Brain and Cognition 56 (2004) 153–164
www.elsevier.com/locate/b&c
Physiological evidence for response inhibition in choice reaction
time tasks
Borı́s Burlea,*, Franck Vidala,b, Christophe Tandonneta, Thierry Hasbroucqa,b
a
Laboratoire de Neurobiologie de la Cognition, Centre National de la Recherche Scientifique and Université de Provence, Marseille, France
b
Institut de Médecine Navale du Service de Santé des Armées, Toulon, France
Accepted 1 June 2004
Available online 12 September 2004
Abstract
Inhibition is a widely used notion proposed to account for data obtained in choice reaction time (RT) tasks. However, this concept is weakly supported by empirical facts. In this paper, we review a series of experiments using Hoffman reflex, transcranial magnetic stimulation and electroencephalography to study inhibition in choice RT tasks. We provide empirical support for the idea that
inhibition does occur during choice RT, and the implications of those findings for various classes of choice RT models are discussed.
Ó 2004 Elsevier Inc. All rights reserved.
Keywords: Reaction time; Inhibition; Hoffman reflex; TMS; EEG; Laplacian; Models
1. Introduction
During the last 50 years, much progress has been
made in understanding basic information processing
mechanisms. This progress is intimately linked to the
development of the reaction time (RT) paradigm. Within this framework, the procedures in which the subjects
are required to choose between different response alternatives have proved to be particularly fruitful. Different
models of choice RT have been developed and tested
with behavioral techniques. All of them treat information processing as a gradual process based on the accumulation of information over time and most of them
comprise at least two processing levels: one stimulus-related level and one response-related level (e.g., McClelland, 1979). In such models, the response-related level
is made of information accumulators or integrators,
each accumulator being associated to one response alternative. In recent versions of these models, following the
Hebbian perspective (Hebb, 1949) the accumulators cor*
Corresponding author. Fax: +33 491 71 49 38.
E-mail address: [email protected] (B. Burle).
0278-2626/$ - see front matter Ó 2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.bandc.2004.06.004
respond to peculiar populations of neurons (see Usher &
McClelland, 2001). A given response is emitted as soon
as one accumulator—or the difference between two
accumulators (e.g., Spencer & Coles, 1999)—reaches a
predefined threshold. The RT of the model is a function
of the ‘‘time’’ (in model time units) necessary to reach
this threshold. Only one response being correct on a given trial, the possible responses are thus in competition
in order to reach the threshold first. The competition,
however, can take different forms. Among the various
possible implementations, the presence or absence of
inhibitory mechanisms is an important feature.
1.1. Response competition and inhibition
In its simplest form, the competition is just an accumulation-race between the different accumulators without any interference between the two accumulators:
The two accumulators are independent, and the one
that reaches the threshold first triggers the response.
This scheme (Fig. 1A) is implemented in counter models, accumulator models and some horse-race with-winner-takes-all models (Audley & Pike, 1965; Cohen,
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B. Burle et al. / Brain and Cognition 56 (2004) 153–164
Fig. 1. Schematic representation of the response accumulators level in
the various classes of models developed in the text. (A) Models without
inhibition, (B) models with lateral inhibition and (C) models with feedforward inhibition.
Dunbar, & McClelland, 1990; Laberge, 1962; Vickers,
1970, 1979).
A more refined form of competition without inhibition is implemented in ‘‘random walk’’ and diffusion related models (Ashby, 1983; Laming, 1968; Link &
Heath, 1975; Stone, 1960; Ratcliff, Van Zandt, & McKoon, 1999): In such models of two-choice RT, only one
accumulator is present with two boundaries, each of
which corresponds to an alternative response. At each
moment, the accumulator accumulates evidence for
one of the two responses, and the response is given when
the accumulation reaches one of the two thresholds.
Note that, in this second class of models, the two responses are mutually exclusive, in the sense that only
one response can be activated at each moment.
Inhibition is an intermediate variable introduced in
RT models in order to account for (i) behavioral effects
obtained in the so-called Ôconflict tasks,Õ such as EriksenÕs flanker task (Eriksen & Schultz, 1979), Simon
(Zorzi & Umiltá, 1995) and Stroop tasks (Kornblum,
Hasbroucq, & Osman, 1990) and (ii) to extend classic
models to situations with more than two response alternatives (Grossberg, 1976, 1978; McClelland & Rumelhart, 1981; Usher & McClelland, 2001). This
psychological concept has its roots in clinical and experimental physiology where it is considered as a functional
counterpart of neural activation. Importantly, neural
inhibition is defined not as an absence of excitation
but as an active process suppressing an excitatory action
(see e.g., Buser, 1984). Inhibition has essentially been
studied in the stop-signal paradigm (Logan & Cowan,
1984; Osman, Kornblum, & Meyer, 1986; van Boxtel,
van der Molen, Jennings, & Brunia, 2001; Vince,
1948). In the prototypical version of this paradigm, the
participants perform a RT task requiring the discrimination of two stimuli and the selection of one motor response. A stop-signal is presented occasionally and
unpredictably in a proportion of trials, instructing the
participant to withold his (her) response to the choice
RT stimulus. Participants usually comply with this
requirement and successfully inhibit their ongoing processing provided that the stop-signal occurs soon enough during the RT: the later the stop-signal, the
harder the response inhibition. In such tasks, unlike in
regular choice RT, inhibition can directly be quantified
through the proportion of successfully stopped responses and its time properties can be inferred (Logan
& Cowan, 1984; Osman et al., 1986). In contrast, the
choice RT models resorting to the notion of inhibition
assume that this intermediate variable lengthens, or
postpones, the execution of a given response. For instance, Eriksen and Schultz (1979) resorted to this notion in order to account for the results obtained in the
context of the flanker compatibility task (Eriksen &
Eriksen, 1974) in which the participant typically has to
make a left- or a right-hand keypress according to the
identity of a letter (A or H). This target is flanked by
noise letters on each side. The flankers are either ‘‘compatible’’ (e.g., AAA) or ‘‘incompatible’’ (e.g., HAH)
with the target. Eriksen and Schultz proposed that the
flankers automatically activate the required response
when the display is compatible and the non-required response when the display is incompatible. In the latter
case, the activated response competes with the required
response that is consequently inhibited. The more the
incorrect response is activated, the more the required response is inhibited and the longer the RT (Eriksen &
Schultz, 1979).
1.2. Feed-forward and lateral inhibition
A useful distinction has recently been proposed by
Band and van Boxtel (1999) in the context of the stopsignal paradigm. These authors distinguished the Ômanifestation,Õ the ÔagentÕ and the ÔsiteÕ of inhibition in the
stop-signal paradigm. The manifestation is the mechanism by which inhibition is effective, while the agent
can be defined as the source of inhibitory activity and
the site as the locus where the inhibition can be recorded. We shall retain this distinction to address the issue of inhibition in choice RT. In light of this
distinction, it appears that two types of inhibition assumed to mediate choice RT performance have so far
been proposed; they essentially differ by their agent.
The agent of the lateral inhibition is located at the site
of inhibition, that is at the accumulatorsÕ level (Fig.
1B). With this scheme, the accumulators only receive positive inputs from upstream levels and they inhibit each
other as a function of their positive inputs and a response is executed when the activation level of its accumulator bypasses a given pre-defined threshold. The use
of this notion of lateral inhibition is particularly well expressed by Coles, Gratton, Bashore, Eriksen, and
B. Burle et al. / Brain and Cognition 56 (2004) 153–164
Donchin (1985): ‘‘During the epoch immediately following the stimulus many responses may be in initial stages
of activation. The responses are thus in competition (cf.
reciprocal inhibition—Sherrington, 1906/1947). The
speed with which a response is executed depends, in
part, on the extent of response competition. The greater
this competition, the longer the latency of the correct response[. . .]. There is a process of response competition
by which concurrently activated responses inhibit each
other.’’ (pp. 530). A caveat regarding such an assertion
is, however, in order. Indeed, SherringtonÕs reciprocal
inhibition is a wired property of agonist and antagonist
spinal motor nuclei: When the flexors of one joint are
being excited, the extensors of the same joint are inhibited and vice versa. Since in usual RT tasks the response
alternatives very seldom involve the agonist and antagonist of the same joint, the analogy is at best a metaphor. In contrast, the agent of the feed-forward—or
top–down—inhibition (Burle, Bonnet, Vidal, Possamaı̈,
& Hasbroucq, 2002a; Heuer, 1987; Kornblum et al.,
1990; Kornblum, Stevens, Whipple, & Requin, 1999;
Sherrington, 1906/1947) is located upstream from the response accumulators: Every positive input from upstream levels to an accumulator is accompanied by a
negative input originating from the same level to the
other accumulators (Fig. 1C). The weighted sum of the
positive and negative inputs received by one accumulator determines its activation level. Like in the no-inhibition models, a response is executed when the activation
level of its accumulator reaches a given pre-defined
threshold.
1.3. Executive control and inhibition
Appropriate behavior does not always consists in making the correct response. It sometimes consists in withholding a response. This is the case in go–nogo tasks
and obviously in Stop-tasks. In those tasks, inhibition is
often considered as the main aspect of the task: The prepotent response has to be actively suppressed, or inhibited. However, the idea that incorrect responses can be
intentionally and actively suppressed has also been proposed for choice RT. Ridderinkhof (2002) analyzed in detail the RT distribution in the Simon task, by using the
delta-plot technique. Briefly, the delta-plots represent
the size of the Simon effect as a function of increasing
RT. Such an analysis revealed that the Simon effect decreases as RT is getting longer (De Jong, Liang, & Lauber, 1994). To account for this finding, Ridderinkhof
(2002) extended the dual route model of compatibility
(Kornblum et al., 1990). The main idea of the dual route
model is that, in case of the Simon task, the position (the
irrelevant dimension) of the stimulus activates (more or
less automatically) the ipsilateral response through a direct route, whereas the relevant dimension (e.g., the color)
activates the correct response through a controlled route.
155
Within this framework, Ridderinkhof (2002) proposed
that the incorrect response, activated by the irrelevant
dimension of the stimulus, can be actively suppressed,
and that such a suppression can be seen in the delta-plots.
By manipulating factors thought to change the need for
suppressing the incorrect response activation, Ridderinkhof (2002) observed correlative changes in the delta-plots
indexing changes in executive control, providing empirical support for the model. Burle, Possamaı̈, Vidal, Bonnet, and Hasbroucq (2002b) used the same logic to
better specify what is going on after ‘‘partial errors.’’
Thanks to EMG recordings, it is possible, in overt correct
trials, to detect very small EMG activities in the muscles
associated to the incorrect response. Burle et al. reasoned
that on those particular trials, given that the incorrect response was largely activated, its suppression should be
very strong. Such an inhibition was expected to be evidenced in the delta-plots. Burle et al. (2002b) observed
large negative going delta-plots, suggesting a strong inhibition of the incorrect response.
1.4. Possible agents of inhibition
Among the candidates for the agent of feed-forward
inhibition in choice RT tasks, two structures, closely related, have been proposed: The anterior cingulate cortex
and the supplementary motor area (SMA). Arguments
for locating the agent in the cingulate cortex comes
mostly from monkeys studies. Sasaki and colleagues
(Gemba & Sasaki, 1990; Sasaki, Gemba, & Tsujimoto,
1989) ran a series of experiments using go–nogo tasks,
in which the activity of the homolog of the cingulate cortex was recorded. They observed ÔNogo potentialsÕ in
this region, which they interpreted as reflecting the inhibition of the response. In a second step, they stimulated
the structure generating these Nogo potentials in the go
task. Such stimulations induced a suppression of the
motor command, providing additional argument for
an inhibitory role of this structure. In humans, with electroencephalographic (EEG) measurements, Nogo
potentials have also been observed in two components
obtained in Nogo trials: The first difference is an
enhancement of a negative component occurring about
200 ms after the nogo signal (Nogo N2), and the second
is a positive component at about 350 ms after the nogo
stimulus, both maximal at fronto-central electrodes
(Kok, 1986). Thanks to source localization techniques,
the N2 component has sometimes been located in the
anterior cingulate cortex in go–nogo tasks (Bokura,
Yamaguchi, & Kobayashi, 2001; Nieuwenhuis, Yeung,
van den Wildenberg, & Ridderinkhof, 2003) and in conflict tasks (van Veen & Carter, 2002). Correlatively, the
activation of the anterior cingulate cortex observed with
fMRI in studies of the go–nogo task has been interpreted as reflecting the haemodynamic counterpart of
the Nogo potentials recorded with EEG.
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B. Burle et al. / Brain and Cognition 56 (2004) 153–164
The SMA, a structure closely related to the cingulate
cortex, might also be a good candidate. It has often been
considered as a structure which role would essentially be
inhibitory (Goldberg, 1985; Tanji & Kurata, 1985; Vidal, Bonnet, & Macar, 1995). Among the main arguments in favor of this view are the effects of
microstimulations of the SMAs in human patients.
From the pioneering work of Penfield and Welch
(1951) (cited in Porter, 1990) it appears that for the
smallest intensities, stimulations of the SMA do not
evoke motor responses but rather suppress ongoing
movements. These data have been confirmed later by
Fried et al. (1991) for speech and Fried (1996) for the entire spectrum of motor responses tested, although the
current threshold had to be higher. In the same line,
Chauvel, Rey, Buser, and Bancaud (1996) reports that
for 225 tested SMAs in 140 patients the most frequent
effects consisted of speech or movement arrests. These
arrests corresponded to 75% of the SMAs tested. Movement inhibition was elicited significantly more often
than movements of the upper limbs. In the work of
Chauvel et al. (1996), positive (elicitation of a movement) and negative (inhibition of an ongoing movement) signs of stimulation corresponded to
overlapping sites. However, Lim et al. (1994) claimed
that they identified a sub region in the rostral part of
the SMA (that they called ‘‘supplementary negative
area’’) the stimulation of which elicited movements or
speech arrest (speech is just a complex movement). They
considered that speech arrest was mainly due to inhibition of the movements of the tongue an the other muscles used in phonation. In other words, stimulation did
not induce a transient aphasia. Although one cannot exclude that the effects of electrical stimulations might
have been to disrupt the normal functioning of the
SMA (namely generating movements), taken together,
these data from stimulation studies in humans suggest
that inhibiting motor responses is an important function
of the SMA or, at least, of one of its sub-regions.
sists in considering that inhibition reflects covert neural
processes that can eventually be revealed by neurophysiological methods. Such an approach necessary integrates the concepts and methods issued from both
experimental psychology and the neurosciences. One
experimental strategy consists in using changes in neural
activity as intermediate indices of the information processing operations executed by the nervous system so
as to implement a response in choice RT conditions.
The function of such indices is to constraint the models.
The simulations developed must account for the functional relationships between these indices and the RT.
In other words, they are submitted to a cross-validation
process that allows one to test the information processing models and to precisely specify the functional significance of the recorded neural activities (Requin, 1987).
The use of physiological indices necessitates that the
relationships between inhibition—as a psychological
concept—and the recorded neural activity are made explicit through an ‘‘indexation function’’ (Teller, 1984).
The results therefore rely on a logic derived from models
specifying how inhibition is physiologically implemented
during RT. In a psychophysiological stance, the site of
inhibition is of prime interest because (i) all RT models
locate the site of inhibition at the same level as the response accumulators that trigger response execution
and (ii) there is little doubt that the anatomical structures that trigger response execution constitute the cortico-spinal tract. Such structures were therefore
considered to be candidates for being the site of inhibition. These considerations, which constitute the indexation functions at the origin of our approach, led us to
track the site of inhibition from the muscular periphery
up to the motor cortex (Fig. 2). In this end, we successively used Hoffman reflex, transcranial magnetic stimu-
1.5. The quest for the site of inhibition
Now, although the agent of inhibition has been the
focus of several studies, much less is know about its possible sites. In a choice task, the presence of inhibition is
inferred from a difference in RT between two experimental conditions. However, most behavioral results interpreted in terms of inhibition can as well be explained
in alternative ways, and inhibition in choice RT is a
compelling theoretical construct weakly supported at
the empirical level. In other words, inhibition is insufficiently constrained to constitute a valid heuristics and,
in spite of its explanatory value, response inhibition in
choice RT has not yet received strong empirical support.
It remains in fact a theoretical notion, or in other words
a vue de lÕesprit. One way to constrain the notion con-
Fig. 2. The cortico-spinal track along with a representation of the
three techniques used in the series of experiments: H reflex, TMS and
EEG.
B. Burle et al. / Brain and Cognition 56 (2004) 153–164
lation (TMS) and electroencephalographic (EEG)
techniques.
2. The experiments
2.1. Behavioral
recordings
procedures
and
electromyographic
In all the experiments reported below, the subjects
were to respond to visual stimuli by flexing either the left
or the right thumb. The EMG activity of the response
agonists was systemically recorded by means of surface
electrodes disposed on the skin of the thenar eminences
above the flexor pollicis brevis. In the Hoffman (H) reflex experiment (Hasbroucq, Akamatsu, Burle, Bonnet,
& Possamaı̈, 2000), the stimuli were presented to the left
or right of a fixation and the stimulus-response mapping
was varied: In half the blocks, the participants had to
give a right hand response when the stimulus appeared
on the right side (and a left response to a left stimulus),
whereas on the other half of the blocks, subjects had to
use the reverse mapping (right response to left stimulus
and left response to right stimulus). In the TMS experiment (Burle et al., 2002a), the stimuli were presented at
the fixation and their color, green or red, indicated
which response to make. In the EEG experiment (Vidal,
Grapperon, Bonnet, & Hasbroucq, 2003), the subjects
were to perform a stroop-like task: The words ‘‘rouge,’’
‘‘bleu’’ and ‘‘vert’’ (red, blue and green in french,
respectively) were presented centrally in one of the three
ink-colors (red, blue or green). For each subject, one
ink-color was associated with the right response, one
with the left response, and the last one was associated
with a nogo. All the combinations were equiprobable,
leading to 33% of compatible trials, 33% of incompatible
trials and 33% of nogo trials. The reader will find the details of the experimental procedures in the above cited
papers.
157
unique synapse of the loop. Thus, the gain of the reflex
loop is cerebrally controlled by way of presynaptic inhibition and any change in reflex amplitude reflects modulations in presynaptic inhibition and originates from
supra-spinal structures. In the conducted experiment,
the reflex was elicited at different times during the RT
interval both in the muscle involved in the required response and in the muscle involved in the non-required
response. Four stimulations dates were used: 40, 80,
120, and 160 ms after stimulus presentation. Based on
RT value on each trial, those stimulation dates were
converted in date relative to the onset of the voluntary
EMG instead of the stimulus. Therefore, one could
evaluate the changes in excitability as a function of
pre-EMG interval. The results of the experiment are
presented in Fig. 3.
During most of the RT interval, the amplitude of the
reflexes remains stable; suddenly about 35 ms prior to
the onset of the voluntary EMG, the amplitude of the
reflex elicited in the involved muscle increases and,
symmetrically, the amplitude of the reflex elicited in
the non-involved muscle decreases. This pattern clearly
reveals that the arrival of the voluntary motor command on the a motoneurons controlling the response
agonist is preceded by a removal of the presynaptic
inhibition of these neurons and by a reinforcement of
the presynaptic inhibition of the motoneurons controlling the alternative response. The increase in the presynaptic inhibition of the motoneurons controlling the
non-required response substantiates the idea according
to which this response is inhibited during the RT interval. The spinal cord therefore appears to be a site of
inhibition.
2.2. Inhibition at the spinal level
In a first study, we looked for a possible manifestation of inhibition at the spinal level. In this aim, we resorted to the Hoffman (or H) reflex technique. The
median nerve was electrically stimulated at the level of
the wrist in order to recruit its sensory fibers. Among
these fibers are the Ia afferences that project directly to
the a motoneurons, these two types of neurons form
the basis of the monosynaptic reflex loop (see Fig. 2).
The electric stimulation of the Ia afferences provokes
the synchronous discharge of the muscle motor units,
termed H reflex, which is quantified by surface EMG
recordings. An important point is that the gain of the
loop is permanently controlled by the brain via an inhibitory spinal interneuron projecting upstream from the
Fig. 3. Amplitude (in z scores) of the H reflex as a function of the time
pre-response. The EMG response started at time 0. During the major
part of the RT, the H reflex remains stable both in the involved and in
the non-involved hand. About 35 ms before EMG onset, the
excitability of the motor nuclei involved in the response increases,
whereas the excitability of the motor nuclei involved in the incorrect
response decreases.
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B. Burle et al. / Brain and Cognition 56 (2004) 153–164
2.3. Inhibition at the cortico-spinal level as revealed by
transcranial magnetic stimulation
In a second step on the track of inhibition, we have
used the technique of TMS so as to probe the excitability of the zone of the primary motor cortex controlling
the thumb flexion and the downstream structures. The
coil was optimally positioned for stimulating the thumb
representation in the left motor cortex. The stimulation
transynaptically activates the cortifugal cells that project
onto the spinal a motoneurons. The stimulation recruits
two populations of interneurons. The first population is
excitatory (EC on Fig. 2), projects directly to the pyramidal cells and is responsible for the motor evoked potential (MEP); the second population is inhibitory (IC,
Fig. 2), projects onto the excitatory interneurons, and
is responsible for the silent period, that is a suppression
of the muscle activity for a brief period of time (for a
brief review, see Burle et al., 2002a).
The physiological effect of TMS was quantified with
classic surface EMG techniques. The subjects were to
exert a tonic activity in their response agonists in order
to start a trial. The TMS was delivered at different times
during the RT interval, that were chosen as a function of
each subject RT distribution: The first stimulation was
delivered at 1/4 of the first decile of the RT distribution,
the second at 1/2, the third at 3/4, and the last at the value of the first decile. In the following, we shall focus on
the duration of the silent period elicited by the stimulation of the inhibitory population of interneurons. The
duration of the SP due to the stimulation of inhibitory
interneurons of the involved cortex decreases as one gets
closer in time to the response (Fig. 4), which indicates
that this cortex becomes progressively more excited.
Symmetrically, the duration of the SP due to the stimulation of the non-involved motor cortex increases as
time elapses, which shows that this structure becomes
Fig. 4. Duration of the silent period as a function of the post-stimulus
time. The duration of the silent period decreases in the involved cortex,
indexing an increase in excitability, whereas it increases in the noninvolved cortex, revealing an inhibition.
increasingly inhibited. One can thus conclude that, like
the spinal cord, the primary motor cortex constitutes a
site of inhibition.
2.4. Inhibition at the cortical level as revealed by surface
Laplacian estimation
We have further tracked the inhibition with EEG
techniques augmented by approximation of the surface
Laplacian (Tandonnet, Burle, Vidal, & Hasbroucq,
2003; Taniguchi, Burle, Vidal, & Bonnet, 2001; Vidal
et al., 2003). The spatial definition of conventional
monopolar recordings is poor but can be drastically improved by Laplacian transformation. The Laplacian
acts as a high-pass spatial filter and thus removes the
blurring effects of current diffusion through the highly
resistive skull. It provides a good approximation of the
corticogram (Gevins, 1989). In the conducted experiment, the Laplacian was approximated by the source
derivation method (Hjorth, 1975) modified by MacKay
(1983). This method allows one to estimate the Laplacian at a nodal electrode located at the center of a virtual
equilateral triangle at the apexes of which are positioned
three other active electrodes. In the conducted experiment, nodal electrodes were positioned at sites corresponding to C3 0 and C4 0 , that is 0.5 cm anterior to the
C3 and C4 locations in the 10–20 system of the international federation. Fig. 5 presents the activity recorded
for the go trials over the involved and non-involved motor cortices.
In the period preceding the response (100 to 0 ms,
shaded area), a negative wave develops over the involved motor cortex and, symmetrically a positive wave
develops over the non-involved cortex. The resemblance
between this pattern and the pattern of excitation–inhibition observed in stimulation studies suggests that the
Fig. 5. Amplitude of the surface laplacian recorded over the motor
cortices ipsi- and contralateral to the response. A negativity develops
over the motor cortex contralateral to the response (involved cortex),
and an positivity develops over the cortex ipsilateral to the response
(non-involved cortex).
B. Burle et al. / Brain and Cognition 56 (2004) 153–164
negative wave reflects the activation of the involved motor cortex, while the positive wave reflects the inhibition
of the non-involved motor cortex. In this context, the
EEG data strengthen the notion that the motor cortex
is a site of inhibition in choice RT tasks (Vidal et al.,
2003). The activity time-locked to the stimulus for both
go and nogo trials in the incompatible condition is presented in Fig. 6.
The negative and positive waves respectively recorded over the involved and non-involved cortices
are recognizable although they are not as well time
locked to the stimulus than to the response. Importantly, a positive wave also develops over the motor
cortices in no-go trials at about the same time as the
positive wave observed over the non-involved cortex
in go trials. The presence of this positive wave is
important for at least three reasons. First, since in
no-go trials participants have really to inhibit their responses, it supports the interpretation of the positive
wave observed in go trials in terms of inhibition. Second, it shows that the positive wave can be obtained
in absence of a negative counterpart over the involved
motor cortex, which suggests that the agent of inhibition is to be found upstream in the information processing flow, possibly in the anterior cingulate cortex
and/or the SMA. As a consequence, this type of inhibition appears to be more feed-forward than lateral.
Third, and more importantly, it strongly suggests that
the activation of the involved motor structures and
the inhibition of the non-involved ones is not a wired
property of the motor structures but rather reflect the
implementation of the voluntary motor command. Another argument for such a strategic implementation
159
Fig. 7. Amplitude of the laplacian obtained over the motor cortices in
a simple RT task. No ipsilateral positivity is observed before the
response. The SMA is not activated neither before the response.
comes from unpublished data from our lab. Macar
and Vidal (2002) asked their subjects to produce a
2.5 s duration separated by two left thumb key-presses.
In one condition, that served as a control and that was
not included in the published paper, the subjects had to
give the first key-press as fast as possible after the onset
of a response signal. They therefore had to perform a
simple RT task, as the response was completely known
in advance. We used these data to check whether the
positivity was still present in simple RT. The results
are presented in Fig. 7. The figure shows the laplacian
estimates obtained on C4 (contralateral to the response), C3 (ipsilateral) and FCz (over the SMA).
The data are averaged time-locked to the response
(not to EMG as in Fig. 5). In the period preceding
the response (150 to 0 ms, shaded area). One can
clearly see the contralateral negativity, but no ipsilateral positivity before the response, indicating that the
ipsilateral cortex was not inhibited by the activation
of the contralateral one. Note further that the SMA
is not active before the response, contrary to what Vidal et al. (2003) observed in choice RT. Such absence
of activity of the SMA when there is no ipsilateral inhibition is compatible with the idea that the SMA is the
agent of the inhibition.
3. Discussion
Fig. 6. Amplitude of the laplacian obtained over the motor cortices
during a variant of the Stroop task including one-third of go–nogo
trials (Vidal et al., 2003). The data presented correspond to the
incompatible situation. In the go task, one can observed the negativity/
positivity observed time-locked to the response, although less clear
because of the stimulus-locked averaging. In the nogo situation, one
can see a positivity very similar to the one observed over the ipsilateral
cortex of the go task.
The results of the three studies converge in demonstrating that in between-hand two-choice RT, the unimanual motor command is expressed bilaterally: the
activation of the motor structures involved in the required response is accompanied by an inhibition of the
structures involved in the other alternative response.
Our results therefore provide direct support for the compelling theoretical notion of inhibition for which there
was little empirical support.
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B. Burle et al. / Brain and Cognition 56 (2004) 153–164
3.1. Connectivity between homologous structures or
command implementation?
A first question concerns the nature of the symmetrical activation-inhibition pattern observed in the three
studies. Does this pattern result from the intrinsic spinal
and/or cortical connectivity or does it reflect a strategic
option in the implementation of the central motor
command?
Such a balance in excitability is of course reminiscent
of SherringtonÕs reciprocal inhibition (Sherrington,
1906/1947), which is a wired property of agonist and
antagonist motor nuclei: When the flexors of one joint
are being excited, the extensors of the same joint are
inhibited and vice versa (for an illustration in the context of reflex studies see e.g., Brunia, 1984). Reciprocal
inhibition, however, has been described between the
flexors and the extensors of the same joint but never between homologous response agonists as in our studies.
The increase in presynaptic inhibition of the non-involved motoneuronal pool observed in the H-reflex
study must therefore reflect a property of the central
motor command (for a discussion, see Hasbroucq
et al., 2000).
This spinal inhibition, as well as the inhibition of the
non-involved motor cortex evidenced in the TMS
study, has not been empirically dissociated from its
activation counterpart. Since the potent influence of
transcallosal connections has been demonstrated in a
number of studies (Chen, Yung, & Jie-Yuan, 2003;
Meyer, Roricht, Grafin, Kruggel, & Weindl, 1995),
the possibility that the inhibition observed in our stimulation experiments results from hardwired inter-hemispheric connections cannot be discarded. In other
words, these studies do not allow one to decipher
whether the inhibition of the non-involved structures
is due to an inter-hemispheric connectivity that would
mechanically follow the activation of the involved motor cortex or whether it reflects a strategic option in the
implementation of the voluntary motor command. In
contrast, the EEG study demonstrates that the inhibition expressed by the development of a positive wave
over the non-involved motor cortex can be obtained
in isolation during nogo trials, and that a contralateral
negativity can be obtained without ipsilateral positivity
in simple RT. These observations suggest that the inhibition of the non-involved structures is independent of
the activation of the involved structures and supports
the idea that it reflects the implementation of the central motor command rather than intra-cortical connectivity. Other dissociations between the activation and
inhibition have been observed. Although it was not
the primary goal of their study, the results obtained
by Taniguchi et al. (2001) suggest that the contralateral
negativity is similar between simple (precued) RT and
choice RT, but that the ipsilateral positivity is reduced
in simple (precued) RT.1 Tandonnet et al. (2003) suggested that motor preparation (time preparation) affects the contralateral negativity but not the
ipsilateral positivity.
Therefore, one possibility is that, in choice RT tasks,
the motor command specifies both the activation of the
involved motor structures and the inhibition of the
structures involved in the alternative responses. Such a
bilateral balance mechanism may serve to prevent erroneous responding by reducing the sensitivity of the noninvolved motor structure from upstream influences.
Indeed, the inhibition component is possibly due to
the between-response choice required by the task, bearing in mind that in the three studies, before the response
signal the two responses were equiprobable, and the
subjects were unaware of what response they would
have to make after the occurrence of the imperative
stimulus. To prevent an error in this context, the subjectÕs interest is to inhibit the alternative response, to ensure that only the correct response will be triggered.
3.2. Feed-forward or lateral inhibition?
The TMS data do not shed light on this issue: the
inhibition component revealed by the increase in silent
period duration during the RT interval can as well reflect the reciprocal inhibition of the two motor cortices
and the implementation of a selective pattern whose
agent would be located elsewhere in the nervous system.
In constrast, most authors agree that the modulation
in H-reflex amplitude reflect variations in the presynaptic inhibition of the motoneuronal pools (for a review,
see Schieppati, 1987). Such an inhibition is by definition
feed-forward, although not all feed-forward inhibitions
are of presynaptic type, and its agent is indubitably located higher from the spinal cord in the motor system
hierarchy. The occurrence of the positive wave in isolation over the non-involved motor cortex during nogo
trials of the EEG experiment suggests that the inhibition
observed in the go trials originates not from the opposite
motor cortex but from a structure activated sooner during the processing of the information conveyed by the
imperative stimulus, for instance the anterior cingulate
cortex (Band & van Boxtel, 1999) or the SMA. Indeed,
Vidal et al. (2003) showed that the activation/inhibition
pattern they obtained from EEG recordings was preceded (50 ms earlier) by another wave over the SMAs.
This prior activity recorded over the SMAs, might correspond to an inhibition exerted, by these structures,
1
In this study, a preparatory signal could indicate which response
was to be given. Although it is a simple RT task, it was mixed with a
choice RT task (no precue). In this situation, an ipsilateral positivity
was still observable, although of smaller amplitude.
B. Burle et al. / Brain and Cognition 56 (2004) 153–164
on the motor cortex ipsilateral to the response. Let us recall that, in simple RT situation in which no ipsilateral
inhibition was observed, the SMA was not activated neither (Fig. 7). Considered together, the present results are
more in favor of a feed-forward than of a lateral inhibition. Further research is however needed before strong
conclusions regarding this point can be reached. Now,
a comment concerning the relationship between the recent model of Usher and McClelland (2001) and our
empirical demonstration of inhibition in choice RT is
in order. One premise of this model is that lateral inhibition is physiologically more plausible than feed-forward inhibition. In support of this assumption, the
authors refer (without citing them) to combined light
and electron microscopic studies showing that corticocortical long-range connections, including transcallosal
projections, originate from pyramidal cells that are
excitatory (glutamatergic) in nature. In contrast, local
connections are both excitatory and inhibitory (GABAergic, for a review see Peters & Jones, 1984). From this
widely acknowledged organization, Usher and McClelland (2001) inferred that inhibitory influences were predominantly of the lateral or recurrent type (p. 555). This
is contradicted by our results suggesting that the inhibition of the non-involved motor structures originate from
long-range cortico-cortical connections. As a matter of
fact, the feed-forward inhibition that appears most compatible with our findings is very likely implemented by
the projection of excitatory long-range pyramidal cells
onto local inhibitory interneurons, which in turn project
onto the neuronal populations responsible for the nonrequired response. In other words, contrary to Usher
and McClellandÕs claim, the organization of cortico-cortical connections is physiologically compatible with a
feed-forward inhibition (Burle et al., 2002a; Heuer,
1987).
The above discussion may give the impression that
inhibition, and executive control mechanisms, only occur at the cortico-spinal tract level. This is certainly
not the case, and is not what we are claiming neither.
As a matter of fact, several imaging studies of the
go–nogo or stop tasks have revealed that other brain
structures are involved in the processes required by
these tasks, and likely in the inhibitory ones, like for
example the right prefrontal cortex (Bokura et al.,
2001; Konishi, Nakajima, Uchida, Sekihara, & Miyashita, 1998; Rubia et al., 2001). Importantly, however, the
logic developed above cannot be strictly applied to
other structures, as one cannot directly measure the
inhibition, as defined in the introduction (i.e., an active
decrease in excitation). Furthermore, the fact that those
structures are active during a task involving inhibition
does not necessarily mean that those structures are directly involved in inhibitory components. Therefore,
other logics need to be established to expand our quest
for inhibition.
161
3.3. Physiological inhibition and information processing
models
The inhibition demonstrated with the three techniques depends critically on the involvement of the studied structures in the response. In other words, its
manifestation is response specific. In serial stage models
of information processing (Sternberg, 2001; van der Molen, Bashore, Halliday, & Callaway, 1991), the inhibition occurs after the response has been selected on the
basis of the information conveyed by the imperative
stimulus. Now, since it is response specific, the inhibition
we reported likely occurs at the level of response programming or execution. The possibility that this inhibition is feed-forward does not preclude the possibility of
lateral inhibition upstream in the processing. For example, it might well be the case that at the response-selection stage, the competition between the representations
of the two possible responses is implemented through
lateral inhibition. This addresses the question of the
location of the response accumulators in ‘‘neurophysiologically inspired models’’ that typically rely on lateral
inhibition (e.g., Cohen, Servan-Schreiber, & McClelland, 1992; Usher & McClelland, 2001). As stressed
above, in such models, a response is emitted as soon
as one of those accumulators reaches a predefined
threshold. Given the indexation function defined in the
introduction, if such accumulators implement the response execution stage and if the response is given
through the activation of the cortico-spinal tract, they
have to be located at least at the level of primary motor
cortex. As a matter of fact, Spencer and Coles (1999) extended Cohen et al.Õs neural-net model of the Eriksen
task (Cohen et al., 1992) to account for results relative
to the Ôlateralized readiness potentialÕ (Gratton, Coles,
Sirevaag, Eriksen, & Donchin, 1988). They showed that,
in addition to accounting for behavioral data, the model
can also handle electrophysiological results. The important point here is that, as the LRP is thought to arise
from the primary motor cortex, if the response units mimic the LRP, we should conclude that the response units
implement the stages reflected in the LRP, that is at the
primary motor cortices level, which seems inconsistent
with our data suggesting that inhibition is feed-forward
rather than lateral. Another possibility, however, is that
the ‘‘response accumulators’’ describe response selection, programming and execution occurring at later
stages. In this case, such models incorporating lateral
inhibition at the response selection stage remain compatible with feed-forward inhibition at the response execution level. Note that in this case, the ‘‘RT’’ of the
model does not comprise the response execution time.
This would be unproblematic if this time could be assumed to be constant. Different experimental manipulations, however, have been shown to affect response
execution speed (for example response uncertainty:
162
B. Burle et al. / Brain and Cognition 56 (2004) 153–164
Hasbroucq, Akamatsu, Mouret, & Seal, 1995; Possamaı̈, Burle, Osman, & Hasbroucq, 2002; Tandonnet
et al., 2003). It seems therefore necessary to better specify what response units really reflect in such models, and
at which level they are implemented.
A last comment is in order, the inhibition of the
incorrect response nicely fits the psychological notion
that response competition is implemented through a balance of activation and inhibition of the possible responses in regular choice RT. Further, inhibition has
also been proposed to be an efficient tool for executive
control. The data reported in the go–nogo experiment
(Fig. 6) suggest that inhibiting the incorrect response
shares some mechanisms with whithholding a response.
Now, the question of whether the strategic activation
and inhibition of responses in conflict tasks (Burle
et al., 2002b; Ridderinkhof, 2002) involves the same processes, and is implemented in the same way remains an
open question. The data recorded so far do not shed
light on this question, but one can be confident that,
as the substrate of inhibition has been identified, suitable
protocol coupled with the recordings of the correct indices, will soon provide additional information on this
issue.
Acknowledgments
The authors thank Françoise Macar for providing us
the data of the simple RT task, and Michel Bonnet, Laurence Carbonnell, Sonia Allain, and Wery van den Wildenberg for helpful discussions on this topic.
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