Psychophysiology, 37 ~2000!, 385–393. Cambridge University Press. Printed in the USA.
Copyright © 2000 Society for Psychophysiological Research
Changes in spinal excitability during choice reaction time:
The H reflex as a probe of information transmission
THIERRY HASBROUCQ,a MOTOYUKI AKAMATSU,b BORÍS BURLE,a MICHEL BONNET,a
and CAMILLE-AIMÉ POSSAMAÏ a
a
b
Centre de Recherche en Neurosciences Cognitives, Centre National de la Recherche Scientifique, Marseille, France
Neuro-Informatics Laboratory, National Institute of Bioscience and Human Technology, Tsukuba, Japan
Abstract
The aim of the present study was to investigate the modulations in amplitude of H reflexes elicited in a hand muscle,
the flexor pollicis brevis, during the performance of a choice reaction time ~RT! task in which this muscle was directly
involved. Ten subjects were to choose between a left- or a right-thumb key-press according to the lateral location of a
flash of light. The stimulus–response mapping was either compatible or incompatible. Hoffman reflexes were elicited
at different times during the RT by stimulation of the median nerve. Twenty-five milliseconds before the voluntary
response, the amplitude of the H reflex suddenly increased when the muscle was involved in the response and decreased
symmetrically when the muscle was not involved in the response. Mapping compatibility exerted no detectable
influence on the changes in spinal excitability. The latter result supports the assumptions that are at the core of
Sternberg’s additive factor method.
Descriptors: Response competition, Additive factor method, Stimulus-response compatibility
study these operations, the subject must process the information
conveyed by the imperative signal in order to select, program, and
execute the response called by this signal. These sets of operations
are generally referred to as “stages” in the literature. We shall
retain this terminology in the following. Eichenberger and Rüegg
~1984! studied the modulation of the H reflex in the context of a
choice RT task. In one condition of their experiment, the subjects
were to flex the right foot at the onset of a green light and the left
foot at the onset of a red light. H reflexes were elicited in the soleus
muscle at different times during the RT interval. Eichenberger and
Rüegg reported a specific facilitation of the H reflex that was
confined to the leg involved in the response called by the imperative signal. As stressed by Eichenberger and Rüegg, an implication of this finding is that the H-reflex facilitation occurs only after
the decision concerning the limb to be moved has been taken. In
other words, the facilitation of the H reflex occurs after the processes involved in the response selection stage. However, this conclusion does not necessarily apply to the experimental tasks typically
studied by cognitive psychologists. This is because most results
concerning information processing issues have been obtained in
manual key-pressing tasks whereas the conclusion of Eichenberger
and Rüegg has been reached from the study of reflexes elicited in
the soleus. Indeed, Bonnet, Requin, and Semjen ~1981! stressed
that the reflex sensitivity of this muscle is related to its functional
features. In particular, the soleus is used mainly in postural activity
involving the antigravity servo-control of neuromuscular spindles.
To subserve this function, the soleus comprises a high proportion
of small tonic motor units that are more sensitive to proprioceptive
Ia afferents than the motor units composing the upper limb muscles. In humans, the upper limb muscles have a different function:
When triggered in agonist muscles, the electrically evoked monosynaptic reflex ~Hoffmann @H#! increases in amplitude before the
onset of a change in electromyographic activity triggered by a
corticospinal command ~Coquery & Coulmance, 1971!. This facilitation is greater if the electrical stimulation is temporally close
to the onset of the response movement ~e.g., Gottlieb, Agarwal, &
Stark, 1970!. Such a phenomenon is thought to reflect either the
removal of the presynaptic inhibition of the motoneurons’ somesthetic afferents ~Pierrot-Deseilligny, Lacert, & Cathala, 1971! or a
subliminal increase of the excitatory effect of the descending afferent volley reaching the motoneurons ~Porter & Muir, 1971; for
a review see Schieppati, 1987!.
When the electric stimulation is delivered during the reaction
time ~RT! to a sensory signal, the reflex facilitation precedes the
voluntary response movement by several tens of milliseconds and
may therefore constitute an early index of covert response implementation operations. In the choice RT tasks typically designed to
Parts of this work were presented at the meeting “Neural Substrates of
Cognitive Processes. Hommage à Jean Requin” held in Marseille, May
1997.
This work was financed by the DGA, Direction des Recherches Etudes
et Techniques under contract 93-095. B.B. was supported by a doctoral
grant from the Ministère de l’Enseignement Supérieur et de la Recherche
~grant 961175!.
We thank Kees Brunia, Steve Hackley, Allen Osman, Hidekazu Kaneko,
Franck Vidal, and an anonymous reviewer for helpful comments and Bernard Arnaud, Raymond Fayolle, and Guy Reynard for technical assistance.
Address reprint requests to: Thierry Hasbroucq, CNRS-CRNC, 31 chemin
Joseph Aiguier, 13402 Marseille cedex 20, France. E-mail: thierry@lnf.
cnrs-mrs.fr.
385
386
They are mainly involved in phasic nonpostural activities, such as
reaching. Furthermore, the neural organization subserving handmovement control presents some peculiarities. Notably, the hand
muscles have extensive cortical projections and their motoneurons
are apparently not subject to Renshaw inhibition via recurrent axon
collaterals ~see Lemon, 1993!. Because of the anatomo-functional
difference between the respective neural controls of lower and
upper limb muscles, a generalization of conclusions drawn from
the study of monosynaptic reflexes elicited in the soleus to those of
hand muscles appears unwarranted. The first aim of the present
study was to study the modulations of the H reflex elicited in a
hand muscle, the flexor pollicis brevis, during the performance of
a bimanual choice RT.1
The second aim was to use the H-reflex technique to address
one important issue in cognitive psychophysiology: that of discrete
versus continuous transmission of information between processing
stages ~Miller, 1988!. Different models of information processing
have been elaborated. Although numerous studies support the relevance of the decomposition of RT into contingent stages ~see
Sanders, 1990!, the manner in which the information is transmitted
between these stages is still a matter of debate. Different conceptualizations have been proposed with respect to this matter. According to Miller ~1988!, they stand on a continuum going from
models that assume a discrete, all-or-none transmission of their
ouputs to those assuming a continuous transmission. The models
standing at the discrete end of this continuum suppose that only the
final product of the operations performed at stage N is transmitted
to stage N 1 1. As a consequence, the stages are serially organized
and nonoverlapping: Stage N 1 1 can start only when stage N has
completed its operations. Conversely, in the models located at the
opposite end of the continuum, the stages make their partial outputs continuously available to the subsequent stages of processing.
In such models, there is temporal overlap between successive stages.
The operations performed by stage N 1 1 begin on the basis of
partial information transmitted by stage N.
Several arguments have been advanced for and against discrete
and continuous modes of information transmission. They have
been taken up and analyzed in detail in several reviews ~Meyer,
Osman, Irwin, & Yantis, 1988; Miller, 1988; Sanders, 1990!, thus
obviating the need to do so here. In the present study, we propose
to use the H reflex as a mean of revealing the nature of the transmission between the response selection stage and the subsequent
motor processes. It must be stressed that, although the monosynaptic loop is anatomically peripheral, the variations in H-reflex
amplitude do not necessary reflect low-level motor processes. For
instance, Bonnet, Decety, Jeannerod, and Requin ~1997! demonstrated that the amplitude of this reflex varies during a task as
cognitive as mental simulation of an action. Besides, the changes
in reflex amplitude reflect the presynaptic inhibition of the motoneurons proprioceptive afferents as well as the subthreshold depolarization of these cells ~for reviews see, e.g., Bonnet et al., 1981,
and Schieppati, 1987!. During RT, the modulations in presynaptic
inhibition precede the forthcoming voluntary muscle contraction
by several tens of milliseconds. In a flow chart diagram, they can
be placed upstream with respect to the peripheral mechanisms
1
Jaeger, Gottlieb, and Agarwal ~1982! did elicit stretch reflexes in
agonist muscles during a choice task. However, in this study the reaction
signal was the reflexogenic torque perturbation itself. This procedure simply allowed the authors to index spinal excitability at a constant time ~about
20 ms! after the presentation of the reaction signal.
T. Hasbroucq et al.
involved in the generation of the voluntary muscle contraction.
Thus, in an information processing model specifying when processes occur in time, they would be located after response selection
~because they are response specific! but before the recruitment of
the motoneurons by the descending voluntary command.
To address the information transmission issue, we have manipulated the compatibility of the stimulus–response mapping ~Fitts &
Deininger, 1954!. This manipulation consists simply of varying, by
changing the task instructions, the mapping of the stimuli onto the
responses. Consider, for instance, a task in which the stimuli are
flashes of light appearing to the left or to the right of a fixation and
the responses, finger presses respectively performed on the left or
on the right of the subject’s body. The compatible mapping would
assign each stimulus to its ipsilateral response ~e.g., left stimulus 2
left response! while the incompatible mapping would assign each
stimulus to its contralateral response ~e.g., left stimulus 2 right
response!. Compatible mappings invariably lead to shorter RTs
than incompatible mappings ~for a review see Kornblum, Hasbroucq, & Osman, 1990!. It is generally considered that incompatible mappings require more time-consuming operations than
compatible ones and that such manipulations affect the stage of
response selection ~see, e.g., Hasbroucq, Guiard, & Ottomani, 1990!.
The latter consideration entails the assumption that the effect of
stimulus–response mapping is “selective,” in the sense that it does
not affect all information processing stages.
A supplementary assumption, frequently incorporated in discrete models, is that of constant output, which specifies that the
output of a stage is independent of factors influencing its duration.
In the case of discrete transmission, the assumption of selective
influence and constant output lead one to expect that the compatibility of the stimulus–response mapping affects specifically the
stage of response selection. In other words, the following motor
stages ~i.e., response programming and execution! should remain
unaffected by the mapping manipulation. Thus, in this case, the
delay between the facilitation of the H reflex and the voluntary
response should be unaffected by the compatibility of the stimulus–
response mapping. In contrast, in the most extreme version of the
hypothesis of continuous transmission, selective influence implies
that the compatibility of the stimulus–response mapping affects
response selection and all subsequent motor processes ~while sparing the stages located upstream from response selection!. Note that
in its initial version, the continuous flow model ~Eriksen & Schultz,
1979! assumed a threshold for overt responding, thereby making
response execution an all-or-none discrete process. However, later
work led Eriksen and his colleagues to consider that this very last
process was continuous in nature ~see, e.g., Coles, Gratton, Bashore,
Eriksen, & Donchin, 1985; Eriksen, Coles, Morris, & O’Hara,
1985!. Coles et al. ~1985! summarized this view nicely: “. . . , the
fact that the temporal characteristics of response execution can be
modified and that the response can be initiated without being executed, suggests that response execution is best conceived as a
continuous process” ~Coles et al., 1985, p. 551!.2 Such a proposal
leads one to expect that all the stages following response selection
should last longer for incompatible than for compatible mappings.
If such were the case, the delay between the H-reflex facilitation
and the onset of the response should be longer when the mapping
is incompatible than when it is compatible.
2
The latter view, which is challenged in the present study, is not shared
by all continuous modelers. Notably, McClelland ~1979! considered response execution as the only discrete stage in information processing.
Spinal excitability during choice reaction time
Materials and Methods
Subjects
Fourteen subjects with normal or corrected-to-normal visual acuity
volunteered for the experiment. All of them had practice in RT
tasks. The subject’s informed consent was obtained according to
the declaration of Helsinki. Four subjects were discarded because
they did not show a detectable H reflex. Among the 10 subjects
retained for the entire experiment, 7 were right handed and 3 were
left handed. Two of the subjects were authors, the others were
recruited from the pool of students of the laboratory and paid at a
flat rate. The retained subjects were aged between 22 and 47 years
~mean 5 28 years!.
Electromyographic (EMG) Recordings
The electromyographic activity of both flexores pollicis brevis was
recorded. Paired Ag-AgCl electrodes ~Vickers!, 6 mm in diameter,
were fixed 1 cm apart on the skin of the thenar eminences. The
signal was monitored continuously, amplified ~Grass P5, gain 5000!,
filtered ~band pass, 15 Hz–1 kHz!, and digitized online ~A0D rate
2 kHz!. In each trial, the EMG activity was recorded during the
1,700 ms extending from the onset of the warning signal from the
end of the time allowed for the response ~see the section “Behavioral Set-Up and Task” below!.
Electrical Stimulation
H reflexes were elicited with a Grass S8 electrical stimulator the
output of which was connected to a Grass S1U5A stimulus isolation unit. Electrical stimulations ~square pulses, 1-ms duration!
were delivered over the median nerve of the dominant hand at the
wrist. Because the responses were key presses exerted with either
the left or the right thumb ~see below!, the electrical stimulation
was delivered to the involved median nerve when the response was
made with the thumb of the dominant hand and to the uninvolved
median nerve when the response was made with the thumb of the
387
nondominant hand. Figure 1 shows schematically the elicitation of
an H reflex in the flexor pollicis brevis with the technique used in
the present experiment.
The stimulating electrodes were two brass discs, 15 mm in
diameter and 5-mm thick. The face of each electrode in contact
with the subject’s skin was coated with conductive paste and strapped
onto the wrist using an elastic band. The cathode and anode were
fixed on the internal and external parts of the wrist, respectively.
The stimulation was first set for each subject at an intensity producing an H response without an M response in the slightly activated muscle ~corresponding to a 40–300-g pressure; see the section
“Adjustment Trials” below!. The intensity of the electrical stimulation was then set such that the amplitude of the H reflex was
about half the amplitude of the maximal reflex that could be elicited.
Adjustment Trials
Some computer-controlled series of adjustment trials were performed during the training session to select the subjects for the
experiment ~see above!. These series of trials were also performed
during the experimental session before the subject started the task
in order to adjust the intensity of the electrical stimulation. During
these series of trials, the subjects exerted a pressure sufficient to
close the light but not the hard microswitches of the response
device ~see the section “Behavioral Set-Up and Task” below!. This
was done to ascertain that background muscle tension was present,
which is a necessary condition to elicit H reflexes in upper arm
muscles ~Burke, Adams, & Skuse, 1989!. After the last stimulation
of the adjustment trials, the EMG signal, averaged over trials and
aligned to the occurrence of the stimulation, was displayed on the
screen to be examined visually. When the experimenters judged
the signal and the evoked response satisfactory, they recorded the
beginning and end the H reflex using cursors, so as to define the
scoring window for analysis of responses on the experimental
trials ~see the section “Signal Processing” below!.
Figure 1. Experimental set up for studying the H reflex in the present study: location of stimulating electrodes ~cathode visible!,
ground electrode, and surface electrodes for recording the electromyographic activity of the flexor pollicis brevis. The Figure shows
schematically: ~1! the monosynaptic reflex loop and the possible modulation of this loop via the mechanism of presynaptic inhibition
and ~2! Ia projections to supraspinal structures.
388
Behavioral Set-Up and Task
The experiment was controlled by a Hewlett Packard Vectra microcomputer. The subject sat at a table. The subject faced an opaque
screen on which three light-emitting diodes ~LEDs! were fixed at
a distance of 1.5 cm apart. The central LED ~red! served as a
fixation point and the two outer LEDs ~green! displayed the response signals. The two outer LEDs were at a visual angle of about
28. Two plastic buttons were placed on the table, separated by a
distance of 10 cm. Each button was mounted on two superposed
microswitches. A pressure of 40 g over a course of 0.1 cm closed
the upper ~light! microswitch and a pressure of 600 g over a course
of 0.3 cm closed the lower one. The response buttons were to be
operated with the left and right thumbs, respectively. To start a
trial, the subject was to lightly press on the response buttons with
the thumbs so as to maintain the light microswitches closed and the
hard microswitches open ~see the section “Adjustment Trials” above!.
One second later, the central red LED was lit as the warning signal.
After a constant foreperiod of 700 ms, a response signal was given
by switching on one of the two outer green LEDs. The response
was to execute a flexion of one thumb to close the hard switch of
the corresponding button. It caused the warning and response signals to be turned off. The time allowed for the response was
1,000 ms. Because the trials were self-paced, the intertrial interval
was variable across trials.
Design and Instructions
A block comprised 100 trials. The crossing of the two response
signals ~left or right! and of the five times of stimulation ~stimulation delivered either 40, 80, 120, or 160 ms after the response
signal or no stimulation delivered! defined 10 experimental events.
In each block, the first order sequential effects for trial-to-trial
transitions were counterbalanced ~Possamaï & Reynard, 1974!.
The subjects were to produce a pressure with either the left or right
thumb in response to the illumination of either the left or the right
LED. In the compatible mapping condition, the subjects were to
pressure the button ipsilateral to the response signal ~left signal 2
left thumb, right signal 2 right thumb!. In the incompatible mapping condition, this mapping was reversed ~left signal 2 right
thumb, right signal 2 left thumb!.
There were two sessions, one training session and one experimental session. During the training session, the subject was to
perform successively two blocks of trials. No H-reflex stimulation
was delivered during this session and the mapping was alternated.
Five of the retained subjects began with the compatible mapping,
the other five with the incompatible mapping. Once this behavioral
training was completed, the session ended with some computercontrolled series of adjustment trials ~see above!, which were performed so as to determine whether or not an H reflex could be
elicited in the flexor pollicis brevis of each subject. The experimental session began with similar series of adjustment trials. These
were performed to adjust the intensity of the electrical stimulation.
The subjects retained for this session then performed eight blocks
of trials in which the electrical stimulation was delivered according
to the pseudorandom series described above. As for the training
session, the mapping was alternated every other block. The subjects were given a few minutes of rest between each block. The
instructions emphasized both speed and accuracy.
Signal Processing
Voluntary response latency was defined as the interval between the
response signal and the onset of the change in EMG activity involved in the execution of the overt voluntary response. In this
T. Hasbroucq et al.
aim, the EMG activity recorded during each trial was inspected
visually. To this end, the signal was displayed on the computer
screen aligned to the onset of the response signal. An experimenter
marked the voluntary response latency by placing a cursor with the
computer mouse.
The time of occurrence and the duration of the responses evoked
during the adjustment trials ~see above! served to define the intervals that will be termed “H-reflex windows” in the following. One
H-reflex window was defined for each subject and stimulation
times; these scoring windows were 13–20 ms in length. For each
test trial, the peak-to-peak amplitude of the nonrectified EMG
signal recorded during the appropriate H-reflex window was computed. This index will be referred to as “reflex amplitude” in what
follows.
Results
Error Rate and Rejection of Correct Trials
Errors occurred in 1.92% of the total number of trials. The effect
of mapping compatibility was marginally significant on the error
rate: The subjects tended to commit more errors for the incompatible mapping ~2.48%! than for the compatible mapping ~1.92%!,
Wilcoxon test: T~10! 5 8, p 5 .05. Erroneous trials were excluded
from further processing.
Seven hundred correct trials ~10.94%! during which the voluntary EMG activity occurred before or during the corresponding
H-reflex window were rejected. This rejection was intended to
eliminate spurious enhancement of the H reflex by the motoneuronal depolarization due to the voluntary muscular contraction.3
Due to excessive tonic activity or electrical artifacts, 159 ~2.48%!
other correct trials were discarded.
Voluntary Response Latency on Correct No-Stimulation Trials
A first analysis of variance ~ANOVA! involving mapping ~compatible, incompatible! and involvement of the electrically recruited
muscle in the required response during the stimulation trials ~involved, noninvolved! as within-subject factors was performed on
correct no-stimulation trials. As expected from previous work ~for
a review, see Umiltà & Nicoletti, 1990!, the compatible stimulus–
response mapping yielded shorter voluntary response latencies
~191 ms! than the incompatible mapping ~224 ms!, F~1,9! 5 48.22,
p , .001. The involvement of the stimulated median nerve in the
response had no detectable effect on voluntary response latency,
neither as a main effect F~1,9! , 1, nor as a component term in its
interaction with mapping, F~1,9! 5 1.09, p . .10.
These results are comparable to those reported in other studies
and show that the subject’s strategy was not modified by the possible occurrence of the electric stimulation during a trial.
Assessment of the H Reflex During Adjustment
and Experimental Trials
The latency and duration of the H reflex were determined for the
adjustment trials so as to define the H-reflex scoring windows for
3
In the slightly activated soleus, more than 50% of the motor units can
be recruited by the H stimulation and the reflex discharge of the motoneurons is followed by a refractory period that lasts several tens of milliseconds. During this silent period, the motoneurons are insensitive to voluntary
corticospinal commands ~Bonnet et al., 1981!. Previous work has shown
that this is not the case in the flexor pollicis brevis, in which the voluntary
contraction can occur right after or even at the same time as an electrically
evoked H reflex ~see Romaiguère et al., 1997, Figure 1, p. 186!.
Spinal excitability during choice reaction time
the experimental trials. The H reflex began, on the average, 27 ms
after the stimulation ~range: 26–28 ms! and lasted on the average
15 ms ~range: 13–20 ms!.
Because H reflexes are not easy to elicit in upper arm muscles,
one may wonder whether we did actually evoke this response
during the experimental trials. First, we checked that the H reflex
was actually elicited by examining visually the averaged H reflexes time-locked to the electrical stimulation for each subject and
stimulation time ~see Figure 2!.
Next, the following procedure was used to test this possibility.
For each subject, the average reflex amplitudes for both muscles
~involved and noninvolved in the response! and for the compatible
and incompatible mappings were computed over all correct nonrejected trials, irrespective of the time of stimulation. In each condition, the means of the resulting values were tested against the
null hypothesis by way of the Student’s t test ~one-sample analysis!. For the compatible mapping, this test revealed the presence of
an H reflex both when the muscle was involved in the response,
t~9! 5 3.63, p , .01, and when it was not involved, t~9! 5 3.59,
p , .01. Likewise, for the incompatible mapping, the H reflex was
elicited both when the muscle was involved in the response, t~9! 5
3.55, p , .01, and when it was not involved, t~9! 5 3.11, p , .02.
389
Time Course of the H Reflex and the Discrete
vs. Continuous Issue
The voluntary response latency was taken as the reference in time.
The H reflexes recorded during the correct stimulation trials were
thus categorized according to their timing with respect to the onset
of the voluntary response. The time axis was then divided into
20-ms intervals. Note that because of the rejection procedure used
in this study, the latest H reflex occurred on average 15 ms ~range:
13–20 ms! before the voluntary EMG activity in the flexor pollicis
brevis. In what follows, this interval will be termed the “exclusion
window.” The first six bins ~i.e., from 2135 ms to 215 ms on
average before the onset of the voluntary EMG activity! comprised
76.79% of correct nonrejected stimulation trials. The remaining
bins contained too few trials to be considered in further analyses.
The number of reflexes recorded per subject for the six bins considered in the analyses is presented in Table 1.
First, the mean voluntary response latency data corresponding
to these bins were submitted to an ANOVA, the within-subject
factors of which were mapping ~compatible, incompatible! and
involvement of the electrically recruited muscle in the response
~involved, noninvolved!. As for the no-stimulation trials, the compatible mapping yielded shorter RTs ~179 ms! than the incompat-
Figure 2. Averages of the electromyographic activity in millivolts ~ordinate! during the 60 ms following the H stimulation ~abscissa!
for one subject. Only the nonrejected trials are included in the summation. The averages are time-locked to the electrical stimulation;
for this subject, the H-reflex window lasted 13 ms ~from 26 to 39 ms following the electrical stimulation!. The four panels correspond
to the four stimulation times: 40, 80, 120, or 160 ms after the response signal. The solid line represents the H reflex in the responding
muscle, the dashed line represents the H reflex in the nonresponding muscle.
390
T. Hasbroucq et al.
Table 1. Number of Reflexes Recorded per Subjects (Lines) per Bins
(Rows in ms) Considered in the Analyses
Time before the onset of voluntary EMG activity
Subjects
213402115
21140295
2940275
2740255
2540235
2340215
S
1
2
3
4
5
6
7
8
9
10
60
23
71
52
54
58
41
43
79
78
86
67
82
82
97
65
62
85
67
52
63
60
64
47
90
67
39
83
88
63
55
74
82
54
85
56
86
73
85
86
82
87
48
91
55
83
95
74
104
68
86
97
76
97
44
90
96
109
35
34
432
408
423
423
425
419
419
467
458
381
S
559
745
664
736
787
764
4255
ible mapping ~205 ms!, F~1,9! 5 39.85, p , .001. Although smaller
than that obtained on the no-stimulation trials ~33 ms!, this 26-ms
effect is crucial for testing our predictions concerning the discrete
versus continuous issue. There was no effect of the involvement of
the electrically recruited muscle, either as a main effect, F~1,9! , 1,
or as a component term in its interaction with mapping, F~1,9! , 1.
This pattern essentially replicates that evidenced in no-stimulation
trials ~see above!.
Next, to reduce the between subject variability in H-reflex amplitude, a standardization procedure was used. The mean and standard deviation of all retained reflexes ~see above! were calculated
separately for each subject. The individual amplitudes of all retained reflexes were then converted into Z scores calculated from
these references. These Z scores were submitted to an ANOVA
with mapping ~compatible, incompatible!, involvement of the electrically recruited muscle in the response ~involved, noninvolved!
and the six bins preceding the exclusion window as within-subjects
factors. The results are presented in Figure 3.
There were no main effects of time bin, F~5,45! 5 1.41, p . .10;
involvement of the electrically recruited median nerve in the
response, F~1,9! 5 1.78, p . .10; or mapping, F~1,9! , 1. Interestingly, the effect of the muscle involvement depended on the bin,
F~5,45! 5 10.05, p , .001. As can be seen from Figure 3, this
two-term interaction reflects a divergence in the amplitude of the
H reflex occurring during the last bin, that is at least 13 ms—and
25 ms on average—prior to the voluntary change in EMG activity.
This finding not only replicates in the flexor pollicis brevis the
results obtained by Eichenberger and Rüegg ~1984! in the soleus
but also demonstrates a balance in spinal excitability between homologous spinal structures: The increment of H-reflex amplitude
when the muscle is involved in the response is paralleled by a
decrement of H-reflex amplitude when the muscle is not involved.
To the best of our knowledge, this is a new finding, which will be
commented upon further in the discussion section below.
Planned comparisons ~Hoc, 1983! strengthened this interpretation by showing that the H reflex increased when the muscle was
involved, F~5,45! 5 6.58, p , .001, and decreased when the
muscle was not involved, F~5,45! 5 4.02, p , .005. Further examination of Figure 3 suggests that this balance in excitability
occurred suddenly during the last 20-ms bin. This finding was
confirmed by supplementary comparisons showing no noticeable
change in reflex amplitude before the last 20-ms bin, neither in the
involved, F~4,36! , 1, nor in the noninvolved muscle, F~4,36! , 1.
In contrast, when restricted to the last two bins, both the increase
in the involved muscle, F~1,9! 5 17.10, p , .01, and the decrease
in the noninvolved muscle, F~1,9! 5 7.99, p , .02, were significant.
Now, with respect to our predictions concerning the discrete
versus continuous issue ~see the introductory section above!, the
interaction between muscle involvement and time bin was essentially independent of mapping compatibility, F~5,45! 5 2.06,
p . .10. This result suggests that the time course of the changes in
H-reflex amplitude is unaffected by mapping compatibility. In other
words, the 26-ms effect of mapping reported on voluntary response latency occurred before the changes in spinal excitability.
This outcome is in agreement with a model assuming a discrete
transmission between response selection and the motor processes
involved in the changes of spinal excitability.
Discussion
In the present experiment, H reflexes were successfully elicited in
the flexor pollicis brevis during the performance of a two-choice
RT task in which the alternative responses consisted in thumb key
presses. The compatibility of the stimulus–response mapping was
manipulated and affected the subjects’ performance: The compatible mapping yielded shorter voluntary response latencies than the
incompatible mapping. In this context, two findings are of special
importance: ~1! Near the end of the reaction interval, the H reflex
suddenly increased when the muscle was involved in the response
and decreased when the muscle was not involved in the response;
and ~2! the compatibility of the mapping specifically affected the
processing operations performed before the task-related changes in
H-reflex amplitude. These two points will be discussed briefly
below.
Modulations in H-Reflex Amplitude During Reaction Time
An important result of the present study is that it is possible to
elicit H reflexes in the flexor pollicis brevis by stimulating the
median nerve during RT. This condition was necessary to address
information-processing issues by combining reflexogenic methods
with usual choice RT tasks ~see also Romaiguère et al., 1997!.
Using a foot choice RT, Eichenberger and Rüegg ~1984! had demonstrated a specific facilitation of the H reflex in the soleus involved in the to-be-performed response. In most of their subjects,
Spinal excitability during choice reaction time
391
Figure 3. Amplitude of the H reflex in Z scores ~ordinate! as a function of the time at which it occurred before the onset of the
voluntary electromyographic activity ~abscissa!. Because the trials in which the voluntary electromyographic activity began before the
end of the H-reflex window were rejected ~see text!, it was not possible to obtain any H-reflex value later than 15 ms on average before
the onset of voluntary electromyographic activity ~this value is an average because the width of the window was adjusted individually
for each subject between 13 and 20 ms!. The vertical dotted lines show this exclusion window. The time from 215 ms backwards is
divided into 20-ms bins. The boundaries of these bins are depicted by the ticks on the abscissa. In each bin, we have calculated the
median amplitude of the H reflexes that fall into this bin and this value is indicated at the midpoint of the corresponding bin as a filled
~responding muscle! or as an open circle ~nonresponding muscle!.
this change in spinal excitability was restricted to the muscle involved in the forthcoming movement. However, Eichenberger and
Rüegg also reported that in one athletic subject that the H reflex
elicited in the noninvolved soleus became slightly inhibited by the
end of the RT interval. In the present study in which the subjects
had extensive practice with RT tasks, the change in spinal excitability was twofold: The H reflex was facilitated when the muscle
was involved in the response and depressed when the muscle was
not involved in the response. Now, does this symmetrical pattern
result from the intrinsic spinal connectivity or does it reflect the
central motor command? Such a balance in excitability is of course
reminiscent of Sherrington’s ~1906! reciprocal inhibition 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!. However, to our knowledge, this has been described between the flexors and extensors of
the same joint but not between homologous muscles such as the
flexores pollicis brevis.
There is a possible relationship between the balance in excitability observed in the present experiment and the spinal circuit
responsible for a bilateral reflex, the flexion withdrawal-crossed
extension pattern. A noxious stimulation of the skin on a part of a
limb elicits a reflex of flexion at the joints proximal to the stimulation site. Within the spinal cord, segmental neurons crossing to
the contralateral cord cause the activation of the extensor motor
nuclei on that side. Admittedly in our study, the electrical stimulation necessary to elicit an H reflex caused a smarting of the skin
that could have recruited the nociceptors at the origin of such a
reflex pattern. However, the time course of the changes in reflex
amplitude does not appear to be compatible with such an interpretation. Indeed, the crossed extension should manifest itself irrespective of the time of stimulation whereas, in our study, the difference
in excitability between the involved and noninvolved motor nuclei
occurred only during the last 35 ms preceding the voluntary muscular contraction. Therefore, we favor an interpretation in which
the balance in excitability evidenced in this study reflects a property of the central command rather than the spinal circuitry. One
possibility is, for instance, that the central command specifies both
a removal of the presynaptic inhibition of Ia afferences to the
involved a motoneurons and an increment of the presynaptic inhibition exerted of Ia afferences to the contralateral noninvolved a
motoneurons. Such a bilateral balance mechanism may serve to
prevent erroneous responses by reducing the sensitivity of the
noninvolved motor nucleus to the servo-control of the proprioceptive reflex loop ~Smith, Roberts, & Atkins, 1972!. This balance in
392
T. Hasbroucq et al.
excitability can be viewed as evidence for a between-limb response competition ~in the sense of Sherrington’s reciprocal inhibition!, a mechanism often assumed by human psychologists to
account for their results ~see, e.g., Eriksen, 1995, p. 105! but for
which—to the best of our knowledge—no direct physiological
support has yet been provided in awake primates.
Implications of the Present Findings
for Cognitive Architecture
The second point that deserves comments is that the motor processes reflected in the changes in H-reflex amplitude are unaffected by the compatibility of the stimulus–response mapping.
This entails that the effect of mapping on RT occurs entirely
before the task-related modulations in spinal excitability. Indeed,
the present results show that mapping compatibility influences
some processes while sparing the motor processes, which supports the “selective influence” and “constant output” assumptions. On the other hand, they suggest that the information is
transmitted discretely from response selection to the stage reflected in the changes in H-reflex amplitude. This outcome is
exclusively compatible with a discrete, all-or-none transmission
between the response selection stage and the subsequent motor
processes and supports the assumptions of selective influence
and constant output often incorporated in serial architecture models. In particular, they corroborate the information-processing
model underlying the additive factor method ~AFM, Sternberg,
1969!. This method has been elaborated under the assumptions
that stage durations constitute additive components of RT and
that there exist experimental factors whose manipulation affect
the duration of specific stages, which implies output constancy
and discrete between-stage transmission.
One might object that our results constitute weak evidence in
favor of the AFM because the modulations of spinal excitability
occur shortly before the onset of the response and that these changes
might implement some late ballistic processes initiated by a discrete pulse from earlier cognitive processes. If such were the case,
the present results would not allow one to decipher the nature of
information between cognitive stages. This, we maintain, is unlikely. Recall that in our study, RT was measured as the onset in
change of EMG activity of the agonist muscles occurring about
100 ms before the closing of the response switch ~see, e.g., Smid,
Mulder, & Mulder, 1990!, which means that the changes in H-reflex
amplitude anticipates the behavioral response by about 125 ms.
Now, several studies have shown that different “cognitive variables” affect the interval lasting from the change in electrical muscle activity and the overt response ~e.g., Coles et al., 1985;
Hasbroucq, Akamatsu, Mouret, & Seal, 1995; Smid et al., 1990!.
These findings suggest that different cognitive operations occur
during this motoric portion of RT. Because the changes in spinal
excitability reported here do occur before any detectable voluntary
muscular activity, they are unlikely to implement a last noncognitive ballistic stage of RT.
Now, we must acknowledge that the AFM has been criticized
on several grounds and that a number of studies have provided
empirical evidence against its basic assumptions. Most of this
evidence comes from the analysis of brain potentials recorded
during bimanual task involving multiattribute stimulus configurations ~e.g., Miller & Hackley, 1992; Osman, Bashore, Coles,
Donchin, & Meyer, 1992; Osman, Moore, & Ulrich, 1995; Smid
et al., 1990; Smid, Lamain, Hogeboom, Mulder, & Mulder, 1991!.
In these studies the dependent variable of interest was the difference, called the lateralized readiness potential ~LRP!, between the
electrical brain activity recorded over the ipsilateral and contralateral motor cortices. The results obtained in the framework of this
approach suggest that the stages located upstream from response
selection transmit partial information about some stimulus attributes
to the motor stages before the stimulus configuration is completely
identified. In contrast to most of these studies ~see, however, Smulders, Kok, Kenemans, & Bashore, 1995!, the present study addressed the issue of how the information conveyed by the unique
relevant feature of a single-attribute stimulus is transmitted from
response selection to the motor stages. It must thus be stressed that
the present study is particular both in terms of the physiological
variables analyzed, and in terms of the task performed by the
subjects. Future research should specify the functional meaning of
the presently available electrophysiological variables and determine how the task properties may govern the implementation of a
given functional architecture.
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~Received November 17, 1998; Accepted June 21, 1999!