The processing of proprioceptive signals

Ncuropsychologia. Vol. 17. pp. 683 10 687. P Pergamon PrcrsLtd. 1979. Primedin Grear

0028-3932

Britain.

79il201-0683SO2.00~0

NOTE THE

PROCESSING

Discipline,

The Flinders

OF PROPRIOCEPTIVE

SIGNALS

D. J. GLENCROSSand M. M. KORESIAS Psychology

University

of South I7 April

(Received

Australia,

Bedford

Park,

5042, Australia

1979)

Abstract--Simple and two-choice reaction times were investigated in two experiments using proprioceptive stimuli. The form of the stimulus was the release of the passively supported forearm. The responses were to halt the falling arm and to activate a microswitch held in the hand. Latencies were also determined from the EMG activity. The findings indicated that the latency of two-choice situations were not significantly different from the simple situation, and that compatible responses were significantly faster than incompatible responses.

OF PARTICULARinterest

in the understanding of motor control is the role of proprioception, because of its intimate relationship with movement, through spinal and supraspinal feedback processes and because of the recognition of specialized organizational mechanisms (I, 3, 3, 4, 51. There have been several approaches to the investigation of proprioception, including the direct study of the latency or reaction time to proprioceptive stimulation and the investigation of amendments to movements based on proprioception [6]. These two approaches have suggested that proprioceptive information processing may be different from the visual and auditory system. For example, the early work of CHERXIKOFFand TAYLOR [7] reported mean proprioceptive reaction times of I29 msec and II9 msec for two groups of subjects. There is considerable evidence of very rapid amendment times, based on proprioceptive signals. HIGGIX and AXCEL [5] reported mean reaction times of I36 msec to the displacement of a joy stick and amendment times of 98 msec to movements in the wrong direction. In a similar situation, MEGAW [9] reported a mean error correction time of 92 msec. Do these rapid processing times indicate some special feature of the proprioceptive feedback sbstem? The present study undertook to investigate directly simple and two-choice propriocepiike reaction time situations to determine whether the function is the same that accompanies visual, auditory and tactile conditions, or whether the proprioceptive system is especially designed for rapid responding. even in dual or multiple stimulation situations. There appears to be no evidence in the literature on choice proprioceptive reaction times. It was proposed to use sudden limb displacement as the proprioceptive signal, the response being to halt the falling limb. Reaction time was determined from EMG, and a microswitch activated by a finger response. The EMG signal that was used to trigger the timer was the muscle action potential, M3, associated with the voluntary phase of the movement [I, 41.

EXPERIMENT Twelve male subjects with an age range assessed by a verbal questionnaire.

from

I-METHOD

19 to 30 yr were used.

All were right-hand

dominant

as

ApparoruJ The proprioceptive stimulus was provided by the release of the subject’s forearm, which was held at right angles to the upper arm, which in turn was held vertically to the side of the body. Both the right and left forearms were supported by nylon cords attached to light steel pins inserted into electro-mechanical, rubber mounted solenoids and at the wrists by leather straps. White noise was used to mask extraneous auditory cues. EMG activity was recorded from the biceps brachii and triceps brachii muscles of each arm of the subject using surface electrodes placed 3 cm apart along the longitudinal axis of the muscle.

683

NOTE

684

The muscle activity was measured by two fast, full wave EMG integrators, which were used to trigger two timing counters. A comparator device that allowed for adjustments of the threshold level of the muscle action was incorporated into the EMG integrators. Displacement of potential, which would trigger the counters, the forearm was recorded by using a 180’ rotary potentiometer. T\so microswitches, one held in each hand and operated by depressing the thumb, were used to record the ‘manual’ reaction time to the proprioceptive signal. The four channels of EMG, the displacement record, the moment of release of the solenoid. the EMG signal which triggered the timer, and the activated microswitch were all placed on the U-V paper record of an eight channel physiological recorder (Devices Limited Type M 19). The paper speed was 50 mm,‘sec. Experimenral

There

design and procedure

were four treatment

conditions:

(i) Simple reaction time (S,R,), in which the stimulus was the release of the right forearm to which the response was to stop the movement and at the same time press the microswitch held in the right hand. The procedure was repeated using the left arm. There were a total of 20 test trials, IO with each hand. (ii) Two-choice “go, no-go” situation (SLR,), in which the two stimulus conditions were the release of either the right or left forearm in a random order. For the first 20 trials, if the right forearm release was the stimulus, the response was stopping the right arm and microswitch; if the stimulus was the release of the left forearm, no response was made. For the second 20 trials, the situation was reversed, whereby the response was made with the left arm to the left forearm release, whilst there was no response to the right forearm release. (iii) Two choice situation (S,RL), in which either arm could be released in a random order, and the response was the stopping of the arm which was released, together with the depressing of the corresponding microswitch. There were a total of 40 trials, the stimuli being presented in a randomized order. (iv) Two-choice incompatible situation (f.SLRI), in which the arm opposite to that released responded by moving upwards, at the same time depressing the microswitch. Thus if the right forearm was released, the left forearm responded by being flexed and the microswitch depressed. There were a total of 40 trials, the stimuli being presented in a randomized order. The presentation of the stimulus was always preceded by an auditory warning signal indicating a randomized foreperiod of l-4 sec. The 12 subjects completed the four treatment conditions in accordance with a counterbalanced 4 x 4 latin square design, three subjects being allocated to a particular order.

RESULTS

AND

DISCUSSION

Two sets of reaction time scores were available for analysis, namely, those based on the EMG and the microswitch. The diff‘erences between the four treatments conditions were significant; EMG, F(3.33) = 17.65, P < 0.01 ; these differences are largely attributable to the delays microswitch. F (3.33) = 60.56, P < 0.01. However, in the incompatible condition. The difference between simple reaction time (S, R,) and two-choice reaction time (SIRI) is I6 msec (EMG records) and 23 msec (microswitch records) (see Table I). Comparing the simple situation (S,R,) with the two-choice “go, no-go” condition (SLRl), the reaction time is lengthened 27 msec (EMG) and 38 msec (microswitch). These differences just reach significance (P < 0.05) and can be attributed largely to the increased stimulus processing in the choice situation, as the response condition is assumedly the same in both the simple and choice tasks.

‘able

I. Means

(msec)

and

S.D.

of the two reaction time measures Experiment I

on the four treatment

SIR,

SzR,

S>Rz

IS2RZ

EMG Mean S.D.

II7 28

144 45

133 36

203 78

Microswitch Mean S.D.

154 28

192 53

177 40

285 77

conditions

in

NOTE

685

However, these results seem inconsistent when the two, two-choice conditions are compared. In the twochoice (S,R,) and two-choice “go, no-go” (SIR,) conditions, the latency of the latter is lengthened I I msec (EMG) and I5 msec (microswitch). Although these differences are not significant, the implication is that the “go, no-go” (S,R,) situation is more complex than the .SIRL condition. This indication or trend may be explained by the fact that the stimuli have different codes, viz. the right stimulus means respond with the rtght arm, whilst left stimulus means do not respond with the left arm. If the compatibility is reduced so that the response is made with the arm opposite to that stimulated, then the latency lengthens significantly. The differences are 70 msec (EMG) and I08 msec (microswitch). A second experiment was conducted that permitted an interactive analysis of stimulus and response effects, after STERNBERG(IO].

EXPERIMENT

2-METHOD

Subjects

There

were eight subjects,

Experimental

four males and four females,

with a mean age of 52.5 yr.

design and procedure

There were four treatment

conditions,

and the procedure

was essentially

the same as for Experiment

I.

(i) Simple reaction time (S, R,), involving one stimulus and one response as used in Experiment I. (ii) Two-choice situation (SIR,) in which either the right or left arm was released in a random order, to which a response was always made with one specified arm. Following IO trials in which the right arm responded, there was a second batch of trials when the left arm responded. (iii) Two-choice situation (.S2R,) in which the right arm responded to the right arm release and the left arm responded to the left arm release. The order of the stimuli was randomized as in Experiment I. (iv) Two-choice situation (S, R2) in which to only one stimulus either the right or left arm response could be made. The subject was told that one arm would be released (e.g. the right arm), but that the subject could choose with which arm he responded. He was, however, required to randomly vary the responding arm and furthermore was advised to try to make the decision when the stimulus occurred, and not in advance of the stimulus. There were IO trials with the right arm as the stimulus, followed by IO trials with the left arm as stimulus.

RESULTS

AND DISCUSSION

The results of Experiment 2 are based solely on the EMG records (see Fig. I ). The main effects of conditions were not significant: there were no significant main effects for stimuli, F(I, 7) = 0.54, P > 0.05, or for the number of responses, F(I, 7) = 0.41, P > 0.05, but there was a significant two-way interaction. responses r stimuli, F(l, 7) = 6.43, P < 0.04.

150-

1403 3 I- 1309 ; z 2 120s v

3, .

.

‘\. ‘\5 /

*__--e---3 . )

110.

1

FIG. 1. Reaction

times for all the data

and for the compatible

data

in experiment

2.

686

NOTE

It is apparent in conditions SrR, and .S, RJ that there are a combination of same arm (compatible) responses and opposite arm (incompatible) responses. If the results of Experiment 1 are analysed on the basis of compatible data alone. then there are no signiticant main etTects of responses F (I, 7) = 2.23, P > 0.05, stimuli. F (I, 7) = O.SI, P > 0.05 or interaction effects, f (I. 7) = 0.47, P > 0.05. There is a slight trend for the two response situations (S, RI and S: R2) to ha\e a larger latsncy than the single response conditions (S, R, and .SLR,), but this is not signiticant. That is, if two responses habe to be diferentiatcd. the processing time increases by only 6 msec oker the single response conditions. If the stimulus conditions are compared, the increase in latency of the two stimulus conditions over the one stimulus condition is only 2 msec. which is not significant. Incompatible responses are significantly longer than compatible responses, F(I, 14) = 32.72, P < 0.01.

DISCUSSION The results of the present experiments suggest that the proprioceptive system has specialized features in the processing of feedback information. In the compatible (same arm) conditions, when the arm is dropped. activity is set LIP in the gamma motoneurons, causing the intrafusal fibres to contract, and directly or indirectly influencing the alpha system, enhancing acerent information which is the basis for the voluntary responses. Further, the MZ component in the EMG responses [I, 11 of 55-60 msec possibly involves the reticular mechanism. facilitating arousal and attentional processes. Thus in the compatible condition there seems to be a series of feedback loops for facilitating the response. setting up tensions in the muscles to preserve and facilitate the processing of afferent information, preparing muscles to initiate the appropriate responses and orienting attention to the muscle (movement) groups involved. All of these mechanisms are not operational in the incompatible (opposite arm) responses, resulting in an additional delay of some 70- IO0 msec. The etfect of choosing between two stimuli (stimulus identification) or two responses (response selection), seemed to have little intluence on the latencies, compared with the simple no choice situations for the compatible data. This finding is not consistent bvith the comparable situations for visual, auditory or tactile modalities [I I, 121. Rather, the data argues in favour of an attention-orientation model suggested by TREVARTHEN [I31 and DLDFtELD [IJ], emphasizing that the attention-orienting properties serves to reduce processing load before the information reaches cortical level.

REFERENCES I. 2. 3. 4. 5 6 7. 8. 9. IO. I I. 17. 13. 14.

COOKE, J. D. and EAST~IAN, M. J. Long-loop retlexes in the tranquilized monkey. E.rp/ Brnin Res. 27, 491-500, 1977. EVAKTS, E. V. Brain mechanisms in movement. Scienr. Anr. July 1973, 96-103. EVAKTS. E. V. and T~~\JI, J. Gating of motor cortex reflexes by prior instruction. Brain Res. 479-494, 1974. LEE, R. G. and TATTON, W. G. Motor responses to sudden limb displacement in primates with specific ens lesions and in human patients with motor system disorders. J. Con. Sri. ~Vel~rol. 3, 255-293, 1975. MARSUE>, C. D., MERTON, P. A. and MORTON, H. B. Servo action in human voluntary movement. iVntl,re, Lord 238, 14-143, 1972. GLES~KOSS, D. J. Control of skilled movements. Ps,vcho/. Bull. 84, 14-29, 1977. CHER~IROFF, R. and TAYLOR, F. Reaction time to kinaesthetic stimulation resulting from sudden arm displacement. J. e.rp. Ps~cllol. 33, I-S, 1957. HIGGINS, J. R. and ASCEL, R. W. Correction of tracking errors without sensory feedback. J. exp. P.~ychol. 84, 4 12-4 16, 1970. ME~~AW, E. D. Directional errors and their correction in a discrete tracking task. Er~orro~?lics 15,633-643, 1972. STERNRERG, S. The discovery of processing stages: extensions of Donder’s method. .Jcrn p.~,vchol. 30; Arrmion ord Performnnce 11. W. G. KOSTER (Editor). pp. 276-3 15, 1969. LEONAI
On a Studi dans

2 experiences

consisxit

les temps de reaction

utilisant

au relachement

ment.

5~s r6ponses

temps

que d'activer aussi

determinks

que

les latences

msnt

sixples plus

d'apres

differentes

et que

rapides

Deutschsprachige

d'arreter

dans

le mouvement tenu dans

l'activite

de celles

les reponses

bestand

unter Verwendung bestanden

en meme

Les latences

Les resultats

dans

etaient

ne sent pas les situa-

siqnificative-

incompatibles.

wurden

propriozeptiver

in zwei Experimenten Keize. Der Stimulus

eines passiv unterstiitzten Unterarms. darin, den fallenden

kleinen Schalter

zu bedienen,

Die Latenzzeiten

wurden

Die Ergebnisse

passive-

de chute

a 2 choix

constaGes

Le stimulus

support6

Zusammenfassung:

im Loslassen

Antworten

FXG.

compatibles

Einfache und Zweiwahlreaktionszeiten untersucht

et 3 2 choix

la main.

les situations

les reponses

que

sixples

proprioceptifs.

de l'avant-bras

l'interrupteur

@taienz

tlons

stimulus

brusque

Qtaient

montrent

siqnificativement

des

der in der Hand gehalten wurde.

demnach durch EMG-Aktivitgiten bestimmt.

zeigten, daf3 die Latenzen

auf die Zweiwahlsitua-

tionen sich nicht signifikant

von der einfachen

schieden und dafl zweckm2ssige

Antworten

als Knzweckmgssige.

Die

Arm zu halten und einen

Situation

signifikant

un'cer-

rascher kamen