memory
trace, especially toward the latter part of the retention interval
(Romo et al., 1999; Hernández et al., 2002).
|
|
What is the nature of the transient memory in SI? One potential account
holds that SI maintains an immediate sensory memory, such as the
"iconic" and "echoic" memory traces described in visual and
auditory modalities (Sperling, 1960; Darwin et al., 1972; Lu et al.,
1992). This "echo," however, should not be viewed as a mere sensory
aftereffect divorced from the subsequent memory trace. First, in
experiment 1, the elevated performance of the task for same-finger
comparisons suggests that the SI memory trace was used directly in the
comparison task when the retention interval was very short. Second, in
experiment 2, disruption of the SI trace at 300 or 600 msec affected
the subsequent comparison made as long as 1500 msec later, indicating
that the immediate memory trace in SI was essential for the formation
of the longer-lasting memory.
Some discrepant observations must be reconciled before the role of SI
in tactile working memory can be fully understood. The neural circuits
underlying working memory for vibrotactile stimuli have been
investigated in detail by Romo et al. (1999), Salinas et al. (2000),
Romo and Salinas (2001), and Hernández et al. (2002) in a series
of electrophysiological recording studies with monkeys. These authors
have identified populations of neurons in SII, the prefrontal cortex,
and premotor cortical areas the activity of which differentially
encodes the frequency of the first vibration and that sustain this
differential activity across the retention interval. However, they did
not observe sustained activity among neurons in SI (Salinas et al.,
2000), leading them to conclude that neurons in SI do not participate
in maintaining the vibrotactile working memory trace. This disagreement
with our conclusions may be a result of procedural differences. The monkeys studied by Romo and colleagues were given several months of
training on the task, whereas our human subjects were given no previous
training at all. Intensity of training could influence the neural
mechanisms of working memory. For example, during the course of
extensive training given to the monkeys, the temporal entrainment of
the SI stimulus representations might have improved (Recanzone et al.,
1992a,b), allowing a faster or more efficient transfer of information
to "later" cortical areas, such as SII. The contribution of SI to
working memory might diminish under these conditions. Additional work
will be required to determine whether SI plays a major role in storing
information about unfamiliar stimuli and a lesser role in well
rehearsed stimuli.
In conclusion, although early sensory cortical areas are commonly
viewed as contributing only to the on-line processing and representation of sensory events, the present findings add to a growing
body of evidence that these areas also constitute important components
of the networks subserving perceptual learning and short- and long-term
memory more generally (Kosslyn et al., 2001). As such, they are
consistent with a model in which the populations of cortical neurons
that explicitly encode sensory information also store that information
for subsequent use (Fuster, 2001; Harris et al., 2001a).
| |
FOOTNOTES |
Received July 8, 2002; revised July 2, 2002; accepted July 11, 2002.
This study was supported by a fellowship from the Italian Ministry of
Universities and Scientific and Technological Research (J.A.H.) and
grants from the Telethon Foundation, Consiglio Nazionale delle
Ricerche, Ministero della Sanità, Ministero dell'Istruzione, Università e Ricerca, and the James S. McDonell Foundation.
Correspondence should be addressed to Dr. Justin Harris,
School of Psychology, University of Sydney, New South Wales 2006, Australia. E-mail: justinh{at}psych.usyd.edu.au.
| |
REFERENCES |
-
Baddeley A
(1996)
The fractionation of working memory.
Proc Natl Acad Sci USA
93:13468-13472[Abstract/Free Full Text].
-
Civardi C,
Cantello R,
Asselman P,
Rothwell JC
(2001)
Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans.
NeuroImage
14:1444-1453[Web of Science][Medline].
-
Cohen LG,
Bandinelli S,
Sato S,
Kufta C,
Hallett M
(1991)
Attenuation in detection of somatosensory stimuli by transcranial magnetic stimulation.
Electroencephalogr Clin Neurophysiol
81:366-376[Web of Science][Medline].
-
Darwin CT,
Turvey MT,
Crowder RG
(1972)
An auditory analogue of the Sperling partial report procedure: evidence for brief auditory storage.
Cognit Psychol
3:255-267.
-
Disbrow E,
Roberts T,
Poeppel D,
Krubitzer L
(2001)
Evidence for interhemispheric processing of inputs from the hands in human S2 and PV.
J Neurophysiol
85:2236-2244[Abstract/Free Full Text].
-
Francis ST,
Kelly EF,
Bowtell R,
Dunseath WJ,
Folger SE,
McGlone F
(2000)
fMRI of the responses to vibratory stimulation of digit tips.
NeuroImage
11:188-202[Web of Science][Medline].
-
Fuster JM
(2001)
The prefrontal cortex: an update: time is of the essence.
Neuron
30:319-333[Web of Science][Medline].
-
Fuster JM,
Jervey JP
(1981)
Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli.
Science
212:952-955[Abstract/Free Full Text].
-
Goldman-Rakic PS
(1996)
Regional and cellular fractionation of working memory.
Proc Natl Acad Sci USA
93:13473-13480[Abstract/Free Full Text].
-
Hallett M
(2000)
Transcranial magnetic stimulation and the human brain.
Nature
406:147-150[Medline].
-
Harris JA,
Petersen RS,
Diamond ME
(2001a)
The cortical distribution of sensory memories.
Neuron
30:315-318[Medline].
-
Harris JA,
Harris IM,
Diamond ME
(2001b)
The topography of tactile working memory.
J Neurosci
21:8262-8269[Abstract/Free Full Text].
-
Hernández A,
Salinas E,
Garcia R,
Romo R
(1997)
Discrimination in the sense of flutter: new psychophysical measurements in monkeys.
J Neurosci
17:6391-6400[Abstract/Free Full Text].
-
Hernández A,
Zainos A,
Romo R
(2000)
Neuronal correlates of sensory discrimination in the somatosensory cortex.
Proc Natl Acad Sci USA
97:6191-6196[Abstract/Free Full Text].
-
Hernández A,
Zainos A,
Romo R
(2002)
Temporal evolution of a decision-making process in medial premotor cortex.
Neuron
33:959-972[Web of Science][Medline].
-
Jones EG,
Powell TP
(1969)
Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions.
Brain
92:717-730[Free Full Text].
-
Killackey HP,
Gould HJ,
Cusick III CG,
Pons TP,
Kaas JH
(1983)
The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys.
J Comp Neurol
219:384-419[Web of Science][Medline].
-
Kosslyn SM,
Ganis G,
Thompson WL
(2001)
Neural foundations of imagery.
Nat Rev Neurosci
2:635-642[Web of Science][Medline].
-
Lu Z-L,
Williamson SJ,
Kaufman L
(1992)
Behavioral lifetime of human auditory sensory memory predicted by physiological measures.
Science
258:1668-1670[Abstract/Free Full Text].
-
Maldjian JA,
Gottschalk A,
Patel RS,
Detre JA,
Alsop DC
(1999)
The sensory somatotopic map of the human hand demonstrated at 4T.
NeuroImage
10:55-62[Web of Science][Medline].
-
Manzoni T
(1984)
Callosal mechanism for the interhemispheric transfer of hand somatosensory information in the monkey.
Behav Brain Res
11:155-170[Web of Science][Medline].
-
Miyashita Y,
Chang HS
(1988)
Neuronal correlate of pictorial short-term memory in the primate temporal cortex.
Nature
331:68-70[Medline].
-
Mountcastle VB,
Talbot WH,
Sakata H,
Hyvarinen J
(1969)
Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys: neuronal periodicity and frequency discrimination.
J Neurophysiol
32:452-484[Free Full Text].
-
Mountcastle VB,
Steinmetz MA,
Romo R
(1990)
Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys.
J Neurosci
10:3032-3044[Abstract].
-
Münchau A,
Bloem BR,
Irlbacher K,
Trimble MR,
Rothwell JC
(2002)
Functional connectivity of human premotor and motor cortex explored with repetitive transcranial magnetic stimulation.
J Neurosci
22:554-561[Abstract/Free Full Text].
-
Pascual-Leone A,
Walsh V,
Rothwell J
(2000)
Transcranial magnetic stimulation in cognitive neuroscience: virtual lesion, chronometry, and functional connectivity.
Curr Opin Neurobiol
10:232-237[Web of Science][Medline].
-
Paus T,
Jech R,
Thompson CJ,
Comaeu R,
Peters TM,
Evbans AC
(1997)
Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex.
J Neurosci
17:3178-3184[Abstract/Free Full Text].
-
Penfield W,
Rasmussen T
(1950)
In: The cerebral cortex of man: a clinical study of localization of function. New York: Hafner.
-
Petrides M
(2000a)
Dissociable roles of mid-dorsolateral prefrontal and anterior inferotemporal cortex in visual working memory.
J Neurosci
20:7496-7503[Abstract/Free Full Text].
-
Petrides M
(2000b)
The role of the mid-dorsolateral prefrontal cortex in working memory.
Exp Brain Res
133:44-54[Web of Science][Medline].
-
Postle BR,
Berger JS,
D'Esposito MD
(1999)
Functional neuroanatomical double dissociation of mnemonic and executive control processes contributing to working memory performance.
Proc Natl Acad Sci USA
96:12959-12964[Abstract/Free Full Text].
-
Recanzone GH,
Merzenich MM,
Jenkins WM,
Grajski KA,
Dinse HR
(1992a)
Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task.
J Neurophysiol
67:1031-1056[Abstract/Free Full Text].
-
Recanzone GH,
Merzenich MM,
Schreiner CE
(1992b)
Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task.
J Neurophysiol
67:1071-1091[Abstract/Free Full Text].
-
Robinson CJ,
Burton H
(1980)
Somatotopographic organization in the second somatosensory area of M. fascicularis.
J Comp Neurol
192:43-67[Web of Science][Medline].
-
Röder B,
Spence C,
Rösler F
(2002)
Assessing the effect of posture change on tactile inhibition-of-return.
Exp Brain Res
143:453-462[Web of Science][Medline].
-
Romo R,
Salinas E
(2001)
Touch and go: decision-making mechanisms in somatosensation.
Annu Rev Neurosci
24:107-137[Web of Science][Medline].
-
Romo R,
Hernández A,
Zainos A,
Salinas E
(1998)
Somatosensory discrimination based on cortical microstimulation.
Nature
392:387-390[Medline].
-
Romo R,
Brody CD,
Hernández A,
Lemus L
(1999)
Neuronal correlates of parametric working memory in the prefrontal cortex.
Nature
399:470-473[Medline].
-
Romo R,
Hernández A,
Zainos A,
Brody CD,
Lemus L
(2000)
Sensing without touching: psychophysical performance based on cortical microstimulation.
Neuron
26:273-278[Web of Science][Medline].
-
Ruben J,
Schwiemann J,
Deuchert M,
Meyer R,
Krause T,
Curio G,
Villringer K,
Kurth R,
Villringer A
(2001)
Somatotopic organization of human secondary somatosensory cortex.
Cereb Cortex
11:463-473[Abstract/Free Full Text].
-
Salinas E,
Hernández A,
Zainos A,
Romo R
(2000)
Periodicity and firing rate as candidate neural codes for the frequency of vibrotactile stimuli.
J Neurosci
20:5503-5515[Abstract/Free Full Text].
-
Shoham D,
Grinvald A
(2001)
The cortical representation of the hand in macaque and humans S-I: high resolution optical imaging.
J Neurosci
21:6820-6835[Abstract/Free Full Text].
-
Sperling G (1960) The information available in brief visual
presentations. Psychol Monogr 74: No. 498.
-
Strafella AP,
Paus T,
Barrett J,
Dagher A
(2001)
Repetitive transcranial magnetic stimulation of the human cerebral cortex induces dopamine release in the caudate nucleus.
J Neurosci
21:RC157[Abstract/Free Full Text].
-
Super H,
Spekreijse H,
Lamme VAF
(2001)
A neural correlate of working memory in the monkey primary visual cortex.
Science
293:120-124[Abstract/Free Full Text].
-
Ungerleider LG,
Courtney AM,
Haxby JV
(1998)
A neural system for human visual working memory.
Proc Natl Acad Sci USA
95:883-890[Abstract/Free Full Text].
-
Wassermann EM
(1998)
Risk and safety of repetitive transcranial magnetic stimulation: report on suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation.
Electroencephalogr Clin Neurophysiol
108:1-16[Medline].
-
Whitsel BL,
Petrucelli LM,
Werner G
(1969)
Symmetry and connectivity in the map of the body surface in somatosensory area II of primates.
J Neurophysiol
32:170-183[Free Full Text].
-
Zhou YD,
Fuster JM
(1996)
Mnemonic neuronal activity in somatosensory cortex.
Proc Natl Acad Sci USA
93:10533-10537[Abstract/Free Full Text].
-
Zhou YD,
Fuster JM
(2000)
Visuo-tactile cross-modal associations in cortical somatosensory cells.
Proc Natl Acad Sci USA
97:9777-9782[Abstract/Free Full Text].
Copyright © 2002 Society for Neuroscience 0270-6474/02/22198720-06$05.00/0
This article has been cited by other articles:
|
|
|
|
 
D. Artchakov, D. Tikhonravov, Y. Ma, T. Neuvonen, I. Linnankoski, and S. Carlson
Distracters Impair and Create Working Memory-Related Neuronal Activity in the Prefrontal Cortex
Cereb Cortex,
November 1, 2009;
19(11):
2680 - 2689.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. WENGER, A. M. COPELAND, J. L. BITTNER, and R. D. THOMAS
Evidence for criterion shifts in visual perceptual learning: Data and implications
Atten Percept Psychophys,
October 1, 2008;
70(7):
1248 - 1273.
[Abstract]
[PDF]
|
|
|
|
|
|
|
J. Pantoja, S. Ribeiro, M. Wiest, E. Soares, D. Gervasoni, N. A. M. Lemos, and M. A. L. Nicolelis
Neuronal Activity in the Primary Somatosensory Thalamocortical Loop Is Modulated by Reward Contingency during Tactile Discrimination
J. Neurosci.,
September 26, 2007;
27(39):
10608 - 10620.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. L. Kaas, H. van Mier, and R. Goebel
The Neural Correlates of Human Working Memory for Haptically Explored Object Orientations
Cereb Cortex,
July 1, 2007;
17(7):
1637 - 1649.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Kostopoulos, M.-C. Albanese, and M. Petrides
Ventrolateral prefrontal cortex and tactile memory disambiguation in the human brain
PNAS,
June 12, 2007;
104(24):
10223 - 10228.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M.-C. Albanese, E. G. Duerden, P. Rainville, and G. H. Duncan
Memory Traces of Pain in Human Cortex
J. Neurosci.,
April 25, 2007;
27(17):
4612 - 4620.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Li Hegner, R. Saur, R. Veit, R. Butts, S. Leiberg, W. Grodd, and C. Braun
BOLD Adaptation in Vibrotactile Stimulation: Neuronal Networks Involved in Frequency Discrimination
J Neurophysiol,
January 1, 2007;
97(1):
264 - 271.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Preuschhof, H. R. Heekeren, B. Taskin, T. Schubert, and A. Villringer
Neural Correlates of Vibrotactile Working Memory in the Human Brain
J. Neurosci.,
December 20, 2006;
26(51):
13231 - 13239.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Pleger, C. C. Ruff, F. Blankenburg, S. Bestmann, K. Wiech, K. E. Stephan, A. Capilla, K. J. Friston, and R. J. Dolan
Neural Coding of Tactile Decisions in the Human Prefrontal Cortex
J. Neurosci.,
November 29, 2006;
26(48):
12596 - 12601.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Zaksas and T. Pasternak
Directional Signals in the Prefrontal Cortex and in Area MT during a Working Memory for Visual Motion Task.
J. Neurosci.,
November 8, 2006;
26(45):
11726 - 11742.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. F. Goldberg, C. A. Perfetti, and W. Schneider
Perceptual knowledge retrieval activates sensory brain regions.
J. Neurosci.,
May 3, 2006;
26(18):
4917 - 4921.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Pleger, F. Blankenburg, S. Bestmann, C. C. Ruff, K. Wiech, K. E. Stephan, K. J. Friston, and R. J. Dolan
Repetitive Transcranial Magnetic Stimulation-Induced Changes in Sensorimotor Coupling Parallel Improvements of Somatosensation in Humans
J. Neurosci.,
February 15, 2006;
26(7):
1945 - 1952.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Alonso, P. Bekinschtein, M. Cammarota, M. R.M. Vianna, I. Izquierdo, and J. H. Medina
Endogenous BDNF is required for long-term memory formation in the rat parietal cortex
Learn. Mem.,
September 1, 2005;
12(5):
504 - 510.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Schwartz, F. Assal, N. Valenza, M. L. Seghier, and P. Vuilleumier
Illusory persistence of touch after right parietal damage: neural correlates of tactile awareness
Brain,
February 1, 2005;
128(2):
277 - 290.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Morgen, N. Kadom, L. Sawaki, A. Tessitore, J. Ohayon, H. McFarland, J. Frank, R. Martin, and L. G. Cohen
Training-dependent plasticity in patients with multiple sclerosis
Brain,
November 1, 2004;
127(11):
2506 - 2517.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Balslev, L. O. D. Christensen, J.-H. Lee, I. Law, O. B. Paulson, and R. C. Miall
Enhanced Accuracy in Novel Mirror Drawing after Repetitive Transcranial Magnetic Stimulation-Induced Proprioceptive Deafferentation
J. Neurosci.,
October 27, 2004;
24(43):
9698 - 9702.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
TOP
ABSTRACT
INTRODUCTION
