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The central control of sensory transmission and its possible relation to reaction time
Acta Psycholog
rformmce II ( W. G. Koster, ed.) 1969, 339-357 0 North-Holland Publishing Company, Amsterdam
A. ANGEL of Physiohgy,
he University,
Sheffield IO, England
Itisshown that the amount of information
reach ng the cerebral cortex after the second of a pCr of equal intensity stimuli appFed to the same peripheral me semlsorymodality varies inverse with the stimulus intern the stimuli. For a simple stim,ulus activated task the reaction time d to the information reaching the cerebral cortex by the equation: d= kl i- k2 (RT-L). Where log is the psychological magnitude of the stimulus kl and kz are constants, RT is the reaction time and L is the latency ofthecerebral response evoked by the stimulus in the primary cortical receiving
1. INTRODUCTION t has been shown by many ARSHALL (1941), JARCH~(1949), d A~~ASSIAN(1958) that in cats MOUNTCASTLE et al. (1952), c anaes retisecl with bar the responses recorded from the ckq?lj’ e cerebral cortex to, the second of a primary sens y receiving area 0 of peripheral stimuli become reduced in size when the interval rating the two stimuli is between 40-150 msec. When the two stimuli are separated by 30-40 msec no responses could be obtained to the secwd stimuli of the pair. In the rat and coypu deeply anresthetised no responses with trichloroethylene, urethane, barbiturates or fluotha were obtain& from the cerebral cortex to the seco of a pair of peripheral stimuli when the interval of separation was lo-50 msec, and nses did not recover fully unless the stimuli were separated rsec-1 see (ANGEL, 1967). In some preparations the cortical responses to pairs of stimuli separated by 2-10 msec showed summation (hiGEL, 1963, 1967). Furthermore, it was also shown that as well as the deerease in size of the cortical responses to the second of of stimuli the response latency became increased (ANGEL, 1967). of the decrease in the size of the cortical response to the second of a pair of peripheral stimuli has been shown to be due to a decrease in the ability of the venuobasal thalamus to transmit ascending information. MAXSHALL (1941), ANGEL (1967); and ANDERSEN et al. (1964) 339
340
rbiturates a cu have shown that in the cat anaesthetised with thalaunic volley causes a prolonged hyperpolarisation of cells located in the ventrobasal thalamus. When two stimuli are delivered to a human subject who has to a positive reaction to the second it is found that the time taleeli to respond to the second of a pair of stimuli varies inversely interstimulus interval (cf. SMITH, 1967; WELFORD, 196’7). Various hypotheses have been advanced to explain this phenomenon, involving either the strategy of the subject (ELITHORNand LAWRENCE, 1955; .A.NNETT,1966) or the limitations imposed by the handling system I@VELFORD, 1952; DAVIS, MT). It is the intention of this pa that the physiology of transmission by the central nervous be adeqtiate, under certain circumstances, to explain the behaviour rsf human subjects to paired peripheral stimulation. 2. METHODS 2. I. Animal experiments The animals were either anaesthetised with urethane 1(1.5-l.8 g/ OF were unanaesthetised with recording electrodes implanted into the skull; or for two experiments cats were used which had had, under deep &her anaesthesia, a section of the neuraxis just rostra1 to the exit of the trigeninal nerve; a midpontine pretrigeminal preparation (BATINIet al., 1%9). The anaesthesia was then discontinued. In the anaesthetised animals access to the cerebral cortex and thalamus was allowed by an extensive craniotomy, on the left hand side, after reflexion of the temporalis muscle. The dura mater was opened and reflected. To expose the medulla, the neck muscles were reflected back from the base of the skull and the arch of the atlas and some of the skull overlying the posterior part o the cerebellum were removed. The cerebellum was always left intact. The animal was held firmly in a stereotaxik: frame. The skin of the head was clamped between an inner perspex ring and an outer metal clip. The pool so formed over the cerebral cortex was filled with liquid paraffin B.P. (which had been saturated with physiological saline) at a temperature of 37OC. The animals were kept at a rectal temperature of 37OC by placing them over a small radiator through which water at 39OC was circulated. The electrodes used to record potentials from the surface of the cortex were of dver wire, insulated except at the tips, which were fused into smalJ balls. One of these was placed over the primary somatic
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solution and with a resist-
er cathode-follower was reparations a concentric hiasm under stereotaxic
lectrical stimuli were applied to the periphery by means of lint ne pad was wrapped around the wrist a negative electrode. The pressu r er the electrodes was kept as 910~ gular pulses of lOc! psec duration ‘ble. The stimuli were ret as of the stimuli was controlled from olated from earth. The tir an a digital timing unit (Digitim=r, Devices Ltd.). Stimuli were also delivered via the glass micropi ette, in which case the pipette was made the negative electrode, the positive electrode being clipped onto the neck muscles. Average records of the responses e made with a special purpose digital computer (Biomac 10001, ta Latiratories Ltd.). The site of the microelectrode was determined by histological examination of the tissues after the nervous system had been fix-a with the microelectrode in situ. 2.2.
urnan experiments
Electrical stimuli were applied to the periphery by mears of lint soaked in 3 M NaCl wrapped around the index l(negative electrode] little fingers. Recording elect:rodes were affixed to the scalp over the primary cortical receiving area (~~AwsoN, 1947, 1950, 19%). The rees were amplified and averaged with the special purpose digital ter. The MT was measured in one ot”’two ways: either the stk~ulus started a digital clock counti:ng in msec which was stopped
342
A. ANGEL
a button; or the stimulus started the digi its stores at the rate of 1/msec; pushing the button then caus crement of the store location identified end of the experimental period the contents of the read out in the form of punched paper ta 3. &iSULTS For convenience the results can be divided i is concerned with the experiments on the transmission o formation in animals. The second with the behavio to peripheral stimulation. 3.1. Animal experiments X1.1.
Paired stimuli
The responses to paired stimuli applied to the periphery have been recorded at three sites along the dorsal column sensory pathway. At the 1~~1s of the first sensory synapse, the cuneate nucleus: ~nsory synapse, the ventrobasal thalamus and the third sensory synapse in he cerebral cortex. Ex;z,mination of the responses recorded from the cuneate nucleus showed that, in general, the size of the post-synaptic mass response to the second of a pair of electrical stimuli applied to the for unchanged unless the interval between stimuli was 15 msec o latency of the naptic mass response was, in the majority of experiments, una with separations of the stimuli as little as 3 msec (ANGEL, 1867). In some experiments a small increase in the response latency was observed with separations of stimuli of 5 msec or less. 1C shows the effect of p&=ed stimuli on the siize and latency of the post-synaptic mass response recorded from the cuneate nucleus in a rat deeply anaesthetised with urethane. Each point on the graph is the mean of twenty consecutive responses. When the responses from cells located in the ventrobasal thalamus were studied it was found that the si;t.e of the post-synaptic mass rense of a collection of cells or the probability of discharge of single in the deeply anaesthdxd rat, was unchanged if the stimuli were sepa’ked by 500 msec or more. With intervals of less than 500 msec the size, or probability of discharge, decreased proportionally with the stimulus interval, until with intervals of 30-40 msec or less the second UIUSdid not e tit a response. At the same time as the decrease in
1 mscc
onses to the second of a pair of peripheral the stimulus interval in the anaesthetised rat B and CJ and in the unanaesthetised rabbit behaviour of a single cortical cell, B a single thalamic cell a?d C the post-synaptic cuneat; mass response. The circles indicate *t--C grcbahility of cXllUlai discharge or percentage size of the CL&U
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cuneate response, the dots the mean latency of the responses. 40 consecutive stimuli the Bf the cells responded 40 times rcentage shows the mean probability was plotted as unity. size of the first positive wave of the cortical evoked response (circles) and the mean latency (dots) to 26r consecutive stimuli.
io
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344
AJWGEL
the mass response size or the robability of discharge, the tern of latency the post-synaptic responses became inc li were 100-300 change was always the same. In the rat, when msoc apart, the ktencies of the responses to the second stimulus th shorter intervals sed. An example and response latency of a single thalamic cell as a fu stimulus interval is :shown in fig. 1 Records from the cerebral cortex showfti the same re to paired stimuli as did the responses from the ventro The area of cortex which was stulied was that which g1 latency responses to peripheral stimulation (ANG haviour of the response probab lity and response lat cortical cell to paired periphera stimuli has been pl The behaviour of the mass corti I response recorded from the primar; somatic receiving area of the cortex of an unanaesthetised ra implanted electrodes is shown in fig. 1D. It can be seen that, in essence, the: behaviour of the cortical response to paired stimuli was the same as that shown by the deeply anaesthetised animal (compare rig, 1A and ID,); except that in the unanaesthetised animal the cortical res shows a recovery to closely spaced, 1040 msec, stimuli. This t behaviour though less marked has also been seen in anaest animals (&GEL, 1967). Thus if one accepts the thesis that the amplitude of the post-syn mass discharge, or the probability of discharge of single cells, ret from a nucleus gives an indication of the size or effectiveness of the vdky transmitted by the nucleus, then these observations indicate that the: decrease in responsiveness seen at the cortex occur& maimy as a consequence of the decreased thalamic transmission to the second of a pair of synchronous ascending volleys. This observation has been conf!irrned in anaesthetised animals by comparing the cortical responses to paird stbuli applied to cuneo-thalamic and thalamo-cortical fibres. It is found that stimulation of the presynaptic thalamic fibres gives a respmsc pattern to paired stimuli essentially similar to paired peripheral stimuli, whereas paired stimuli applied to post-synaptic elements show that at the time when the responses to the second of a pair of stimuli applied to the presynaptic fibres are reduced in size or absent, the cortical responses to the same separations of stimuli applied to the st-synaptic elements are unaltered or increased in size (ANGEL,1967).
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haviour has been found in animals without central ows the responses to the first and seco tion of 50 msec applied either to the optic chiasm tical f&e.; in a mi pontine pretrigeminal cat.
Fig. 2. Responses recorded from the primary visual cortex in a midpontine pretrigeminal cat to the first and second stimuli (1 and 2) of a pair ssparnted by 50 msec and applied to the optic chiasm (A) or the geniculo-cortical fibres (B). Each record r;;hows five superimposed responses. The horizontal line represents 10 msec, the ~rtical one 1 mV. Positivity at the active electrode is signalled as an upward deflexion in this and subsequent figures.
3.1.2. Interpretatiorz 0 f the cmticul mm resporzse The complex cortical mass response to peripheral stim be divided into three major components for convenience and descriptive These are a first positive deflexion (labelled P, fig. 3A) by a first negative deflexio (labelled N, fig. 3A) and lastly positive deflexion (labelled 2 fig. 3A). The evokeo zzsponses from the primary somatic receiving cortical area in the anaesthetised monkey and the unanaesthetised rabbit to single and paired stimuli are shown in fig. 3. They show another feature of the changes in the responses to paired stimuli, in that in the deeply anaesthetlsed animal (fig. 3A) with intervals of separation of 200 msec or less the shape of the responses becomes altered. With decreasing intervals of separation the cortical response usually consisting of a positive wave only. In the relatively lightly anaesthetised animal (reflex withdrawal of the hindlimb to a strong pinch jl;st present) and in The unanaesthetised animal this change in the shape of the cortical .responses is not so marked, an.d may not be seen fig. 3B and 3C. In experiments on animals it has been found that the size of the first sitive wave of the cortical response is (a) directly relatled to the ulus strength (fig. 4A), both in the anaesthetised and unanaest
346
A.
ANGEL
Averaged responses recorded from the primary sensory cortex of a deeply anaesthetised rat (A), a ‘lightly’ anaesthetised monkey (B) and an unanaesthetised rabbit (C). The responses to a sin le stimulus alone (I), to the second of a pair at a separation of 600 (II) and 100 msec (III) are shown for c,:ach animal. The separation in (IV and V) are 30 and 10 msec (A], SO and 20 rnsec (B) and 60 msec (C IV). The horizontal ruling sents 10 msec: intervals. The vertical calibration represents 1.5 mV for 50 JN for (B) and 500 yV for (C). 60 consecutive responses to forepaw stimulation at a rate of x set were averaged.
t&d preparation, (b) shows exactly the same behaviour to paired s;timuli as the post-synaptic mass responses recorded from the ventrow there is an almost basal +&alamus (fig. 1A and B, ANGEL, X967), halan-& response linear relation between the size of the post-syna z:nd the first p&tive wave of the cerebral evoked response tf;g. 4D) ZIIXI(d) when the size of the thalamic response is increased by preceding s; imulus to a forepaw %y strong stimulation applie+danywhere OX t surface the first positive wave o the cortical response is also increased in size (ANGEL and DAWSON, 1961, 1963).
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AND REACTION
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Fig. 4. “Phis figure shows the relation between the first positive wave of the cortical response (A) and the first negative wa (B) versus the stimulus strength; and the xclation between the first positive an
negative waves (C) in an u!n-
anaesthctised rabbit. (D) shows the relation between the percentage probability of response of a thalamic cell (ordinate) versus the percentage size of the first positive wave of the cortical response (abscissa) of a rat deeply anxsthetised with urethane. Each point on the graphs is the mesn of 40 consecutive responses.
egittive wave of the cortical sponse also shows a direct relation to the size of the stimulus, (fig. 4 sl~ouvsthe same behaviou,to ired stimuli as the first positive wave of the ce sponse (ANGEL, 19671, and also shows exactly the same o single cortical cells responding with e size of the first negative wave is also f the first positive wave of the co (ANGEL,1967, fig. 4C). n fact it has been found that the size of this nent of the cortical response is directly relat probability of cortical cells (ANGEL and would seem, therefore, that the size of the first positive wave of the
A. ANGEL
rough measure the size of the volley asand the size of the first negative wave of the ugh measure of the initial response of the
crf irerarivepetiph?td stinaaciation
ts may experience difficulty in the digits if they are separaited Al), whereas they have no difficulty in retrk applied to the skin of the r sec. Thuts there: is an apparent f the nervous system to brief, large, ore normal peripheral stimuli. OUNTCASTLE (19599 lt,kt id stimuli at rates up to s of the deeply anaesthei ilt is found that the first skes a norma response. The second stimulus of a pair of stimuli at the show a gradual recovery reaching a steady level which depends on, A graph of the sizes sf the first s to iterative stimulation al various
ems the subjects were presented with digits, a 1 msec click, or a 1 msec ng 12’ at the eye. The stimuli were cutaneous stimuli the subjats had fe.tt the shock, or the second of 31pair t%ne from al digtal clock, reset the Going through this procedure made it ue, For the auditory and the subject was time. Those subjects
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Fig.
5. Shows the percentage size of the first positive wave of ~.he clerical response ~CBeach stimulus of a train: la) at 100 msec (circles), 20 a5 %I m (large dots), 23 at 40 msec (triangles), 30 at 30 msec (squares) and 50 ;at 20 m separation (small dots).
fig. GA). The reaction times to 300 consecutive cutaneous stirn~~~ either alone or paired plotted as histograms are shown in fig. early parts of the cerebral evoked responses to the same stim shown in fig. 7. It can be seen that the reaction times may ~XS, relation both to the mean latency of the cortical response and t of the first positive wave of the response. In fact, the behaviour cerebral responses of man to paired stimuli is exactly the of the rat, rabbit, or monkey, the mean latency of the cerebral responses increasing as the stimuli are brought closer and t response decreasing. That the major factor in any relation reaction time arnd the cortical response will relate to first positive wave rather than the latency is shown by th reaction time is altered dramatWl,y by increasing the stimulus (fig. 623). Increas.ing the stimulus st.rength howe the latency of the cerebral evoked response of the first positive wave, fig. 7EXX It is of inte of
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GEL
ii
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T:
the stimuli were delivered in a regular time sequence there evidence at all that ll:herewas any process of learning 32.2.
esponses $0 trains of stimuli
For this experiment the subjects were asked to press the bu they bad seen the Jlast flash in a train of four at a rate of msec. It was found that the reaction time to this stimulus was i when compared to the reaction time to a single flash but less rezxtion time to thee second of a pair of st,imuli at the same se The results plottti as histograms for four subjects are sho
Fig. 7. This f~igur~ sbows the averaged cerebral subject as in fig. 6 performing a response) to a sin digits (A) and to the second of a pair separated by 3 and 50 msec (II) and to, two stimuli separated by 10 msec at -0, and 2.3 X &reshCl~fd(G). 3 averages of 100 consecuti sulperimposed in A-El+ 2 averages of LOOresponse cGbrati0n repil=sents 40 m:;ec, the verti
3.2 .ti3.
Pairs of sthurli in different modalities
animals it is found that in order to obtain the deer ticas response to the second of a pak of the same modality and applied to the not too far apart spatially. In these ex distinction between the occlusive eff same peripheral lucus and the phenom III\
35
. ANGEL
352
uninfluenc T_herefore, the cortical response to a flash would : preceding stimulus applied to the digits. It was fo time to a flash was unaltered or sli tly decreased by flash with a click. The click-flash se ration was 100 msec. from four subjects are shown i time to a single flash war3239 msec, to the by a click or an electric shock to the digits it was respectively.
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Fig. 8. This figure shows histograms of the number of responses vmw the time of tirIe response to the nearest msec for 4 different subjects in resgsnw to (from top to bottom of each group) a single flash, the seesnd of a pair of flashes separated by 100 msec, a flash preceded (100 msec) by a click and the fourth flash of a train at a separation of 100 msec. The fifth histogram in A shows the reaction time to a flash of a subject who appeared to be able to predict each time a flash would occur. 4.
~IsUJSSIo1N
Thus i.t has been shown that in anaesthetised animals the cortical responses to pairs oC:peripheral stimuli vary according to t between the stimuli, and that this variation occurs mainly as a decrease in the ability of tile thalamic relay nucleus to transmit t!x second ascending volley of a pair (MARSHALL, 1941); ANDERSEN et al., 1964;
t WCSfound in the
ec or more, or
en shown in the unanasthetised y the same interpretation
cat SCHWARTZ
of ahe surface cortical re-
as well as the information taking a cortex after the second of a pair of less information ab\.jut the stimulus arrives at the cortex, ROSNEK (1961) has shown that if the separation of Qwo electrical stimuli a plied to the digits is from 15-500 msec subjects will underestimate the intensity of the second stimulus. hus the physiology of transmission of two afferent volleys agrees with the psyical observations that the sensitivity of the central system is nal at least as far as the afferent inem now arises of whether or not one can equate the physiological and psychological ‘refractory states” for a simple task which requires a unit output -- press, or not press - to :Lunit
input. Limitations of the handling system suggested by WELF~RD(.l’XZ 1967) and DAVAS (1957) appear inadequate to explain the behaviour of human subject to simple tasks (KOSTER and BEKKER, 1967a,b). Let of the ostulate that the reaction time is some function us therefore, agnitude of the applied stimulus, a parameter psychological should take into account any change in the sensitiAy of the s SHERRINGTC)N (1906)showed that the latency of mally spinat; reflexes
A, ANGlX
354
decreased as the strength of the s must take into account that not only does thz a reaching the cerebral cortex become deer but that it also arrives at the cortex at shown that the psychological the physical m nitude (S) by a M = kSn or 1
so that a plct of log M versus log S gives equal to the value of the exponent. Such a for the stimulus strength and the first posi response fig. 4A, (a&partfrom the stimuli n can make the assumption that a measure of the stimulus .may be given by the log sponse. Further, since there is a linear relation mve and the fir.st negative wave of the c has been shown to be some measure of we may postulate that the initial output psychological intensity of th7 stimulus. RT-L lmsr;) 300
r
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240220. 2001 1800 160UO-
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20
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30
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40
IIC
60
log siar
Fig.. 9. This figun: shows the relation found in the subject whose reaction times and cortical reriponsesare shown in fig. 4 and 7, between the reaction time minus the cortica?in:sponse latency and the log of the size of the first positive wave of the cortical response (dots). The regression line for the points has been plotted.
SE
REACTION TIME
355
on ha:, reached
have as a closed loop servo ich abruptly cha:nges its to contradict in any way ich has been used to explain the beThe pri;sent experiments 1~ ser’ ,ry modality. ?_Jnt in two or three dimen-
A~~~wLE
NTS
esearch Council rpose digital computer used in these inve me a grant to attend
CCLESand T. A. SEARS,1964. The ventrobasal complex of potential field synaptic transmission and excitab of both yre-synaptic and post-synaptic components. J. Pkysiol. 370--399, ission in tbe sensory Ipathwayto A., 1%3. The level of failure of tra , 32-33P. do~eiy spaced stimuli. J. Physiol. 9 iP6P. Cortical responses to paired stimuli applied per sit sites along the somato-sensory pathway. J. Pf ysiol. I the thalamus:
.hKSL,
356 ,~GEL, a. and G. D. DAWSON,1961. Modification
of thal
sensory stimulation. I. Physiol. 1963. The facilitation of rhalamic and --, in the dorsal column sensory pathway by stro tian. Y. Physiol. ANNETT, J., 1966. Payoff: Quart, I exp, Psychol. BATINI, C., G. M~ZRUZZI, Effects of complete pontine transection on rhythm: the m 97, 1-12. a single chanmel inform DAVIS, R., 1957. The human operator Quart. I. exp. Psychol. 9, 11 DAWS~N,D. G., 1947. Cerebral respo nerve in man. I. Neurol. --# 1950. Cerebral responses 6, 326-329. s 1956. The relative excitability and conduction and motor nerve fibres in man. J. Physiol. 131,43 E~LITHORN, A. and C. LA~UNCE, 1955. Central in observations, Quart. 3. exp. Psychol. 7, JARCHO, L. W., 1949. Excitability of cortical af anaesrhesia. I’. Neurophysiol, 12, 447 KOSTEIK, W. G. and I’. A. M. EKKEH,1967a. Some ex’Perimen In: Attention and Performance, A, F. 27, 64-70. and 1967b. Stimulus intensity and the p fractory per& I..I).O. Anr *la1 Progress MAIPSHALL, W. II., 1941. Observations on sub-tort nisms of cats under nembutal anaesthcsia. J. Nturop -, C. N. WOOLSEYand P. BARD, 1941. Ob mechanisms of cat and monkey. I. Neurophysiol. MOUNTCASTLE, V. B., M. R. COWANand C. R. HARRKXIN, representation of some forms of deep sensibility. nerv. ment. ms. 30, 339~-370. and T. P. S. POWELA,, 1959, Neural mechanisms subservin ous sensibility, with special relerence to the role of afferent inhibition in sensory perception and discrimination, Bull. Johns Hopkins Wasp. 105, 201-232. POGGIO,G. I? and V. B. MOUNTC.‘ASTLE, 1963, The functional properties of ven= trobasal thalamic neurons studied in unanaesthetiwd ’ monkey. J. Nc*ophysiol. 26, 775-8~. ROSE,J.@E. and V. B. MOUNTCASTLE, 1959, Touch and kinesthesis. In: Handbook of Physiology, Neurophysiology 1, American Physiological Society, 387429.
--
TRA
ISSION
AND REACTION
1 factors limiting
TIME
spatio-temporal
357
discriminations. ation, New York: ates of alertness ectroenceph. clin.
4. ~e~~very functions of somatosensory cerebral evoked responses in man. Electrosiol. 17, 126--135. rative action of the nervous system. New eriod. Psychol. ~h~physi~s of sensory function. ry ~~mrnun~~a~i~n, New York:
In: LT.
Press and
Patterns of activity in single CO&al of the digits in monkeys. J. Necrophysiol.
SXAN, t9i%.
ical refractory period’ and the timing of a review and a theory. Brit. J. Psychol. ~*cgtic~n in the brain. fed.), Acta Psycho].
In: Attention
an
rformmce II ( W. G. Koster, ed.) 1969, 339-357 0 North-Holland Publishing Company, Amsterdam
A. ANGEL of Physiohgy,
he University,
Sheffield IO, England
Itisshown that the amount of information
reach ng the cerebral cortex after the second of a pCr of equal intensity stimuli appFed to the same peripheral me semlsorymodality varies inverse with the stimulus intern the stimuli. For a simple stim,ulus activated task the reaction time d to the information reaching the cerebral cortex by the equation: d= kl i- k2 (RT-L). Where log is the psychological magnitude of the stimulus kl and kz are constants, RT is the reaction time and L is the latency ofthecerebral response evoked by the stimulus in the primary cortical receiving
1. INTRODUCTION t has been shown by many ARSHALL (1941), JARCH~(1949), d A~~ASSIAN(1958) that in cats MOUNTCASTLE et al. (1952), c anaes retisecl with bar the responses recorded from the ckq?lj’ e cerebral cortex to, the second of a primary sens y receiving area 0 of peripheral stimuli become reduced in size when the interval rating the two stimuli is between 40-150 msec. When the two stimuli are separated by 30-40 msec no responses could be obtained to the secwd stimuli of the pair. In the rat and coypu deeply anresthetised no responses with trichloroethylene, urethane, barbiturates or fluotha were obtain& from the cerebral cortex to the seco of a pair of peripheral stimuli when the interval of separation was lo-50 msec, and nses did not recover fully unless the stimuli were separated rsec-1 see (ANGEL, 1967). In some preparations the cortical responses to pairs of stimuli separated by 2-10 msec showed summation (hiGEL, 1963, 1967). Furthermore, it was also shown that as well as the deerease in size of the cortical responses to the second of of stimuli the response latency became increased (ANGEL, 1967). of the decrease in the size of the cortical response to the second of a pair of peripheral stimuli has been shown to be due to a decrease in the ability of the venuobasal thalamus to transmit ascending information. MAXSHALL (1941), ANGEL (1967); and ANDERSEN et al. (1964) 339
340
rbiturates a cu have shown that in the cat anaesthetised with thalaunic volley causes a prolonged hyperpolarisation of cells located in the ventrobasal thalamus. When two stimuli are delivered to a human subject who has to a positive reaction to the second it is found that the time taleeli to respond to the second of a pair of stimuli varies inversely interstimulus interval (cf. SMITH, 1967; WELFORD, 196’7). Various hypotheses have been advanced to explain this phenomenon, involving either the strategy of the subject (ELITHORNand LAWRENCE, 1955; .A.NNETT,1966) or the limitations imposed by the handling system I@VELFORD, 1952; DAVIS, MT). It is the intention of this pa that the physiology of transmission by the central nervous be adeqtiate, under certain circumstances, to explain the behaviour rsf human subjects to paired peripheral stimulation. 2. METHODS 2. I. Animal experiments The animals were either anaesthetised with urethane 1(1.5-l.8 g/ OF were unanaesthetised with recording electrodes implanted into the skull; or for two experiments cats were used which had had, under deep &her anaesthesia, a section of the neuraxis just rostra1 to the exit of the trigeninal nerve; a midpontine pretrigeminal preparation (BATINIet al., 1%9). The anaesthesia was then discontinued. In the anaesthetised animals access to the cerebral cortex and thalamus was allowed by an extensive craniotomy, on the left hand side, after reflexion of the temporalis muscle. The dura mater was opened and reflected. To expose the medulla, the neck muscles were reflected back from the base of the skull and the arch of the atlas and some of the skull overlying the posterior part o the cerebellum were removed. The cerebellum was always left intact. The animal was held firmly in a stereotaxik: frame. The skin of the head was clamped between an inner perspex ring and an outer metal clip. The pool so formed over the cerebral cortex was filled with liquid paraffin B.P. (which had been saturated with physiological saline) at a temperature of 37OC. The animals were kept at a rectal temperature of 37OC by placing them over a small radiator through which water at 39OC was circulated. The electrodes used to record potentials from the surface of the cortex were of dver wire, insulated except at the tips, which were fused into smalJ balls. One of these was placed over the primary somatic
Y TRANSMISSION
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341
solution and with a resist-
er cathode-follower was reparations a concentric hiasm under stereotaxic
lectrical stimuli were applied to the periphery by means of lint ne pad was wrapped around the wrist a negative electrode. The pressu r er the electrodes was kept as 910~ gular pulses of lOc! psec duration ‘ble. The stimuli were ret as of the stimuli was controlled from olated from earth. The tir an a digital timing unit (Digitim=r, Devices Ltd.). Stimuli were also delivered via the glass micropi ette, in which case the pipette was made the negative electrode, the positive electrode being clipped onto the neck muscles. Average records of the responses e made with a special purpose digital computer (Biomac 10001, ta Latiratories Ltd.). The site of the microelectrode was determined by histological examination of the tissues after the nervous system had been fix-a with the microelectrode in situ. 2.2.
urnan experiments
Electrical stimuli were applied to the periphery by mears of lint soaked in 3 M NaCl wrapped around the index l(negative electrode] little fingers. Recording elect:rodes were affixed to the scalp over the primary cortical receiving area (~~AwsoN, 1947, 1950, 19%). The rees were amplified and averaged with the special purpose digital ter. The MT was measured in one ot”’two ways: either the stk~ulus started a digital clock counti:ng in msec which was stopped
342
A. ANGEL
a button; or the stimulus started the digi its stores at the rate of 1/msec; pushing the button then caus crement of the store location identified end of the experimental period the contents of the read out in the form of punched paper ta 3. &iSULTS For convenience the results can be divided i is concerned with the experiments on the transmission o formation in animals. The second with the behavio to peripheral stimulation. 3.1. Animal experiments X1.1.
Paired stimuli
The responses to paired stimuli applied to the periphery have been recorded at three sites along the dorsal column sensory pathway. At the 1~~1s of the first sensory synapse, the cuneate nucleus: ~nsory synapse, the ventrobasal thalamus and the third sensory synapse in he cerebral cortex. Ex;z,mination of the responses recorded from the cuneate nucleus showed that, in general, the size of the post-synaptic mass response to the second of a pair of electrical stimuli applied to the for unchanged unless the interval between stimuli was 15 msec o latency of the naptic mass response was, in the majority of experiments, una with separations of the stimuli as little as 3 msec (ANGEL, 1867). In some experiments a small increase in the response latency was observed with separations of stimuli of 5 msec or less. 1C shows the effect of p&=ed stimuli on the siize and latency of the post-synaptic mass response recorded from the cuneate nucleus in a rat deeply anaesthetised with urethane. Each point on the graph is the mean of twenty consecutive responses. When the responses from cells located in the ventrobasal thalamus were studied it was found that the si;t.e of the post-synaptic mass rense of a collection of cells or the probability of discharge of single in the deeply anaesthdxd rat, was unchanged if the stimuli were sepa’ked by 500 msec or more. With intervals of less than 500 msec the size, or probability of discharge, decreased proportionally with the stimulus interval, until with intervals of 30-40 msec or less the second UIUSdid not e tit a response. At the same time as the decrease in
1 mscc
onses to the second of a pair of peripheral the stimulus interval in the anaesthetised rat B and CJ and in the unanaesthetised rabbit behaviour of a single cortical cell, B a single thalamic cell a?d C the post-synaptic cuneat; mass response. The circles indicate *t--C grcbahility of cXllUlai discharge or percentage size of the CL&U
0t
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04 = i
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0.8
1.0
04
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.
26
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I
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I
*
60 80 100 msec
60 80 100
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cuneate response, the dots the mean latency of the responses. 40 consecutive stimuli the Bf the cells responded 40 times rcentage shows the mean probability was plotted as unity. size of the first positive wave of the cortical evoked response (circles) and the mean latency (dots) to 26r consecutive stimuli.
io
Lo!
I 5
344
AJWGEL
the mass response size or the robability of discharge, the tern of latency the post-synaptic responses became inc li were 100-300 change was always the same. In the rat, when msoc apart, the ktencies of the responses to the second stimulus th shorter intervals sed. An example and response latency of a single thalamic cell as a fu stimulus interval is :shown in fig. 1 Records from the cerebral cortex showfti the same re to paired stimuli as did the responses from the ventro The area of cortex which was stulied was that which g1 latency responses to peripheral stimulation (ANG haviour of the response probab lity and response lat cortical cell to paired periphera stimuli has been pl The behaviour of the mass corti I response recorded from the primar; somatic receiving area of the cortex of an unanaesthetised ra implanted electrodes is shown in fig. 1D. It can be seen that, in essence, the: behaviour of the cortical response to paired stimuli was the same as that shown by the deeply anaesthetised animal (compare rig, 1A and ID,); except that in the unanaesthetised animal the cortical res shows a recovery to closely spaced, 1040 msec, stimuli. This t behaviour though less marked has also been seen in anaest animals (&GEL, 1967). Thus if one accepts the thesis that the amplitude of the post-syn mass discharge, or the probability of discharge of single cells, ret from a nucleus gives an indication of the size or effectiveness of the vdky transmitted by the nucleus, then these observations indicate that the: decrease in responsiveness seen at the cortex occur& maimy as a consequence of the decreased thalamic transmission to the second of a pair of synchronous ascending volleys. This observation has been conf!irrned in anaesthetised animals by comparing the cortical responses to paird stbuli applied to cuneo-thalamic and thalamo-cortical fibres. It is found that stimulation of the presynaptic thalamic fibres gives a respmsc pattern to paired stimuli essentially similar to paired peripheral stimuli, whereas paired stimuli applied to post-synaptic elements show that at the time when the responses to the second of a pair of stimuli applied to the presynaptic fibres are reduced in size or absent, the cortical responses to the same separations of stimuli applied to the st-synaptic elements are unaltered or increased in size (ANGEL,1967).
SENSORY
TRANSMISSION
AND
REACTION
TIME
345
haviour has been found in animals without central ows the responses to the first and seco tion of 50 msec applied either to the optic chiasm tical f&e.; in a mi pontine pretrigeminal cat.
Fig. 2. Responses recorded from the primary visual cortex in a midpontine pretrigeminal cat to the first and second stimuli (1 and 2) of a pair ssparnted by 50 msec and applied to the optic chiasm (A) or the geniculo-cortical fibres (B). Each record r;;hows five superimposed responses. The horizontal line represents 10 msec, the ~rtical one 1 mV. Positivity at the active electrode is signalled as an upward deflexion in this and subsequent figures.
3.1.2. Interpretatiorz 0 f the cmticul mm resporzse The complex cortical mass response to peripheral stim be divided into three major components for convenience and descriptive These are a first positive deflexion (labelled P, fig. 3A) by a first negative deflexio (labelled N, fig. 3A) and lastly positive deflexion (labelled 2 fig. 3A). The evokeo zzsponses from the primary somatic receiving cortical area in the anaesthetised monkey and the unanaesthetised rabbit to single and paired stimuli are shown in fig. 3. They show another feature of the changes in the responses to paired stimuli, in that in the deeply anaesthetlsed animal (fig. 3A) with intervals of separation of 200 msec or less the shape of the responses becomes altered. With decreasing intervals of separation the cortical response usually consisting of a positive wave only. In the relatively lightly anaesthetised animal (reflex withdrawal of the hindlimb to a strong pinch jl;st present) and in The unanaesthetised animal this change in the shape of the cortical .responses is not so marked, an.d may not be seen fig. 3B and 3C. In experiments on animals it has been found that the size of the first sitive wave of the cortical response is (a) directly relatled to the ulus strength (fig. 4A), both in the anaesthetised and unanaest
346
A.
ANGEL
Averaged responses recorded from the primary sensory cortex of a deeply anaesthetised rat (A), a ‘lightly’ anaesthetised monkey (B) and an unanaesthetised rabbit (C). The responses to a sin le stimulus alone (I), to the second of a pair at a separation of 600 (II) and 100 msec (III) are shown for c,:ach animal. The separation in (IV and V) are 30 and 10 msec (A], SO and 20 rnsec (B) and 60 msec (C IV). The horizontal ruling sents 10 msec: intervals. The vertical calibration represents 1.5 mV for 50 JN for (B) and 500 yV for (C). 60 consecutive responses to forepaw stimulation at a rate of x set were averaged.
t&d preparation, (b) shows exactly the same behaviour to paired s;timuli as the post-synaptic mass responses recorded from the ventrow there is an almost basal +&alamus (fig. 1A and B, ANGEL, X967), halan-& response linear relation between the size of the post-syna z:nd the first p&tive wave of the cerebral evoked response tf;g. 4D) ZIIXI(d) when the size of the thalamic response is increased by preceding s; imulus to a forepaw %y strong stimulation applie+danywhere OX t surface the first positive wave o the cortical response is also increased in size (ANGEL and DAWSON, 1961, 1963).
SQRY TRANSMISSI
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AND REACTION
347
. .
‘0 .
.
.
.
10
1oov
10
toov
A
10
50
100 O/oPI
D
Fig. 4. “Phis figure shows the relation between the first positive wave of the cortical response (A) and the first negative wa (B) versus the stimulus strength; and the xclation between the first positive an
negative waves (C) in an u!n-
anaesthctised rabbit. (D) shows the relation between the percentage probability of response of a thalamic cell (ordinate) versus the percentage size of the first positive wave of the cortical response (abscissa) of a rat deeply anxsthetised with urethane. Each point on the graphs is the mesn of 40 consecutive responses.
egittive wave of the cortical sponse also shows a direct relation to the size of the stimulus, (fig. 4 sl~ouvsthe same behaviou,to ired stimuli as the first positive wave of the ce sponse (ANGEL, 19671, and also shows exactly the same o single cortical cells responding with e size of the first negative wave is also f the first positive wave of the co (ANGEL,1967, fig. 4C). n fact it has been found that the size of this nent of the cortical response is directly relat probability of cortical cells (ANGEL and would seem, therefore, that the size of the first positive wave of the
A. ANGEL
rough measure the size of the volley asand the size of the first negative wave of the ugh measure of the initial response of the
crf irerarivepetiph?td stinaaciation
ts may experience difficulty in the digits if they are separaited Al), whereas they have no difficulty in retrk applied to the skin of the r sec. Thuts there: is an apparent f the nervous system to brief, large, ore normal peripheral stimuli. OUNTCASTLE (19599 lt,kt id stimuli at rates up to s of the deeply anaesthei ilt is found that the first skes a norma response. The second stimulus of a pair of stimuli at the show a gradual recovery reaching a steady level which depends on, A graph of the sizes sf the first s to iterative stimulation al various
ems the subjects were presented with digits, a 1 msec click, or a 1 msec ng 12’ at the eye. The stimuli were cutaneous stimuli the subjats had fe.tt the shock, or the second of 31pair t%ne from al digtal clock, reset the Going through this procedure made it ue, For the auditory and the subject was time. Those subjects
SIW3XLY
TRANSMISSION
AND REAC:TPOl’+J TIME
3
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Fig.
5. Shows the percentage size of the first positive wave of ~.he clerical response ~CBeach stimulus of a train: la) at 100 msec (circles), 20 a5 %I m (large dots), 23 at 40 msec (triangles), 30 at 30 msec (squares) and 50 ;at 20 m separation (small dots).
fig. GA). The reaction times to 300 consecutive cutaneous stirn~~~ either alone or paired plotted as histograms are shown in fig. early parts of the cerebral evoked responses to the same stim shown in fig. 7. It can be seen that the reaction times may ~XS, relation both to the mean latency of the cortical response and t of the first positive wave of the response. In fact, the behaviour cerebral responses of man to paired stimuli is exactly the of the rat, rabbit, or monkey, the mean latency of the cerebral responses increasing as the stimuli are brought closer and t response decreasing. That the major factor in any relation reaction time arnd the cortical response will relate to first positive wave rather than the latency is shown by th reaction time is altered dramatWl,y by increasing the stimulus (fig. 623). Increas.ing the stimulus st.rength howe the latency of the cerebral evoked response of the first positive wave, fig. 7EXX It is of inte of
P*.
GEL
ii
SENSORY
TRANSMZSSX
AND REACTION
T:
the stimuli were delivered in a regular time sequence there evidence at all that ll:herewas any process of learning 32.2.
esponses $0 trains of stimuli
For this experiment the subjects were asked to press the bu they bad seen the Jlast flash in a train of four at a rate of msec. It was found that the reaction time to this stimulus was i when compared to the reaction time to a single flash but less rezxtion time to thee second of a pair of st,imuli at the same se The results plottti as histograms for four subjects are sho
Fig. 7. This f~igur~ sbows the averaged cerebral subject as in fig. 6 performing a response) to a sin digits (A) and to the second of a pair separated by 3 and 50 msec (II) and to, two stimuli separated by 10 msec at -0, and 2.3 X &reshCl~fd(G). 3 averages of 100 consecuti sulperimposed in A-El+ 2 averages of LOOresponse cGbrati0n repil=sents 40 m:;ec, the verti
3.2 .ti3.
Pairs of sthurli in different modalities
animals it is found that in order to obtain the deer ticas response to the second of a pak of the same modality and applied to the not too far apart spatially. In these ex distinction between the occlusive eff same peripheral lucus and the phenom III\
35
. ANGEL
352
uninfluenc T_herefore, the cortical response to a flash would : preceding stimulus applied to the digits. It was fo time to a flash was unaltered or sli tly decreased by flash with a click. The click-flash se ration was 100 msec. from four subjects are shown i time to a single flash war3239 msec, to the by a click or an electric shock to the digits it was respectively.
I.. . ".. Y. -...".."..."~L*L... . . . ..C. . ...._I -mm.. .m* 111*.... . . .. . . ... .:u. ,.UII_.OI. .. . l
I 0
02
04
0.6
CGsec
0
02
04
0.6
0*8sec
Fig. 8. This figure shows histograms of the number of responses vmw the time of tirIe response to the nearest msec for 4 different subjects in resgsnw to (from top to bottom of each group) a single flash, the seesnd of a pair of flashes separated by 100 msec, a flash preceded (100 msec) by a click and the fourth flash of a train at a separation of 100 msec. The fifth histogram in A shows the reaction time to a flash of a subject who appeared to be able to predict each time a flash would occur. 4.
~IsUJSSIo1N
Thus i.t has been shown that in anaesthetised animals the cortical responses to pairs oC:peripheral stimuli vary according to t between the stimuli, and that this variation occurs mainly as a decrease in the ability of tile thalamic relay nucleus to transmit t!x second ascending volley of a pair (MARSHALL, 1941); ANDERSEN et al., 1964;
t WCSfound in the
ec or more, or
en shown in the unanasthetised y the same interpretation
cat SCHWARTZ
of ahe surface cortical re-
as well as the information taking a cortex after the second of a pair of less information ab\.jut the stimulus arrives at the cortex, ROSNEK (1961) has shown that if the separation of Qwo electrical stimuli a plied to the digits is from 15-500 msec subjects will underestimate the intensity of the second stimulus. hus the physiology of transmission of two afferent volleys agrees with the psyical observations that the sensitivity of the central system is nal at least as far as the afferent inem now arises of whether or not one can equate the physiological and psychological ‘refractory states” for a simple task which requires a unit output -- press, or not press - to :Lunit
input. Limitations of the handling system suggested by WELF~RD(.l’XZ 1967) and DAVAS (1957) appear inadequate to explain the behaviour of human subject to simple tasks (KOSTER and BEKKER, 1967a,b). Let of the ostulate that the reaction time is some function us therefore, agnitude of the applied stimulus, a parameter psychological should take into account any change in the sensitiAy of the s SHERRINGTC)N (1906)showed that the latency of mally spinat; reflexes
A, ANGlX
354
decreased as the strength of the s must take into account that not only does thz a reaching the cerebral cortex become deer but that it also arrives at the cortex at shown that the psychological the physical m nitude (S) by a M = kSn or 1
so that a plct of log M versus log S gives equal to the value of the exponent. Such a for the stimulus strength and the first posi response fig. 4A, (a&partfrom the stimuli n can make the assumption that a measure of the stimulus .may be given by the log sponse. Further, since there is a linear relation mve and the fir.st negative wave of the c has been shown to be some measure of we may postulate that the initial output psychological intensity of th7 stimulus. RT-L lmsr;) 300
r
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240220. 2001 1800 160UO-
k--
I
20
I
30
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40
IIC
60
log siar
Fig.. 9. This figun: shows the relation found in the subject whose reaction times and cortical reriponsesare shown in fig. 4 and 7, between the reaction time minus the cortica?in:sponse latency and the log of the size of the first positive wave of the cortical response (dots). The regression line for the points has been plotted.
SE
REACTION TIME
355
on ha:, reached
have as a closed loop servo ich abruptly cha:nges its to contradict in any way ich has been used to explain the beThe pri;sent experiments 1~ ser’ ,ry modality. ?_Jnt in two or three dimen-
A~~~wLE
NTS
esearch Council rpose digital computer used in these inve me a grant to attend
CCLESand T. A. SEARS,1964. The ventrobasal complex of potential field synaptic transmission and excitab of both yre-synaptic and post-synaptic components. J. Pkysiol. 370--399, ission in tbe sensory Ipathwayto A., 1%3. The level of failure of tra , 32-33P. do~eiy spaced stimuli. J. Physiol. 9 iP6P. Cortical responses to paired stimuli applied per sit sites along the somato-sensory pathway. J. Pf ysiol. I the thalamus:
.hKSL,
356 ,~GEL, a. and G. D. DAWSON,1961. Modification
of thal
sensory stimulation. I. Physiol. 1963. The facilitation of rhalamic and --, in the dorsal column sensory pathway by stro tian. Y. Physiol. ANNETT, J., 1966. Payoff: Quart, I exp, Psychol. BATINI, C., G. M~ZRUZZI, Effects of complete pontine transection on rhythm: the m 97, 1-12. a single chanmel inform DAVIS, R., 1957. The human operator Quart. I. exp. Psychol. 9, 11 DAWS~N,D. G., 1947. Cerebral respo nerve in man. I. Neurol. --# 1950. Cerebral responses 6, 326-329. s 1956. The relative excitability and conduction and motor nerve fibres in man. J. Physiol. 131,43 E~LITHORN, A. and C. LA~UNCE, 1955. Central in observations, Quart. 3. exp. Psychol. 7, JARCHO, L. W., 1949. Excitability of cortical af anaesrhesia. I’. Neurophysiol, 12, 447 KOSTEIK, W. G. and I’. A. M. EKKEH,1967a. Some ex’Perimen In: Attention and Performance, A, F. 27, 64-70. and 1967b. Stimulus intensity and the p fractory per& I..I).O. Anr *la1 Progress MAIPSHALL, W. II., 1941. Observations on sub-tort nisms of cats under nembutal anaesthcsia. J. Nturop -, C. N. WOOLSEYand P. BARD, 1941. Ob mechanisms of cat and monkey. I. Neurophysiol. MOUNTCASTLE, V. B., M. R. COWANand C. R. HARRKXIN, representation of some forms of deep sensibility. nerv. ment. ms. 30, 339~-370. and T. P. S. POWELA,, 1959, Neural mechanisms subservin ous sensibility, with special relerence to the role of afferent inhibition in sensory perception and discrimination, Bull. Johns Hopkins Wasp. 105, 201-232. POGGIO,G. I? and V. B. MOUNTC.‘ASTLE, 1963, The functional properties of ven= trobasal thalamic neurons studied in unanaesthetiwd ’ monkey. J. Nc*ophysiol. 26, 775-8~. ROSE,J.@E. and V. B. MOUNTCASTLE, 1959, Touch and kinesthesis. In: Handbook of Physiology, Neurophysiology 1, American Physiological Society, 387429.
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TRA
ISSION
AND REACTION
1 factors limiting
TIME
spatio-temporal
357
discriminations. ation, New York: ates of alertness ectroenceph. clin.
4. ~e~~very functions of somatosensory cerebral evoked responses in man. Electrosiol. 17, 126--135. rative action of the nervous system. New eriod. Psychol. ~h~physi~s of sensory function. ry ~~mrnun~~a~i~n, New York:
In: LT.
Press and
Patterns of activity in single CO&al of the digits in monkeys. J. Necrophysiol.
SXAN, t9i%.
ical refractory period’ and the timing of a review and a theory. Brit. J. Psychol. ~*cgtic~n in the brain. fed.), Acta Psycho].
In: Attention
an