EFFECTS
OF ATTENTION,
REGULARITY AVERAGED
ACTIVATION
ON SHORT-TERM EVOKED
VLVIEN MACLEAN,
AND STIMULUS
‘HABITUATION’
OF THE
RESPONSE
ARNE OHMAN* and MALCOLM
LADERt
institute of Psychiatry, University of London, U.K.
Accepted for publication 19 September 1974
Three studies are reported in which the effects of direction of attention, level ofactivation and regularity of stimulation on the rate of amplitude decrement over time of the auditory evoked vertex responses in humans were examined. Short-term, stimulus-by-stimulus changes were assessed by averaging across trains each of 10 click stimuli. The effect of directing attention towards thestimuli was toenhance theN, - P,component, but usually only underco~dit~ons of high activation and with irregular stimulus presentation. Habituation rate was hardly affected by the experimental manipulations. The most clear-cut relationship between psychological influences and the AER was that between level of activation and the P2 - N2 component.
1. Introduction By presenting stimuli in discrete trains, short-term changes in the electroencephalographic evoked response (AER) can be studied by averaging the first, second, third stimuli, etc. across trains. With regular, relatively short interstimulus intervals (ISI) the amplitude of the N, - P2 component (IOO200 msec latency) rapidly decreases exponentially (Fruhstorfer, 197 I : Fruhstorfer, Soveri and J~rvilehto, 1970; ohman, Kaye and Lader, 1972; Ritter, Vaughan and Costa, 1968). The importance of such short-term ‘habituation’ (cf. &man et al., 1972) of the AER is that it implies a systematic change in the individual evoked responses with stimulus repetition, thus making the interpretation of changes in the averaged response more hazardous. To try to delineate some of the factors influencing the rate of decrement of the AER, ohman and Lader (1972) studied the effect of selective attention by means of a short-term habituation paradigm. Attention had quite clear effects on AER amplitude but not on AER habituation. __. . __ ‘Now at Uppsala, lAddress London,
Department of Psychology, University of Uppsala, Svartblcksgatan IO, S-753 30 Sweden. for correspondence: Dr. M. H. Lader, Institute of Psychiatry, De Crespigny Park, SE5 gAF, U.K. 57
To elucidate further the relationship between attention and habituation. the present study manipulated variables assumed to affect both phenomena. Two important moderator variables of the attention effect on the AER are regularity of IS1 (Naatanen, 1967) and task-induced activation (Eason, Harter and White, 1969; Lindsley, 1970): both variables might influence the rate of short-term decrement of the AER. When the sub.jects’ attention was directed away from the stimuli, ijhman et al. (1972) noted a pronounced exponential decrease with regular ISI, but only a slow linear decrease with irregular ISI. Activation,
however,
P, - N, component
had no effect on the h~~bitu~~tion function, of about 250 msec latency was significantly
but the smaller
during high activation. In the first experiment of the present series, the effect of regularity was assessed both with attention directed towards and away from the auditory stimuli: in the second experiment high and low activation tasks were used to manipulate both attention and activation. Since the attention etfect appeared quite elusive in these experiments, a third experiment was designed in order to maximize the likelihood of detecting an effect of attention on the AER. In all experiments, reaction time (RT) and skin conductance level (SCL) were monitored in order to provide additional estimates of the experimental manipulations. 2. General method The subjects were students or staff members at the Institute of Psychiatry. Their ages ranged from 21 to 40 yr, and they were paid for their participation. The experiments were carried out on-line using a PDP-l2A computer. The EEC was recorded from bipolar saline pad electrodes (C, -- r3 on the IO-20 system) by means of a Grass model 51 IC amplifier of bandpass 0.3-1000 Hz, and fed into an A-D converter of’the computer, The EEG was sampled every 2 msec after the stimulus for a 500 msec epoch. Tests for gross artefact in the background EEG and in the AER were included in the computer programs. SCL, measured as resistance through double-element electrodes (Lader and Wing, 1966), was sampled ilnmediateiy prior to each stimulus. Reaction times were measured in milliseconds by the computer. EEG epochs, skin resistance and RTs were stored in digital form on magnetic tape for later analysis. The subject was seated comfortably in an armchair in a sound-attenuated chamber separated from the experimenter and the recording equipment. The experimental procedure was outlined to the subject, and it was stressed that he should keep his eyes open and fixed on the timer (see below) and avoid moving during the trains of stimuli. To maintain the subject’s attention and alertness constant over the experimental session, a reaction-time task with feedback of information on performance was incorporated into the design.
attention,
actiuatiorz and er:oked resporrse decremetrt
59
Auditory evoked responses were elicited by click stimuli of about 70 db intensity and 1 msec duration, presented through a loudspeaker behind the subject. Each experimental condition incorporated 20 trains of 10 stimuli each. The start of each train was heralded by switching on a red lamp 2 m in front of the subject, the lamp remaining on throughout the train. The interval between the Iamp being switched on and the first stimulus corresponded to the ISI between the clicks for that particular condition. The intertrain interval (ITI) was irregular, varying between 24 and 36 set with a rectangular distribution. During the trains the computer 10 times set in motion a digital timer (Venner model TSA 6614) placed 1 m in front of the subject. In the ‘high activation’ condition, ‘attention’ was manipulated by an RT task. When instructed to ‘attend’ to the clicks, the subject had to press a microswitch as fast as he could in response to each click: after a short delay of at least I see the RT was displayed for 1 set on the digital timer. When instructed ‘not to attend’ to the clicks, the subject produced a visual RT. Each time the timer was activated the subject pressed the microswitch, thereby stopping the timer and enabhng him to read off his visual RT. In the visual RT condition, the interval between visual trials varied randomly between I and 5 set thus avoiding the alternation of visual and auditory stimuli. In the “low activation’ condition, the subject counted the stimuli in each train, but the general organization of visual and auditory stimulation remained the same: the subject counted the number of clicks in each train when ‘attending’ to the auditory modality, and counted the number of times the timer started during each train when visually attentive (‘non-attending’ to clicks). Occasional trains (randomly one in eight) where the number of stimuli was 11 were given, but the extra stimuli were not included in the analyses. Averages were computed across trains, stimulus-by-stimulus, by taking all the first stimuli in the trains, all the second, and so on. Thus, there were 20 constituent evoked potential epochs in each AER. Amplitudes and latencies were measured by setting cursors manually against the peaks of the AERs as displayed on the computer oscilloscope. Variances were also calculated and displayed as a check for artefacts. Four components were measured: a positive peak with a latency of 50-80 msec (PI>; a negative peak with a latency of 80130 msec (N,); a positive peak with a latency of IX-230 msec (PJ; and a negative peak with a latency of 230-280 msec (&). RTs and SCLs were obtained from the computer tape, the former being transformed to a speed measure (1000/x) and the latter to log conductance. Averages were computed stimulus by stimulus as for the AER. Trend analysis with tests of linear and quadratic components was performed on the amplitude data (Edwards, 1960). To assess the effects of attention during the various conditions, planned orthogonal t-tests were carried out (Kirk, 1968). Latencies, SCLs and RTs were subjected to routine analyses of variance.
I’. Mackorr, A. &maa
ho
anti M. Latb-
3. Experiment 1 The purpose of the first experiment was to study the effect of attention on habituation ofthe AER during conditions of regular and irregular stimulation.
Four females and eight males from the staff of the Institute of Psychiatry acted as subjects, seven of whom had participated previously in similar experiments. A 2 x 2 factorial design was used, with attention towards or away from the clicks as one factor, and regular versus irregular ISI for the clicks as the other. In the attending condition the subject was told to respond to the clicks, and that his RT would then be displayed on the timer. In the non-attending condition he was instructed to stop the timer from which he could directly read off his visual RT. In the regular IS1 conditions, the interval between clicks was 3 set, and in the irregular ones it varied between 2.4 and 3.6 set with a rectangular distribution. In the visual RT conditions the timer was activated at intervals varying between 1 and 5 sec. The subject attended the laboratory twice, two conditions being studied on each occasion. The order of the attention conditions was balanced over subjects b~~~~~~~~ sessions, and the order of the ISI conditions was balanced within sessions.
3.2.1. Amplitmk. The N, - P, habituation functions for the four experimental conditions are shown in fig. 1. There was an overall, slightly curved decrease
Fig.
I. Ekts
of stimults regularity and direction ofattention on the IV, - Pz component the auditory evoked response, averaged stimulus by stimulus.
of
Attention,
actiaalion
andecoked responsedecrement
61
over stimuli (F(9,99) = 9.15; p < 0.001; F(lin 1,99) = 45.16; p < 0.001, and F(quad 1,99) = 18.11; p < 0.001). None of the interactions between stimulus repetition and the other factors was significant. The t-tests revealed a significant effect of attention on overall amplitude in the irregular (t(l1) = 2.01; p < 0.05), but not in the regular ISI (t = 1.15). The main effect of attention in the analysis of variance, however, was not significant (F(l,ll) = 3.11) nor was the interaction attention x regularity (F(1 ,I 1) = 0.94). Similarly, the P2 - IV2 amplitude curved down with stimulus repetition, (F(9,99) = 4.23; p < 0.001, with significant linear, F(lin 1,99) = 18.18; p < 0.001, and quadratic, F(quad 1,99) = 12.86; p < 0.001, trend components). Neither the attention nor the regularity factors produced any effects on this measure. 3.2.2. Latencies. The latency of the stimulus repetition (F(9,99) = 3.42; attention was directed towards the N2 component appeared earlier with = 6.68; p < 0.05).
N1 component decreased gradually with p < O.Ol), and occurred earlier when stimuli (F(l,ll) = 4.89; p < 0.05). The regular than with irregular IS1 (F(1 ,l 1)
3.2.3. Reaction time. The RT decreased within trains and reached a minimum after about five stimuli (F(9,99) = 8.63; p < 0.001). This decrease was more pronounced for the auditory than for the visual RT, as indicated by the stimulus x attention interaction term (F(9,99) = 5.25;~ < 0.001). Furthermore the significant three-way interaction suggested that, whereas the nature of the IS1 did not influence visual RT trends, the speed of response to the clicks increased more for the regular than for the irregular IS1 (F(9,99) = 2.48; p < 0.05). Both auditory and visual responses were faster during the regular IS1 (F(l,ll) = 6.59; p < 0.05). 3.2.4. Skin conductance level. During the stimulus, then declined but no other effects were significant.
the SCL rose initially
4. Experiment 2 This experiment aimed at an assessment of the effect of attention tion during tasks assumed to induce high and low activation.
and
on habitua-
4.1. Method Five females and seven males (six psychology students and six staff members) were paid to participate. Again, seven had been subjects before in AER experiments. Two conditions of attention were combined with two levels of activation to form a 2 x 2 factorial design. The high activation auditory and visual conditions were identical to the irregular IS1 conditions in experiment 1. In the low activation conditions, the subjects counted the number of clicks in each
62
V. Maclean,
A. &man
and M. Lader
train while attending to the auditory modality, and the number of times the timer started during each train while attending to the visual modality. He was asked to report the number of non-standard trains at the end of each condition. Again the IS1 varied between 2.4 and 3.6 set for the clicks and between 1 and 5 set for the timer. Each subject was studied twice, two conditions to each occasion. The order of the attention conditions was balanced over subjects between sessions, and the order of the activation conditions was balanced within sessions. 4.2. Results 4.2.1. Amplitude. The mean amplitudes for the N, - P2 component are shown as a function of stimulus number in fig. 2. There was a clearcurved decrease in amplitude with stimulus repetition (F(9,99) = 13.67; p < 0.001, with significant linear, F(lin I ,99) = 74.77; p < 0.001, and quadratic, F(quad 1,99) = 30.13; p -=z0.001 trends). This decrease, furthermore, was more pronounced for the non-attending than for the attending conditions, as attested by the stimulus x attention interaction term (F(9,99) = 3.36;~ < 0.01, and F(lin 1,99) = 19.47; p < 0.001). However, whereas the mean values for the two attention conditions converged in the low activation condition, they diverged in the high activation one (F(lin 1,99) = 4.47; p < 0.05, and F(quad 1,99) = 4.21 ; p
OF ATTENTION,
REGULARITY AVERAGED
ACTIVATION
ON SHORT-TERM EVOKED
VLVIEN MACLEAN,
AND STIMULUS
‘HABITUATION’
OF THE
RESPONSE
ARNE OHMAN* and MALCOLM
LADERt
institute of Psychiatry, University of London, U.K.
Accepted for publication 19 September 1974
Three studies are reported in which the effects of direction of attention, level ofactivation and regularity of stimulation on the rate of amplitude decrement over time of the auditory evoked vertex responses in humans were examined. Short-term, stimulus-by-stimulus changes were assessed by averaging across trains each of 10 click stimuli. The effect of directing attention towards thestimuli was toenhance theN, - P,component, but usually only underco~dit~ons of high activation and with irregular stimulus presentation. Habituation rate was hardly affected by the experimental manipulations. The most clear-cut relationship between psychological influences and the AER was that between level of activation and the P2 - N2 component.
1. Introduction By presenting stimuli in discrete trains, short-term changes in the electroencephalographic evoked response (AER) can be studied by averaging the first, second, third stimuli, etc. across trains. With regular, relatively short interstimulus intervals (ISI) the amplitude of the N, - P2 component (IOO200 msec latency) rapidly decreases exponentially (Fruhstorfer, 197 I : Fruhstorfer, Soveri and J~rvilehto, 1970; ohman, Kaye and Lader, 1972; Ritter, Vaughan and Costa, 1968). The importance of such short-term ‘habituation’ (cf. &man et al., 1972) of the AER is that it implies a systematic change in the individual evoked responses with stimulus repetition, thus making the interpretation of changes in the averaged response more hazardous. To try to delineate some of the factors influencing the rate of decrement of the AER, ohman and Lader (1972) studied the effect of selective attention by means of a short-term habituation paradigm. Attention had quite clear effects on AER amplitude but not on AER habituation. __. . __ ‘Now at Uppsala, lAddress London,
Department of Psychology, University of Uppsala, Svartblcksgatan IO, S-753 30 Sweden. for correspondence: Dr. M. H. Lader, Institute of Psychiatry, De Crespigny Park, SE5 gAF, U.K. 57
To elucidate further the relationship between attention and habituation. the present study manipulated variables assumed to affect both phenomena. Two important moderator variables of the attention effect on the AER are regularity of IS1 (Naatanen, 1967) and task-induced activation (Eason, Harter and White, 1969; Lindsley, 1970): both variables might influence the rate of short-term decrement of the AER. When the sub.jects’ attention was directed away from the stimuli, ijhman et al. (1972) noted a pronounced exponential decrease with regular ISI, but only a slow linear decrease with irregular ISI. Activation,
however,
P, - N, component
had no effect on the h~~bitu~~tion function, of about 250 msec latency was significantly
but the smaller
during high activation. In the first experiment of the present series, the effect of regularity was assessed both with attention directed towards and away from the auditory stimuli: in the second experiment high and low activation tasks were used to manipulate both attention and activation. Since the attention etfect appeared quite elusive in these experiments, a third experiment was designed in order to maximize the likelihood of detecting an effect of attention on the AER. In all experiments, reaction time (RT) and skin conductance level (SCL) were monitored in order to provide additional estimates of the experimental manipulations. 2. General method The subjects were students or staff members at the Institute of Psychiatry. Their ages ranged from 21 to 40 yr, and they were paid for their participation. The experiments were carried out on-line using a PDP-l2A computer. The EEC was recorded from bipolar saline pad electrodes (C, -- r3 on the IO-20 system) by means of a Grass model 51 IC amplifier of bandpass 0.3-1000 Hz, and fed into an A-D converter of’the computer, The EEG was sampled every 2 msec after the stimulus for a 500 msec epoch. Tests for gross artefact in the background EEG and in the AER were included in the computer programs. SCL, measured as resistance through double-element electrodes (Lader and Wing, 1966), was sampled ilnmediateiy prior to each stimulus. Reaction times were measured in milliseconds by the computer. EEG epochs, skin resistance and RTs were stored in digital form on magnetic tape for later analysis. The subject was seated comfortably in an armchair in a sound-attenuated chamber separated from the experimenter and the recording equipment. The experimental procedure was outlined to the subject, and it was stressed that he should keep his eyes open and fixed on the timer (see below) and avoid moving during the trains of stimuli. To maintain the subject’s attention and alertness constant over the experimental session, a reaction-time task with feedback of information on performance was incorporated into the design.
attention,
actiuatiorz and er:oked resporrse decremetrt
59
Auditory evoked responses were elicited by click stimuli of about 70 db intensity and 1 msec duration, presented through a loudspeaker behind the subject. Each experimental condition incorporated 20 trains of 10 stimuli each. The start of each train was heralded by switching on a red lamp 2 m in front of the subject, the lamp remaining on throughout the train. The interval between the Iamp being switched on and the first stimulus corresponded to the ISI between the clicks for that particular condition. The intertrain interval (ITI) was irregular, varying between 24 and 36 set with a rectangular distribution. During the trains the computer 10 times set in motion a digital timer (Venner model TSA 6614) placed 1 m in front of the subject. In the ‘high activation’ condition, ‘attention’ was manipulated by an RT task. When instructed to ‘attend’ to the clicks, the subject had to press a microswitch as fast as he could in response to each click: after a short delay of at least I see the RT was displayed for 1 set on the digital timer. When instructed ‘not to attend’ to the clicks, the subject produced a visual RT. Each time the timer was activated the subject pressed the microswitch, thereby stopping the timer and enabhng him to read off his visual RT. In the visual RT condition, the interval between visual trials varied randomly between I and 5 set thus avoiding the alternation of visual and auditory stimuli. In the “low activation’ condition, the subject counted the stimuli in each train, but the general organization of visual and auditory stimulation remained the same: the subject counted the number of clicks in each train when ‘attending’ to the auditory modality, and counted the number of times the timer started during each train when visually attentive (‘non-attending’ to clicks). Occasional trains (randomly one in eight) where the number of stimuli was 11 were given, but the extra stimuli were not included in the analyses. Averages were computed across trains, stimulus-by-stimulus, by taking all the first stimuli in the trains, all the second, and so on. Thus, there were 20 constituent evoked potential epochs in each AER. Amplitudes and latencies were measured by setting cursors manually against the peaks of the AERs as displayed on the computer oscilloscope. Variances were also calculated and displayed as a check for artefacts. Four components were measured: a positive peak with a latency of 50-80 msec (PI>; a negative peak with a latency of 80130 msec (N,); a positive peak with a latency of IX-230 msec (PJ; and a negative peak with a latency of 230-280 msec (&). RTs and SCLs were obtained from the computer tape, the former being transformed to a speed measure (1000/x) and the latter to log conductance. Averages were computed stimulus by stimulus as for the AER. Trend analysis with tests of linear and quadratic components was performed on the amplitude data (Edwards, 1960). To assess the effects of attention during the various conditions, planned orthogonal t-tests were carried out (Kirk, 1968). Latencies, SCLs and RTs were subjected to routine analyses of variance.
I’. Mackorr, A. &maa
ho
anti M. Latb-
3. Experiment 1 The purpose of the first experiment was to study the effect of attention on habituation ofthe AER during conditions of regular and irregular stimulation.
Four females and eight males from the staff of the Institute of Psychiatry acted as subjects, seven of whom had participated previously in similar experiments. A 2 x 2 factorial design was used, with attention towards or away from the clicks as one factor, and regular versus irregular ISI for the clicks as the other. In the attending condition the subject was told to respond to the clicks, and that his RT would then be displayed on the timer. In the non-attending condition he was instructed to stop the timer from which he could directly read off his visual RT. In the regular IS1 conditions, the interval between clicks was 3 set, and in the irregular ones it varied between 2.4 and 3.6 set with a rectangular distribution. In the visual RT conditions the timer was activated at intervals varying between 1 and 5 sec. The subject attended the laboratory twice, two conditions being studied on each occasion. The order of the attention conditions was balanced over subjects b~~~~~~~~ sessions, and the order of the ISI conditions was balanced within sessions.
3.2.1. Amplitmk. The N, - P, habituation functions for the four experimental conditions are shown in fig. 1. There was an overall, slightly curved decrease
Fig.
I. Ekts
of stimults regularity and direction ofattention on the IV, - Pz component the auditory evoked response, averaged stimulus by stimulus.
of
Attention,
actiaalion
andecoked responsedecrement
61
over stimuli (F(9,99) = 9.15; p < 0.001; F(lin 1,99) = 45.16; p < 0.001, and F(quad 1,99) = 18.11; p < 0.001). None of the interactions between stimulus repetition and the other factors was significant. The t-tests revealed a significant effect of attention on overall amplitude in the irregular (t(l1) = 2.01; p < 0.05), but not in the regular ISI (t = 1.15). The main effect of attention in the analysis of variance, however, was not significant (F(l,ll) = 3.11) nor was the interaction attention x regularity (F(1 ,I 1) = 0.94). Similarly, the P2 - IV2 amplitude curved down with stimulus repetition, (F(9,99) = 4.23; p < 0.001, with significant linear, F(lin 1,99) = 18.18; p < 0.001, and quadratic, F(quad 1,99) = 12.86; p < 0.001, trend components). Neither the attention nor the regularity factors produced any effects on this measure. 3.2.2. Latencies. The latency of the stimulus repetition (F(9,99) = 3.42; attention was directed towards the N2 component appeared earlier with = 6.68; p < 0.05).
N1 component decreased gradually with p < O.Ol), and occurred earlier when stimuli (F(l,ll) = 4.89; p < 0.05). The regular than with irregular IS1 (F(1 ,l 1)
3.2.3. Reaction time. The RT decreased within trains and reached a minimum after about five stimuli (F(9,99) = 8.63; p < 0.001). This decrease was more pronounced for the auditory than for the visual RT, as indicated by the stimulus x attention interaction term (F(9,99) = 5.25;~ < 0.001). Furthermore the significant three-way interaction suggested that, whereas the nature of the IS1 did not influence visual RT trends, the speed of response to the clicks increased more for the regular than for the irregular IS1 (F(9,99) = 2.48; p < 0.05). Both auditory and visual responses were faster during the regular IS1 (F(l,ll) = 6.59; p < 0.05). 3.2.4. Skin conductance level. During the stimulus, then declined but no other effects were significant.
the SCL rose initially
4. Experiment 2 This experiment aimed at an assessment of the effect of attention tion during tasks assumed to induce high and low activation.
and
on habitua-
4.1. Method Five females and seven males (six psychology students and six staff members) were paid to participate. Again, seven had been subjects before in AER experiments. Two conditions of attention were combined with two levels of activation to form a 2 x 2 factorial design. The high activation auditory and visual conditions were identical to the irregular IS1 conditions in experiment 1. In the low activation conditions, the subjects counted the number of clicks in each
62
V. Maclean,
A. &man
and M. Lader
train while attending to the auditory modality, and the number of times the timer started during each train while attending to the visual modality. He was asked to report the number of non-standard trains at the end of each condition. Again the IS1 varied between 2.4 and 3.6 set for the clicks and between 1 and 5 set for the timer. Each subject was studied twice, two conditions to each occasion. The order of the attention conditions was balanced over subjects between sessions, and the order of the activation conditions was balanced within sessions. 4.2. Results 4.2.1. Amplitude. The mean amplitudes for the N, - P2 component are shown as a function of stimulus number in fig. 2. There was a clearcurved decrease in amplitude with stimulus repetition (F(9,99) = 13.67; p < 0.001, with significant linear, F(lin I ,99) = 74.77; p < 0.001, and quadratic, F(quad 1,99) = 30.13; p -=z0.001 trends). This decrease, furthermore, was more pronounced for the non-attending than for the attending conditions, as attested by the stimulus x attention interaction term (F(9,99) = 3.36;~ < 0.01, and F(lin 1,99) = 19.47; p < 0.001). However, whereas the mean values for the two attention conditions converged in the low activation condition, they diverged in the high activation one (F(lin 1,99) = 4.47; p < 0.05, and F(quad 1,99) = 4.21 ; p
