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The role of conditioned stimulus termination in short-latency avoidance responding in cats
Behaviourai Brain Research, 1 (1980) 379-395
379
© Elsevier/North-Holland Biomedical Press
THE ROLE OF CONDITIONED STIMULUS TERMINATION IN SHORT-LATENCY AVOIDANCE RESPONDING IN CATS
K A Z I M I E R Z ZIELII~ISK! and M A E G O R Z A T A P L E W A K O
Department of Neurophysiology. Nencki Institute of Experimental Biology. Warsaw (Poland) (Received February 2nd, 1980) (Accepted June 3rd, ! 980)
Key words: avoidance - - conditioned stimulus termination - - latency distributions - - intertrial responding - - prefrontal lesions - - extinction
SUMMARY
The behavioral effects of two procedures for bar-Fressing avoidance training in cats were studied. In one procedure conditioned stimulus (CS) termination was response-contingent on both shock and non-shock trials; in the other the minimal duration of the CS was equal to the CS-US (unconditioned stimulus) interval. When avoidance responses did not terminate the CS shortlatency avoidance responses were not acquired, the cats made more intertrial responses, and removal of the proreal and orbital gyri interfered more with avoidance responding than was observed in the other group. Abolition of shock application and introduction of a fixed duration of the CS resulted in extinction of the avoidance responses, which was more rapid in cats trained under the response contingent CS termination procedure. The data suggest that responses performed during the CS--US interval should be divided into two subclasses: short-latency responses which not only avoid pain but also avoid fear conditioned to the CS, and long-latency responses which avoid pain and escape from the fear state.
INTRODUCTION
In a series of experiments in which cats were trained in active barpressing avoidance of painful shock, it has been shown that short- and longlatency responses differ in their susceptibility to prefrontal lesions [40-44].
380
! -moval of proreal and orbital gyri in cats resulted in a pronounced decrease in the frequency of short-latency avoidances which does riot recover during post-operative retraining. In contrast, long-latency avoidance responding was as good as in intact cats. On the basis of these data it has been postulated that different physiological mechanisms are responsible for performance of shortand long-latency avoidance responses [14, 41]. According to the contingencies employed in avoidance training, an instrumental response emitted during the predetermined isolated period of conditioned stimulus (CS) action is effective in avoiding the painful unconditioned stimulus (US), which provides the primary source of reinforcement of the learned response. By the laws of classical conditioning the CS acquires fearevoking properties during early stages of training [8, 21, 27, 29, 32]. Two-factor theories of avoidance learning consider the fear elicited by the CS to be a mediator of the avoidance response [20, 29, 35]. Termination of the CS and/or the fear state provides the secondary source of reinforcement of the avoidance response [2, 30, 36]. However, numerous data indicate that autonomic changes, which are considered to be indices of the fear state, are observed with latencies of several hundreds of millisecond or longer [2, 26, 34, 35]. Thus instrumental responses, depending on their latency after the CS onset, can be performed on a background of either weak or fully developed fear. Our hypothesis postulates that avoidance responses that are executed with long latencies may be considered to be escapes from fear, whereas short.latency responses are avoidances of fear [41]. If this hypothesis is correct it may be expected t!:.at experimental conditions in which instrumental responses are effective in avoidance of the US but ineffective in termination of the fear-evoking CS (and thus ineffective in preventing the development, of the fear state), will prevent the acquisition of short-latency avoidance responses. On the other hand, the long-latency avoidance responses, for which the main source of reinforcement is prevention of the US, should be acquired. These predictions were tested in the present study by examining the effects of a procedure in which the minimal duration of the CS was equal to the CS-US interval. MATERIAL AND METHODS
Experiments were carried out on 9 adult male cats split into two groups. The apparatus was a rectangular cage (55 cm long, 55 crn wide and 40 cm high) with a bar measuring 10 x 2 cm located in the center of one wall of the cage, 8 cm above the floor. The source of the CS was a loud-speaker located near the centre of the ceiling of the box, through which 70 dB (re 0.0002 dyn/~,an2)white noise was delivered. The US was a scrambled electric shock of 1.0--4.0 mA
381 intensity delivered through the grid-floor to the paws of the animal. The shock intensity was established individually for each animal, based on observation of the animal's behavior during the first 5 days of training, after which it remained constant throughout the experiments. Ten trials were given daily with intertrial intervals of 40, 60 and 80 sec, randomly distributed. In both groups the trial started with the CS onset. For Group 1 (5 animals) a bar-press executed within 5 sec after CS onset immediately terminated the CS and prevented the shock to the grid floor. For Group 2 (4 a~3imals) a bar-press response emitted within 5 sec after CS onset was equally effective in preventing the shock US. However, the CS was terminated only after 5 sec from its onset. In both groups if an avoidance response did not occur within 5 sec of CS onset the grid floor was electrified and both stimuli lasted until the animal performed the bar-press, which was labeled an escape response. Training was carried out until the cats reached a criterion of 90 avoidance responses in 100 consecutive trials: the last 10 training sessions were referred to as the acquisition criterion period. Then all cats underwent removal of the prefrontal region (proreal and orbital gyri) by aspiration under Nembutal anesthesia. Post-operative training began 10 days after surgery and was carried out until the 90% criterion of avoidance pertbrmance in 100 consecutive trials was again reached. On the day after the postoperative criterion was met, 10 extinction sessions of l0 trials each began. For both groups on each extinction trial the CS was given for a fixed period of 5 sec without US administration and independently of the animal's behavior. After completion of the extinction period the animals were sacrificed with an overdose of Nembutal and their brains were subjected to histological analysis using Kluver's and Nissrs techniques. RESULTS
The course of learning The mean number of trials to reach the acquisition criterion was 300 for Group 1 and 560 for Group 2. However, this difference was not statistically significant. The course of learning was analyzed using the Vincent method [12, 38]. The total number of training trials for a given subject was divided into 5 blocks of equal length. Then for each block of trials group means were calculated using the following measures of behavior: (i) percent frequency of avoidance responding; (ii) median latency of instrumental responses, and (iii) level of intertrial responding per minute. As seen in Table I, the course of acquisition of the avoidance response was similar in both groups. However, Group 2 was characterized by longer latencies of instrumental responses and a higher rate of intertrial respc~nding. The respe,,se latencies were subjected to further detailed analysis.
382 TABLE I
Changes of the mabl indicesof behavior in consecutiveblocks Jf the avoidance response acquisition A, avoidance performance (in % of total trials); B, mean median latencies of instrumental responses (in sec); C, rate of intertrial responding (per min). In the body of the Table group means and the results of analyses of variance are given. A
B
C
Vincentized.fifth
Group !
Group2
Group I
Group2
Group I
Group2
! !1 III IV V
19.1 41.8 65.7 83.2 94.5
19.9 26.9 52.2 72.2 89.8
7.1 5.3 3.6 2.8 2.6
7.5 5.5 4.8 3.9 3.1
0.52 0.58 0.50 0.52 0.26
!L41 0.75 0.76 0.58 0.41
Source of variation
df
ValuesofF statistics
Groups ~. Blocks Interaction
1 ;7 4;28 4;28
5.07 49.45*** < 1
9.23** 28.52*** < 1
< 1 3.08* < i
* P < 0,05; ** P < 0.025; *** P < 0.001. 100
ur
-
100
80
SO
60
60
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y
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10
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T
2
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5
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6
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Ics lus
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Fig. !. Cumulative percentage frequency distributions of response latencies for Group 1 (left panel) and for Group 2 (fight panel) in consecutive Vincentized fifths of training. Filled circles represent avoidance responses, and open circles represent escape responses emitted during joint CS and US presentations. Roman numbers denote consecutive Vincentized fifths of training.
383
Cumulative relative frequency distributions of response latencies in consecutive Vincentized fifths of training are shown in Fig. 1. The method of construction of the functions presented in this figure (and also in Figs. 3 and 4) involved the ordering of frequencies of responding by each subject at 0.1 sec intervals. The cumulative frequency at each 1 sec interval of the CS--US interval and for the first 5 see of joint action of the CS and US was then determined and this subtotal was calculated for each subject as a percentage of the total number of trials within the analyzed block of trials. Then the mean percentage for each group and block of trials was estimated and these means are presented in the figures. Accordingly, the various points on the curves represent the magnitude of the cumulative percentage frequency of responding at successive 1 sec periods after CS onset, relative to the total opportunity for responding in that group and block of trials. Within-group comparisons of the cumulative distributions of response latencies, presented in Table II, indicate that for each consecutive Vincentized fifth of training, response latencies were stochastically shorter than for the preceding one (Smirnov test, [10]). Comparison of the points of Dm~ given in Table II with the median latency values given in Table I indicate that in each case the latency at which the maximal vertical distance occurred between compared distributions from consecutive fifths was greater than the mean median latency of the distribution of the more advanced fifth of training involved TABLE I1
Changes in the distribution of response latencies between consecutive Vincentized.fifths of avoidance acquisition in each experimental group Comparison
Direction of difference
D,,~x
Point of maximum distance ( sec)
SI < Sn Su < S m . S m < Sly Sly < Sv
0.32"* 0.30"* 0.16" 0.18"*
7.65 4.65 5.15 4.25
$1 < Sll $u < S m $m < Sly $1v < Sv
0.28** 0.28** 0.19'* 0.21"*
6.05 5.05 5.25 4.25
Group ! I vs I1 II vs III 111 vs IV IV vs V
Group 2 I II III IV
vs vs vs vs
II I11 IV V
* P < O . 0 0 5 ; ** P < 0 . 0 0 1 .
384 T A B L E !II
Effect of CS termination on the cumulative distril~ution o.f response latencies estimated for consecutive Vincentized fifths of training: Group ! vs Group 2 comparisons
Vincentized fifih
Direction of difference
D~,
Point of maximum distance ( sec)
I I! ill IV V
Gr I Gr ! Gr i Gr I : :r I
0.06 0.15"* 0.26** 0.23** 0.25**
5.65 3.25 3.05 3.05 3.05
< > > > >
Gr 2 Gr2 Gr 2 Gr 2 Gr2
** P < 0.001.
in the comparison. This shows that in the course of avoidance acquisition the greatest changes in responding occurred within the long-latency responses. Between-group comparisons of the cumulative distributions of response latencies {Table III) indicate that in each Vincentized fifth of training, except for the first one, response latencies for Group I were stochastically shorter than for Group 2 (the same test). It is interesting to note that beginning with the second Vincentized fifth of training the latency at which the D~, occurred did not change in spite of the consistent shortening of the mean median ~atencies of responses in each experimental group. Because in Group 2 the CS was not terminated by the avoidance response, on 2.5% of the trials the cats performed additional bar-presses during the prolonged CS action. These are called extra-responses (ERs). Most of them were executed from 0.55 to 1.55 sec after the avoidance response. Two ERs within the same trial were very infrequent. The frequency of extra-responses per time unit of the prolonged CS action did not change significantly over the course of training. The frequency of ERs was compare I with a s~milar measure for intertrial responses (ITRs) for each consecutive Vi lcentized fifths of training. For each ITR the latency of the response from the last CS termination was measured. For each subject and Vincentized fifth the ITRs were ordered at ! sec intervals. Then ITR rates, as frequencies of ITRs per sec, were calculated based on the available time periods for emission of ITRs (up to 40 sec for 100% of intertrial intervals, from 41 to 60 sec for 66.6% of intervals, from 61 to gO sec for 33.3% of intervals). Mean frequencies for each group and Vince,ntized fifth were estimated and are presented in Fig. 2. Similarly, for Group 2, ER rates, as frequencies of ERs per sec,-were estimated for each subject arid block of trials, by dividing the number of ERs emitted by the total duration of the CS
385
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Fig. 2. Frequencies of intertrial responses per sec in consecutive 5 sec periods of the intertrial intervals (open bars) for Group 1 (left panels) and for Group 2 (right panels) in consecutive Vincentized fifths of training. For Group 2 frequencies ofextra-responscs p~r sec are also presented (crossed bar~).
after performance of the avoidance response. As seen in Fig. 2, in both groups the largest portion of ITRs was performed soon after CS termination, after which the frequency of ITRs decreased exponentially. It is interesting to note that beginning with the second Vincentized fifth of training, the frequencies of ERs performed by cats of Group 2 seem to fit the exponentially decreasing curves of the ITR frequencies. The logarithmic values of the frequencies of the ERs and the ITRs executed within 30 see after the CS termination show linear relationships with time• Additionally, the frequencies of f i R s emitted after non-shock and shock trials for each group and Vincentized fifth of training were compared. It was found that more ITRs were performed after escape than after avoidance responses (F:/7= 12.17, P<0.025) aed this difference increased during the course of training (F4/28= 2.99, P < 0.05), although the overall level of intertriai responding was similar in both groups and did not change significantly with training.
386 TABLE IV
Comparison of the main indices of behavior in 50-trial blocks immediately before lesions, just after lesions, and at the end of post-operative retraining Headings o f the columns as in Table I.
Block
A
B
C
Group 1
Group 2
Group I
Group 2
Group 1
Group 2
Ire-operative Post-operative After retraining
94.1 81.2 92.3
93.5 72.5 92.5
2.5 2.9 2.8
3.0 4. I 3.5
0.29 0.73 0.48
0.32 0.68 0.28
Source of variation
df
Valuesof F statistics
Groups Blocks Interaction
1 ;7 2;14 2;14
1.01 12.68"** < I
9.07** 4.55* 1.17
< 1 4.45* < I
* P < 0 . 0 5 ; ** P < 0 . 0 2 5 ; *** P < 0 . 0 0 1 .
Effects of prefrontal lesions Removal of proreal and orbital gyri resulted in a decrease of avoidance performance in 8 out of 9 ::ats. This effect was more long-lasting in Group 2 than in Group 1, as indicated by the mean numbers of trials required to reach the post-operative criterion: 114 trials for Group 1 and 375 trials for Group 2 (P < 0.016, Mann-Whitney test, two-tailed). To separate the effects of lesions from those of post-operative retraining, the last 50 preoperative trials, the first 50 post-olx:rative trials, and the last 50 trials of post-operative retraining were compared. As shown in Table IV the lesions also resulted in an increase in response latencies and an increase in ITRs. Furthermore, Duncan tests indicated that, even at the end of the retraining period, neither the response latenci:-s nor frequency of 1TRs returned to the preoperative levels (P < 0.05). Examination of the distributions of ITRs showed that the post-operative increase in ITR rate was restricted only to the first 5 sec of the intertrial interval. The rate of ERs in Group 2 did not change after the lesions. The post-operative lengthening of response latencies, the decrease in avoidance performance and its recovery after post-operative retraining due to the increase in probability of long-latency avoidance responses, may be inferred from the gradients presented in Fig. 3. The results of statistical analyses of these cumulative frequency distributions are presented in Table V. The data
387 100 •
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/ 60
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2
5
3
v
8 9 T,me
10 in
0 1 2 Seconds
i
i
3
~
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[CS
[C$
lus
lus
Fig. 3. Cumulative relative frequency distributions of response latencies for Group 1 (left panel) and for Group 2 (fight panel) during the last 50 trials before lesions (solid line), during the first 50 trials after lesions (broken line), and during the last 50 trials of post-operative retraining (broken line separated with dots).
TABLE V
Comparisons of the distributions of response latencies estimated for the last 50 trials before lesions (Sl), the first 50 trials after lesions ($2) and the last 50 trials of post-operative retraining ($3)
Comparison
Direction of difference D,,~
Point of maximum distance (sec)
S! >$2 $2 < $3 $1 > $3
0.16"* 0.14" O.! 5**
4.25 5.15 2.15
S, > $2 $2 < $3 St > $3
0.30*** 0.30*** 0.21"**
3.65 5.05 3.65
Group I SIvs $2 $2 vs $3 Si vs $3
Group 2 SI vs $2 $2 vs $3 SI vs $3 * P
P<0.01;
*** P < O . 0 0 1 .
388 indicate that lesions resulted in a more pronounced shift of the distributions toward longer latencies in Group 2 than in Group 1. Post-operative recovery was also less effective in Group 2 than in Group 1. As seen in Fig. 3, the post-operative decrease in the execution of avoidance responses with latencies shorter than 2 sec was irreversible in both groups. Between-group comparisons of distributions for pre- and post-operative blocks of trials indicated that in each case response latencies in Group 1 were stochastically shorter than in G r o u p 2 ( P < 0.001, Smirnov test, two-tailed).
Extinction of avoidance responding For all cats the extinction procedure differed from that during their regular training sessions because of the introduction of the fixed 5 sec duration of the CS and the cessation application of the US shock. As seen in Fig. 4, these changes resulted in a decrease in instrumental responding, which was more rapid in Group l than in Group 2. Examination of individual records showed that during the last three extinction sessions four cats from Group 1 and only one cat from Group 2 did not perform any bar-pressing responses. Comparison of the numbersoftrialson which instrumental responses were performed (Table VI, part A) indicate that Group 1 was less resistant to extinction that Group 2, which resulted in a significant interaction between Groups and Blocks. It can
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3
4
5
6
7
8
9
10
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Fig. 4. Cumulative relative frequency distributions of response latencies for Group I (left panel) and for Group 2 (right panel) during the last 50 trials of post-operative retraining (broken line separated with dots), during the first block of 50 extinction trials (broken line) and during the second block of 50 extinction trials (solid line).
389 TABLE VI
Comparison of the main indices of behavior in 50-trial blocks at the end of post-operative retraining and during the first and second halves of extinction Headings of the columns as in Table 1.
Block
A
B
C
Group I
Group 2
Group 1
Group 2
Group 1
Group 2
After retraining 1st half of extinction 2nd half of extinction
92.8 30.8 !.6
92.5 68.5 27.5
2.8 3.2 4.7
3.5 3.7 3.7
0.48 0.46 0.12
0.28 0.72 1.18
Source of variation
df
Values o f f statistics
1 ;7 2;14 2;14
161.50"* 19.90"* 9.29*
• Groups Blocks Interaction
17.26"* < I 10.90"
2.67 < 1 1.61
* P<0.005;** P<0.001.
also be seen in the same Table that the extinction procedure resulted in some lengthening of response latencies and an increase in the variability of the ITR scores. Performance of ERs decreased considerably, and during the last 50 extinction trials only one ER was emitted by cats in Group 1 and five ERs by cats of Group 2.
Histological verification of the lesions The extent of cortical damage was specified for each cat and the results of reconstructions were transferred into standard drawings to eliminate differences in shape of the cat brain and to facilitate comparison of the lesions. The extents of the largest and the smallest lesions in each Group are presented in Fig. 5. In none of the cats were the lesions complete, and caudal parts of the orbital gyrus were left intact. In cat M-I 1 from Group 1 a superficial lesion on the lateral border of the sulcus presyivius was observed. However, the postoperative performance of this cat did not differ from the others. DISCUSSION
The role of CS termination in avoidance conditioning has been investigated intensively for more than 20 years. Both trace and delayed conditioning procedures have been used. The trace procedure provides an opportunity to
390 GROUP:]: M-11
M-2
M-§
GROUP~
M-9
$21
~
1241
Fig. 5. Reconstructions of the lesions and the cross-sections through the largest and the smallest lesions in each group. From the upper part to the bottom the brain reconstructions are of cats M-2, M-II (Group I) and M-6, M-9 (Group 2).
present CSs of shorter duration than latencies of the avoidance responses [3, 9, 31]. in the delayed procedure a CS of either a fixed duration, equal to the length of the CS-US interval, can be employed [4, 7, 11, 15-17] or CS termination can be postponed for a fixed period of time after performance of the avoidance response [1, 3, 5, 6, 16, 18, 19, 31]. The results of these studies showed that
391 both US omission and CS termination have reinforcing effects on avoidance responding. When CS termination was not contingent upon the execution of the avoidance response the learning was more difficult and the final level of responding lower. These studies also reported that avoidance responses were executed with longer latencies when CS termination was not response-contingent [7, 9, 15-18]. Only the mean (or median) latencies of the avoidance responses were compared, and no attention was paid to the problem of whether a special subclass of avoidance responses, the short-latency responses, were lost. Rather, these studies attempted to evaluate the relative importance of CS termination and US omission for acquisition of the avoidance responding. The final answer to this question was obtained later on, when it was shown in deafferented animals that avoidance responding could be acquired on the basis of only the association between the central motor command to flex the limb and the non-occurrence of the shock [25, 37]. The present paper concerns another problem: whether responses effective in avoidance of the painful US should be divided into subclasses depending on their latency characteristics. Based on the Mowrer-Miller understanding of fear as a secondary drive, it may be assumed that a subject is able to learn to avoid not only pain b , t also fear itself. Responses which are performed shortly after the CS onset, before the fear state reaches its full strength, can terminate not only the CS action but also prevent further increases in fear. Responses performed in later parts of the CS-US interval, when the fear state is fully developed, cannot avoid fear but only terminate it. Thus, the difference between short- and long-latency avoidance responses with respect to the secondary reinforcing properties of CS termination are analogous to those which exist between avoidance and escape responses with respect to the primary reinforcing properties of omission and termination of the painful US. Accordingly, an instrumental response performed at the beginning of the CS.-US interval may be considered as avoidance of pain and avoidance of conditioned fear responses, whereas any emitted with longer latency may be considered as avoidance of pain and escape from conditioned fear state. It has been shown recently that short-latency responses were acquired in later stages of training only after the long-latency responses had been performed on nearly 50~ of trials [14, 39, 44]. The present experiment demonstrated that short-latency responses were not acquired under the procedure in which the avoidance response was ineffective in termination of the fear-evoking CS. There are two possible mechanisms responsible for this outcome. Either the shortlatency avoidance responses were not acquired because the CS of long duration precluded avoidance of fear, or the short-latency responses deteriorate because they were punished by the prolongation of the fear-evoking CS. Since cats trained with a CS that had a minimal duration equal to the CS-US interval did not perform responses with latencies shorter than 1 sec in any stage of training,
392 it may be inferred that the secondary reinforcing effect of CS termination is necessary for acquisition of short-latency responses. In this respect the present experiment is more conclusive than the previous one performed on dogs trained under a partial reinforcement procedure for avoidance [45]. After initial training with both CS termination and US omission contingent upon the instrumental response, the procedure was changed so that on 50% of ~ a l s there was a fixed CS duration and no shock. Between-group comparisons revealed that this change hampered further shortening of response latencies, and the two groups of dogs maintained a difference in speed of responding during all further stages of training and testing. Since the partial reinforcement procedure was introduced after the clogs had reached a criterion of 80~ avoidance and shock trials were therefore infrequent, the between-group differences were considered to be related to the delay of CS-termination and not to the reduction in shock availability. In the dog experiment probably the lack of both the reinforcing effect of CS termination and the punishing effect of CS prolongation were responsible for long-latency responding of the dogs subjected to the partial reinforcement procedure. The term 'avoidance of fear' given to short-latency responses is not precise. In fact, all avoidance responses are performed on a background of fear conditioned not only to the discriminative CS but also to the whole experimental situation. The CS used in avoidance training serves different functions. It signals the painful US which has to be either avoided or escaped, it elicits a complex of autonomic changes which are considered as indices of fear, and it also adds an increment to the background level of fear conditioned to the experimental situation. This last function of the CS, i.e. its non-specific arousing effect, is independent of the signalling property of the CS and increases the frequency of responses that are conditioned to the experimental situation [13]. The direct relation between the CS intensity and the proportion of avoidance responses executed with short latencies has been shown both in cats [14, 44, 46, 47] and in dogs [22-24]. Exceptionally low levels of short-latency avoidance responses were observed with CSi consisting of a decrease in the background noise intensity [44]. When such stimuli were used, the proportion of avoidance responses emitted with latencies shorter than I sec was lower than expected from the probability of intertrial responses for this period of time. Thus, depending on the intensity relations between the CS and the background noise level, CS onset either increases or decreases the level of fear conditioned to the experimental situation and influences the proportion of short-latency avoidance responses which are considered as driven by the non-specific arousing effect of the CS onset [14]. Intertrial responding may be considered as an index of fear conditioned to the whole experimental situation. Data presented in this paper indicate that ITRs were more frequently performed after escape than after avoidance trials.
393 After avoidance trials the frequency of ITRs was higher in Group 2, in which the CS was not terminated by the avoidance response, than in Group 1, in which termination of the CS was response contingent on all trials. In spite of a higher level of fear conditioned to the experimental situation the CS onset in Group 2 did not elicit short-latency avoidance responses at any stage of training and testing. This provides further support for the notion that termination of the CS by the avoidance response is a necessary condition for acquisition of shortlatency responses. The effects of prefrontal lesions presented in this paper are concordant with those previously reported [40-44]. The between-group comparison showed that the smaller thc proportion of short-latency responses performed before lesions the more was the cumulative distribution of response latencies affected by the prefrontal operations. In neither group did the frequency of shortlatency avoidance responses recover after post-operative retraining. Data from the acquisition and post-operative stages of the experiment seem to indicate a lower response strength when CS termination was not contingent upon the avoidance response. However, the avoidance responses acquired under that procedure were more resistant to extinction than in the other group. Abolition of shock and introduction of a fixed duration CS in the extinction sessions was a greater change in the experimental procedure for Group I than for Group 2. The more rapid weakening of avoidance responding in Group I was presumably due to the punishing effect of the CS persisting after the instrumental response. Additionally the level of fear conditioned to the experimental situation, as indicated by ITR rate, was higher in Group 2 than in Group 1. Results of the present experiment demonstrate a strong effect of CS termination on several indices of avoidance behavior. Response-contingent CS termination resulted in more efficient avoidance responding a:,d a lowered level of fear conditioned to the experimental situation. Collectively the data are consonant with the hypothesis that the biological role of short-latency avoidance responses is to avoid fear conditioned to the discriminative CS. ACKNOWLEDGEMENTS
This investigation was supported by Foreign Research Agreement 05-282-A of the U.S. Department of Health, Education and Welfare under PL 480. The authors are indebted to Dr. F.B. Brush for interesting discussions during the preparation of this paper and for his correction of its English style. REFERENCES 1 Bixenstine, V.E. and Barker, E., Further analysis of the determinants of avoidance behavior, J. comp. physiol. Psychol., 58 (1964) 339-343. 2 Biack, A.H., Cardiac conditioning in curarized dogs: the relationship between heart rate and
394
3 4 5 6 7 8
9 10 II 12 13 14 15 16 17 18 19 20 21 22
23
24 25
skeletal behaviour. In W.F. Prokasy (Ed.), Classical Conditioning: A Symposium, AppletonCentury-Crofts, New York, 1965, pp. 20-47. Bones, R.C. and Grossen, N.E., Effects of an informational stimulus on the acquisition of avoidance behavior in rats, J. comp. physiol. Psychoi., 68 (1969) 90-99. Bolles, R.C., Stokes, L.W. and Younger, M.S., Does CS termination reinforce avoidance behavior? J. comp. physiol. Psychol., 62 (1966)201-207. Bolles, R.C. and Tuttle, A.V., A failure to reinforce instrumental behavior by terminating a stimulus that had been paired with shock, Psychon. Sci., 9 (1967) 255-258. Bower, G., Starr, R. and Lazarovitz, L., Amount of response-produced change in the CS and avoidance learning, J. comp. physiol. Psychol., 59 (1965) 13- ! 7. Brush, E.S., Traumatic avoidance learning: the effects of conditioned stimulus length in a free-operant situation, J. comp. physiol. Psychol., 50 (1957) 541-546. Brush, F.R., Brush, E.S. and Solomon, R.L., Traumatic avoidance learning: the effects of CS-US interval with a delayed-conditioning procedure, J. comp. physiol. P~chol., 48 (1955) 285-293. Cole, M. and Wahlsten, D., Response-contingent CS termination as a factor in avoidance conditioning, Psychon. Sci., 12 (1968) 15-16. Conover, W.l., Practical Nonparametric Statistics, John Wiley, New York, 1971. D'Amato, M.R., FazTaro, J. and Etkin, M., Anticipatory responding and avoidance discrimination as factors in avoidance conditioning, J. exp. Psychol., 77 (1968) 41-47. Hilgard, E.R., A summary and evaluation of alternative procedures for the construction of Vincent curves, Psvchol. Bull., 35 (1938) 282-297. Jakubowska, E. and Zieli6ski, K., Dynamogenic effect of stimulus intensity unconfounded by differential densities of reinforcement. Bull. Acad. pol. Sci., Sdr. Sci. Biol., 23 (1975) 135-142. Jakubowska, E. and Zieli6ski, K., Avoidance acquisition in cats as a function of temporal and intensity factors, Acta neurobiol, exp., 39 (1979) 67-86. Kamin, L.J., The effects of termination of the CS and avoidance of the US on avoidance learning, J. comp. physiol. Psychol., 49 (1956) 420-424. Kamin, L.J., The gradient of delay of secondary reward in avoidance learning, J. comp. physiol. Psychoi., 50 (I 957) 445-449. Kamin, L.J., The gradient of delay of secondary reward in avoidance learning tested on avoidance trials only, J. comp. physiol. Psychol., 50 (1957) 450-456. Kamin, L., Campbell, D., Judd, R., Ryan, T. and Walker, J., Two ieterminants of the emergence of anticipatory avoidance, J. comp. physiol. Psychol., 52 (1959) 202-205. Keehn, J.D. and Nakkash, S., Effect of a signal contingent upon an avoidance response, Nature (Lond.), 184 (1959) 566-568. Konorski, J., Conditioned Reflexes mad Neuron Organization, Cambridge University Press, Cambridge, 1948, p. 228. Konorski, J. and Miller, S., Conditioned rcqexes of the motor analyser, Tr. Fiziol. Lab. Akad. !. P. Pavlova, 6 (1936) 119-288 (in Russian). Kowalska, D., Dabrowska, J. and Zielifiski, K., Effects of partial prefrontal lesions in dogs on go-no go avoidance reflex differentiation and reversal learning, Acta neurobiol, exp., 35 (1975) 549-580. Kowalska, D., Dabrowska, J. and Zielifiski, K., Retention of symmetrical go-no go avoidance differentiation after prefrontal lesions in dogs. Bull. Acad. pol. Sci., S6r. Sci. Biol., 23 (1975) 487-494. Kowaiska, D. and Zielifiski, K., Avoidance responding in dogs trained in symmetrical or asymmetrical go, no-go differentiation, Acta neurobiol, exp. 40 (1980) 403-432. Kozlovskaia, I.B., Afferent Control of Voluntary Movements, Nauka, Moskow, 1976, p. 48.
395 26 Martin, I. and Levey, A.B., The Genesis of the Classical Conditioned Response, Pergamon Press, Oxford, 1969, p. 47. 27 Miller, N.E., Studies of fear as an acquirable drive: 1. Fear as motivation and fear-reduction as reinforcement in the learning of n~,v responses, J. exp. Psychol., 38 (1948) 89-101. 28 Miller, N.E., Learnable drives and rewards. In S.S. Stevens (Ed.), Handbook of Experimemal Psychology, Wiley, New York, 1951, pp. 435-472. 29 Mowrer, O.H., On the dual nature of learning. A re-interpretation of "conditioning' and 'problem solving', Harv. educ. Rev., 17 (1947) 102-148. 30 Mowrer, O.H., Learning Theory and Behavior, Wiley, New York, 1960, p. 28. 31 Mowrer, O.H. and Lamoreaux, R.R., Avoidance conditioning and signal duration -- a study of secondary motivation and reward, Psychol. Monogr., 54 (1942) 4-34. 32 Mowrer, O.H. and Lamoreaux, R.R., Fear as an intervening variable in avoidance conditioning, J. comp. PsychoL, 39 (1946) 29-50. 33 Schoenfeid, W.N., An experimental approach to anxiety, escape and avoidance behavior. In P.H. Hoch and J. Zubin (Eds.), Anxiety, Grune and Stratton, New York, 1950, pp. 70-99. 34 Solomon, R.L., Kamin, L.J. and Wynne, L.C., Traumatic avoidance learning: the outcomes of several extinction procedures with dogs, J. abnorm, soc. Psychol., 48 (i 953) 291-302. 35 Solomon, R.L. and Wynne, L.C., Traumatic avoidance learning: the principle of anxiety conservation and partial irreversibility. Psychol. Rev., 61 (1954) 353-385. 36 Soi~ysik, S. and Kowalska, M., Studies on the avoidance conditioning. I. Relations between cardiac (Type l) and motor (Type II) effects in the avoidance reflex, Acta Biol. Exp. (Warszawa), 22 (1960) 157-170. 37 Taub, E. and Bcrman, AJ., Avoidance conditioning in the absence of relevant proprioceptive and exteroceptive feedback, J. comp. physiol. Psychoi., 56 (1963) 1012-1016. 38 Vincent, S.P,, The function of the vibrisae in the behavior of the white rat, Behav. Monogr., 1 (1912) 1-81. 39 Werka, T, and Zielifiski, K., Effects of lesions in the amygdaloid nucleus centralis on acquisition and retention of avoidance reflexes in eats, Acta neurobiol, exp, 38 (1978) 247--270. 40 Zielifiski, K., Retention of the escape after prefrontal Iobectomy in cats, Acta neurobiol, exp.. 30 (1970) 43-57. 41 Zielifiski, K., Effects of prefrontal lesions on avoidance and escape responses, Acta neurobiol. exp., 32 (1972) 393-415. 42 Zielifiski, K., Stimulus intensity and prefrontal lesion effects on latencies of the bar-pressing avoidance response in cats, Bull. Acad. pol. $ci., S~r. $ci. Biol., 20 (1972) 821-826. 43 Zielifiski, K., Changes in avoidance response latencies after prefrontal lesions in cats: group versus individual data, Acta neurobiol, exp., 34 (1974) 477-490. 44 Zielifiski, K., Cueing properties of the decrease of white noise intensity for avoidance conditioning in cats, Acta neurobioL exp., 39 (1979) 263-283. 45 Zielifiski, K., Brennan, J. and Kowalska, D., Auditory frequency generalization in normal and prefrontal dogs trained in varieties of active avoidance reflexes, Acta neurobiol, exp.. 39 (1979) 285-31 I. 46 Zielifiski, K. and Czarkowska, J., Go-no go avoidance reflex differentiation and its retention after prefrontal lesion in cats, Acta neurobiol, exp.. 33 (1973) 467-490. 47 Zielitiski, K. and Czarkowska, J., Quality of stimuli and prefrontal lesions effects on reversal learning in go-no go avoidance reflex differentiation in cats, Acta neurobiol, exp., 34 (1974) 43-68.
379
© Elsevier/North-Holland Biomedical Press
THE ROLE OF CONDITIONED STIMULUS TERMINATION IN SHORT-LATENCY AVOIDANCE RESPONDING IN CATS
K A Z I M I E R Z ZIELII~ISK! and M A E G O R Z A T A P L E W A K O
Department of Neurophysiology. Nencki Institute of Experimental Biology. Warsaw (Poland) (Received February 2nd, 1980) (Accepted June 3rd, ! 980)
Key words: avoidance - - conditioned stimulus termination - - latency distributions - - intertrial responding - - prefrontal lesions - - extinction
SUMMARY
The behavioral effects of two procedures for bar-Fressing avoidance training in cats were studied. In one procedure conditioned stimulus (CS) termination was response-contingent on both shock and non-shock trials; in the other the minimal duration of the CS was equal to the CS-US (unconditioned stimulus) interval. When avoidance responses did not terminate the CS shortlatency avoidance responses were not acquired, the cats made more intertrial responses, and removal of the proreal and orbital gyri interfered more with avoidance responding than was observed in the other group. Abolition of shock application and introduction of a fixed duration of the CS resulted in extinction of the avoidance responses, which was more rapid in cats trained under the response contingent CS termination procedure. The data suggest that responses performed during the CS--US interval should be divided into two subclasses: short-latency responses which not only avoid pain but also avoid fear conditioned to the CS, and long-latency responses which avoid pain and escape from the fear state.
INTRODUCTION
In a series of experiments in which cats were trained in active barpressing avoidance of painful shock, it has been shown that short- and longlatency responses differ in their susceptibility to prefrontal lesions [40-44].
380
! -moval of proreal and orbital gyri in cats resulted in a pronounced decrease in the frequency of short-latency avoidances which does riot recover during post-operative retraining. In contrast, long-latency avoidance responding was as good as in intact cats. On the basis of these data it has been postulated that different physiological mechanisms are responsible for performance of shortand long-latency avoidance responses [14, 41]. According to the contingencies employed in avoidance training, an instrumental response emitted during the predetermined isolated period of conditioned stimulus (CS) action is effective in avoiding the painful unconditioned stimulus (US), which provides the primary source of reinforcement of the learned response. By the laws of classical conditioning the CS acquires fearevoking properties during early stages of training [8, 21, 27, 29, 32]. Two-factor theories of avoidance learning consider the fear elicited by the CS to be a mediator of the avoidance response [20, 29, 35]. Termination of the CS and/or the fear state provides the secondary source of reinforcement of the avoidance response [2, 30, 36]. However, numerous data indicate that autonomic changes, which are considered to be indices of the fear state, are observed with latencies of several hundreds of millisecond or longer [2, 26, 34, 35]. Thus instrumental responses, depending on their latency after the CS onset, can be performed on a background of either weak or fully developed fear. Our hypothesis postulates that avoidance responses that are executed with long latencies may be considered to be escapes from fear, whereas short.latency responses are avoidances of fear [41]. If this hypothesis is correct it may be expected t!:.at experimental conditions in which instrumental responses are effective in avoidance of the US but ineffective in termination of the fear-evoking CS (and thus ineffective in preventing the development, of the fear state), will prevent the acquisition of short-latency avoidance responses. On the other hand, the long-latency avoidance responses, for which the main source of reinforcement is prevention of the US, should be acquired. These predictions were tested in the present study by examining the effects of a procedure in which the minimal duration of the CS was equal to the CS-US interval. MATERIAL AND METHODS
Experiments were carried out on 9 adult male cats split into two groups. The apparatus was a rectangular cage (55 cm long, 55 crn wide and 40 cm high) with a bar measuring 10 x 2 cm located in the center of one wall of the cage, 8 cm above the floor. The source of the CS was a loud-speaker located near the centre of the ceiling of the box, through which 70 dB (re 0.0002 dyn/~,an2)white noise was delivered. The US was a scrambled electric shock of 1.0--4.0 mA
381 intensity delivered through the grid-floor to the paws of the animal. The shock intensity was established individually for each animal, based on observation of the animal's behavior during the first 5 days of training, after which it remained constant throughout the experiments. Ten trials were given daily with intertrial intervals of 40, 60 and 80 sec, randomly distributed. In both groups the trial started with the CS onset. For Group 1 (5 animals) a bar-press executed within 5 sec after CS onset immediately terminated the CS and prevented the shock to the grid floor. For Group 2 (4 a~3imals) a bar-press response emitted within 5 sec after CS onset was equally effective in preventing the shock US. However, the CS was terminated only after 5 sec from its onset. In both groups if an avoidance response did not occur within 5 sec of CS onset the grid floor was electrified and both stimuli lasted until the animal performed the bar-press, which was labeled an escape response. Training was carried out until the cats reached a criterion of 90 avoidance responses in 100 consecutive trials: the last 10 training sessions were referred to as the acquisition criterion period. Then all cats underwent removal of the prefrontal region (proreal and orbital gyri) by aspiration under Nembutal anesthesia. Post-operative training began 10 days after surgery and was carried out until the 90% criterion of avoidance pertbrmance in 100 consecutive trials was again reached. On the day after the postoperative criterion was met, 10 extinction sessions of l0 trials each began. For both groups on each extinction trial the CS was given for a fixed period of 5 sec without US administration and independently of the animal's behavior. After completion of the extinction period the animals were sacrificed with an overdose of Nembutal and their brains were subjected to histological analysis using Kluver's and Nissrs techniques. RESULTS
The course of learning The mean number of trials to reach the acquisition criterion was 300 for Group 1 and 560 for Group 2. However, this difference was not statistically significant. The course of learning was analyzed using the Vincent method [12, 38]. The total number of training trials for a given subject was divided into 5 blocks of equal length. Then for each block of trials group means were calculated using the following measures of behavior: (i) percent frequency of avoidance responding; (ii) median latency of instrumental responses, and (iii) level of intertrial responding per minute. As seen in Table I, the course of acquisition of the avoidance response was similar in both groups. However, Group 2 was characterized by longer latencies of instrumental responses and a higher rate of intertrial respc~nding. The respe,,se latencies were subjected to further detailed analysis.
382 TABLE I
Changes of the mabl indicesof behavior in consecutiveblocks Jf the avoidance response acquisition A, avoidance performance (in % of total trials); B, mean median latencies of instrumental responses (in sec); C, rate of intertrial responding (per min). In the body of the Table group means and the results of analyses of variance are given. A
B
C
Vincentized.fifth
Group !
Group2
Group I
Group2
Group I
Group2
! !1 III IV V
19.1 41.8 65.7 83.2 94.5
19.9 26.9 52.2 72.2 89.8
7.1 5.3 3.6 2.8 2.6
7.5 5.5 4.8 3.9 3.1
0.52 0.58 0.50 0.52 0.26
!L41 0.75 0.76 0.58 0.41
Source of variation
df
ValuesofF statistics
Groups ~. Blocks Interaction
1 ;7 4;28 4;28
5.07 49.45*** < 1
9.23** 28.52*** < 1
< 1 3.08* < i
* P < 0,05; ** P < 0.025; *** P < 0.001. 100
ur
-
100
80
SO
60
60
W
> o E u
t.O
y
L0
o
-
20
20
,
I
2
]
4
.s
6
?
8
g
Time
Ics
10
0 in
T
2
,c
5
,
,
6
?
;
,
g
10
seconds
Ics lus
lus
Fig. !. Cumulative percentage frequency distributions of response latencies for Group 1 (left panel) and for Group 2 (fight panel) in consecutive Vincentized fifths of training. Filled circles represent avoidance responses, and open circles represent escape responses emitted during joint CS and US presentations. Roman numbers denote consecutive Vincentized fifths of training.
383
Cumulative relative frequency distributions of response latencies in consecutive Vincentized fifths of training are shown in Fig. 1. The method of construction of the functions presented in this figure (and also in Figs. 3 and 4) involved the ordering of frequencies of responding by each subject at 0.1 sec intervals. The cumulative frequency at each 1 sec interval of the CS--US interval and for the first 5 see of joint action of the CS and US was then determined and this subtotal was calculated for each subject as a percentage of the total number of trials within the analyzed block of trials. Then the mean percentage for each group and block of trials was estimated and these means are presented in the figures. Accordingly, the various points on the curves represent the magnitude of the cumulative percentage frequency of responding at successive 1 sec periods after CS onset, relative to the total opportunity for responding in that group and block of trials. Within-group comparisons of the cumulative distributions of response latencies, presented in Table II, indicate that for each consecutive Vincentized fifth of training, response latencies were stochastically shorter than for the preceding one (Smirnov test, [10]). Comparison of the points of Dm~ given in Table II with the median latency values given in Table I indicate that in each case the latency at which the maximal vertical distance occurred between compared distributions from consecutive fifths was greater than the mean median latency of the distribution of the more advanced fifth of training involved TABLE I1
Changes in the distribution of response latencies between consecutive Vincentized.fifths of avoidance acquisition in each experimental group Comparison
Direction of difference
D,,~x
Point of maximum distance ( sec)
SI < Sn Su < S m . S m < Sly Sly < Sv
0.32"* 0.30"* 0.16" 0.18"*
7.65 4.65 5.15 4.25
$1 < Sll $u < S m $m < Sly $1v < Sv
0.28** 0.28** 0.19'* 0.21"*
6.05 5.05 5.25 4.25
Group ! I vs I1 II vs III 111 vs IV IV vs V
Group 2 I II III IV
vs vs vs vs
II I11 IV V
* P < O . 0 0 5 ; ** P < 0 . 0 0 1 .
384 T A B L E !II
Effect of CS termination on the cumulative distril~ution o.f response latencies estimated for consecutive Vincentized fifths of training: Group ! vs Group 2 comparisons
Vincentized fifih
Direction of difference
D~,
Point of maximum distance ( sec)
I I! ill IV V
Gr I Gr ! Gr i Gr I : :r I
0.06 0.15"* 0.26** 0.23** 0.25**
5.65 3.25 3.05 3.05 3.05
< > > > >
Gr 2 Gr2 Gr 2 Gr 2 Gr2
** P < 0.001.
in the comparison. This shows that in the course of avoidance acquisition the greatest changes in responding occurred within the long-latency responses. Between-group comparisons of the cumulative distributions of response latencies {Table III) indicate that in each Vincentized fifth of training, except for the first one, response latencies for Group I were stochastically shorter than for Group 2 (the same test). It is interesting to note that beginning with the second Vincentized fifth of training the latency at which the D~, occurred did not change in spite of the consistent shortening of the mean median ~atencies of responses in each experimental group. Because in Group 2 the CS was not terminated by the avoidance response, on 2.5% of the trials the cats performed additional bar-presses during the prolonged CS action. These are called extra-responses (ERs). Most of them were executed from 0.55 to 1.55 sec after the avoidance response. Two ERs within the same trial were very infrequent. The frequency of extra-responses per time unit of the prolonged CS action did not change significantly over the course of training. The frequency of ERs was compare I with a s~milar measure for intertrial responses (ITRs) for each consecutive Vi lcentized fifths of training. For each ITR the latency of the response from the last CS termination was measured. For each subject and Vincentized fifth the ITRs were ordered at ! sec intervals. Then ITR rates, as frequencies of ITRs per sec, were calculated based on the available time periods for emission of ITRs (up to 40 sec for 100% of intertrial intervals, from 41 to 60 sec for 66.6% of intervals, from 61 to gO sec for 33.3% of intervals). Mean frequencies for each group and Vince,ntized fifth were estimated and are presented in Fig. 2. Similarly, for Group 2, ER rates, as frequencies of ERs per sec,-were estimated for each subject arid block of trials, by dividing the number of ERs emitted by the total duration of the CS
385
0.16
IV
0.1;
012 II
O08
OO8
g
L
00~
{3,
014•
-
~. 010
V
010"
0 r"
OO6, It.
002
~=,=---i:=-,,=~ 0
z,O
80
0
Time
after
40 CS
80 off:;~t
0 in
"0
8O
L 0
~0
8o
seconds
Fig. 2. Frequencies of intertrial responses per sec in consecutive 5 sec periods of the intertrial intervals (open bars) for Group 1 (left panels) and for Group 2 (right panels) in consecutive Vincentized fifths of training. For Group 2 frequencies ofextra-responscs p~r sec are also presented (crossed bar~).
after performance of the avoidance response. As seen in Fig. 2, in both groups the largest portion of ITRs was performed soon after CS termination, after which the frequency of ITRs decreased exponentially. It is interesting to note that beginning with the second Vincentized fifth of training, the frequencies of ERs performed by cats of Group 2 seem to fit the exponentially decreasing curves of the ITR frequencies. The logarithmic values of the frequencies of the ERs and the ITRs executed within 30 see after the CS termination show linear relationships with time• Additionally, the frequencies of f i R s emitted after non-shock and shock trials for each group and Vincentized fifth of training were compared. It was found that more ITRs were performed after escape than after avoidance responses (F:/7= 12.17, P<0.025) aed this difference increased during the course of training (F4/28= 2.99, P < 0.05), although the overall level of intertriai responding was similar in both groups and did not change significantly with training.
386 TABLE IV
Comparison of the main indices of behavior in 50-trial blocks immediately before lesions, just after lesions, and at the end of post-operative retraining Headings o f the columns as in Table I.
Block
A
B
C
Group 1
Group 2
Group I
Group 2
Group 1
Group 2
Ire-operative Post-operative After retraining
94.1 81.2 92.3
93.5 72.5 92.5
2.5 2.9 2.8
3.0 4. I 3.5
0.29 0.73 0.48
0.32 0.68 0.28
Source of variation
df
Valuesof F statistics
Groups Blocks Interaction
1 ;7 2;14 2;14
1.01 12.68"** < I
9.07** 4.55* 1.17
< 1 4.45* < I
* P < 0 . 0 5 ; ** P < 0 . 0 2 5 ; *** P < 0 . 0 0 1 .
Effects of prefrontal lesions Removal of proreal and orbital gyri resulted in a decrease of avoidance performance in 8 out of 9 ::ats. This effect was more long-lasting in Group 2 than in Group 1, as indicated by the mean numbers of trials required to reach the post-operative criterion: 114 trials for Group 1 and 375 trials for Group 2 (P < 0.016, Mann-Whitney test, two-tailed). To separate the effects of lesions from those of post-operative retraining, the last 50 preoperative trials, the first 50 post-olx:rative trials, and the last 50 trials of post-operative retraining were compared. As shown in Table IV the lesions also resulted in an increase in response latencies and an increase in ITRs. Furthermore, Duncan tests indicated that, even at the end of the retraining period, neither the response latenci:-s nor frequency of 1TRs returned to the preoperative levels (P < 0.05). Examination of the distributions of ITRs showed that the post-operative increase in ITR rate was restricted only to the first 5 sec of the intertrial interval. The rate of ERs in Group 2 did not change after the lesions. The post-operative lengthening of response latencies, the decrease in avoidance performance and its recovery after post-operative retraining due to the increase in probability of long-latency avoidance responses, may be inferred from the gradients presented in Fig. 3. The results of statistical analyses of these cumulative frequency distributions are presented in Table V. The data
387 100 •
"lII
80
ss
i
/ / I
.#" ~1[J
c
/
,
/ 60
/
ft I!
1.0
(
20
I
2
5
3
v
8 9 T,me
10 in
0 1 2 Seconds
i
i
3
~
5
[CS
[C$
lus
lus
Fig. 3. Cumulative relative frequency distributions of response latencies for Group 1 (left panel) and for Group 2 (fight panel) during the last 50 trials before lesions (solid line), during the first 50 trials after lesions (broken line), and during the last 50 trials of post-operative retraining (broken line separated with dots).
TABLE V
Comparisons of the distributions of response latencies estimated for the last 50 trials before lesions (Sl), the first 50 trials after lesions ($2) and the last 50 trials of post-operative retraining ($3)
Comparison
Direction of difference D,,~
Point of maximum distance (sec)
S! >$2 $2 < $3 $1 > $3
0.16"* 0.14" O.! 5**
4.25 5.15 2.15
S, > $2 $2 < $3 St > $3
0.30*** 0.30*** 0.21"**
3.65 5.05 3.65
Group I SIvs $2 $2 vs $3 Si vs $3
Group 2 SI vs $2 $2 vs $3 SI vs $3 * P
P<0.01;
*** P < O . 0 0 1 .
388 indicate that lesions resulted in a more pronounced shift of the distributions toward longer latencies in Group 2 than in Group 1. Post-operative recovery was also less effective in Group 2 than in Group 1. As seen in Fig. 3, the post-operative decrease in the execution of avoidance responses with latencies shorter than 2 sec was irreversible in both groups. Between-group comparisons of distributions for pre- and post-operative blocks of trials indicated that in each case response latencies in Group 1 were stochastically shorter than in G r o u p 2 ( P < 0.001, Smirnov test, two-tailed).
Extinction of avoidance responding For all cats the extinction procedure differed from that during their regular training sessions because of the introduction of the fixed 5 sec duration of the CS and the cessation application of the US shock. As seen in Fig. 4, these changes resulted in a decrease in instrumental responding, which was more rapid in Group l than in Group 2. Examination of individual records showed that during the last three extinction sessions four cats from Group 1 and only one cat from Group 2 did not perform any bar-pressing responses. Comparison of the numbersoftrialson which instrumental responses were performed (Table VI, part A) indicate that Group 1 was less resistant to extinction that Group 2, which resulted in a significant interaction between Groups and Blocks. It can
'ooI !
t00 s c ~r m
.- O,-.-u-'-G-
/
I
eo
e~
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i
/
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50'
I
o
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!
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/t
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i i"
I
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6
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J
10
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in
$fC.,o n d $
Ics
I
2
3
4
5
6
7
8
9
10
]
Fig. 4. Cumulative relative frequency distributions of response latencies for Group I (left panel) and for Group 2 (right panel) during the last 50 trials of post-operative retraining (broken line separated with dots), during the first block of 50 extinction trials (broken line) and during the second block of 50 extinction trials (solid line).
389 TABLE VI
Comparison of the main indices of behavior in 50-trial blocks at the end of post-operative retraining and during the first and second halves of extinction Headings of the columns as in Table 1.
Block
A
B
C
Group I
Group 2
Group 1
Group 2
Group 1
Group 2
After retraining 1st half of extinction 2nd half of extinction
92.8 30.8 !.6
92.5 68.5 27.5
2.8 3.2 4.7
3.5 3.7 3.7
0.48 0.46 0.12
0.28 0.72 1.18
Source of variation
df
Values o f f statistics
1 ;7 2;14 2;14
161.50"* 19.90"* 9.29*
• Groups Blocks Interaction
17.26"* < I 10.90"
2.67 < 1 1.61
* P<0.005;** P<0.001.
also be seen in the same Table that the extinction procedure resulted in some lengthening of response latencies and an increase in the variability of the ITR scores. Performance of ERs decreased considerably, and during the last 50 extinction trials only one ER was emitted by cats in Group 1 and five ERs by cats of Group 2.
Histological verification of the lesions The extent of cortical damage was specified for each cat and the results of reconstructions were transferred into standard drawings to eliminate differences in shape of the cat brain and to facilitate comparison of the lesions. The extents of the largest and the smallest lesions in each Group are presented in Fig. 5. In none of the cats were the lesions complete, and caudal parts of the orbital gyrus were left intact. In cat M-I 1 from Group 1 a superficial lesion on the lateral border of the sulcus presyivius was observed. However, the postoperative performance of this cat did not differ from the others. DISCUSSION
The role of CS termination in avoidance conditioning has been investigated intensively for more than 20 years. Both trace and delayed conditioning procedures have been used. The trace procedure provides an opportunity to
390 GROUP:]: M-11
M-2
M-§
GROUP~
M-9
$21
~
1241
Fig. 5. Reconstructions of the lesions and the cross-sections through the largest and the smallest lesions in each group. From the upper part to the bottom the brain reconstructions are of cats M-2, M-II (Group I) and M-6, M-9 (Group 2).
present CSs of shorter duration than latencies of the avoidance responses [3, 9, 31]. in the delayed procedure a CS of either a fixed duration, equal to the length of the CS-US interval, can be employed [4, 7, 11, 15-17] or CS termination can be postponed for a fixed period of time after performance of the avoidance response [1, 3, 5, 6, 16, 18, 19, 31]. The results of these studies showed that
391 both US omission and CS termination have reinforcing effects on avoidance responding. When CS termination was not contingent upon the execution of the avoidance response the learning was more difficult and the final level of responding lower. These studies also reported that avoidance responses were executed with longer latencies when CS termination was not response-contingent [7, 9, 15-18]. Only the mean (or median) latencies of the avoidance responses were compared, and no attention was paid to the problem of whether a special subclass of avoidance responses, the short-latency responses, were lost. Rather, these studies attempted to evaluate the relative importance of CS termination and US omission for acquisition of the avoidance responding. The final answer to this question was obtained later on, when it was shown in deafferented animals that avoidance responding could be acquired on the basis of only the association between the central motor command to flex the limb and the non-occurrence of the shock [25, 37]. The present paper concerns another problem: whether responses effective in avoidance of the painful US should be divided into subclasses depending on their latency characteristics. Based on the Mowrer-Miller understanding of fear as a secondary drive, it may be assumed that a subject is able to learn to avoid not only pain b , t also fear itself. Responses which are performed shortly after the CS onset, before the fear state reaches its full strength, can terminate not only the CS action but also prevent further increases in fear. Responses performed in later parts of the CS-US interval, when the fear state is fully developed, cannot avoid fear but only terminate it. Thus, the difference between short- and long-latency avoidance responses with respect to the secondary reinforcing properties of CS termination are analogous to those which exist between avoidance and escape responses with respect to the primary reinforcing properties of omission and termination of the painful US. Accordingly, an instrumental response performed at the beginning of the CS.-US interval may be considered as avoidance of pain and avoidance of conditioned fear responses, whereas any emitted with longer latency may be considered as avoidance of pain and escape from conditioned fear state. It has been shown recently that short-latency responses were acquired in later stages of training only after the long-latency responses had been performed on nearly 50~ of trials [14, 39, 44]. The present experiment demonstrated that short-latency responses were not acquired under the procedure in which the avoidance response was ineffective in termination of the fear-evoking CS. There are two possible mechanisms responsible for this outcome. Either the shortlatency avoidance responses were not acquired because the CS of long duration precluded avoidance of fear, or the short-latency responses deteriorate because they were punished by the prolongation of the fear-evoking CS. Since cats trained with a CS that had a minimal duration equal to the CS-US interval did not perform responses with latencies shorter than 1 sec in any stage of training,
392 it may be inferred that the secondary reinforcing effect of CS termination is necessary for acquisition of short-latency responses. In this respect the present experiment is more conclusive than the previous one performed on dogs trained under a partial reinforcement procedure for avoidance [45]. After initial training with both CS termination and US omission contingent upon the instrumental response, the procedure was changed so that on 50% of ~ a l s there was a fixed CS duration and no shock. Between-group comparisons revealed that this change hampered further shortening of response latencies, and the two groups of dogs maintained a difference in speed of responding during all further stages of training and testing. Since the partial reinforcement procedure was introduced after the clogs had reached a criterion of 80~ avoidance and shock trials were therefore infrequent, the between-group differences were considered to be related to the delay of CS-termination and not to the reduction in shock availability. In the dog experiment probably the lack of both the reinforcing effect of CS termination and the punishing effect of CS prolongation were responsible for long-latency responding of the dogs subjected to the partial reinforcement procedure. The term 'avoidance of fear' given to short-latency responses is not precise. In fact, all avoidance responses are performed on a background of fear conditioned not only to the discriminative CS but also to the whole experimental situation. The CS used in avoidance training serves different functions. It signals the painful US which has to be either avoided or escaped, it elicits a complex of autonomic changes which are considered as indices of fear, and it also adds an increment to the background level of fear conditioned to the experimental situation. This last function of the CS, i.e. its non-specific arousing effect, is independent of the signalling property of the CS and increases the frequency of responses that are conditioned to the experimental situation [13]. The direct relation between the CS intensity and the proportion of avoidance responses executed with short latencies has been shown both in cats [14, 44, 46, 47] and in dogs [22-24]. Exceptionally low levels of short-latency avoidance responses were observed with CSi consisting of a decrease in the background noise intensity [44]. When such stimuli were used, the proportion of avoidance responses emitted with latencies shorter than I sec was lower than expected from the probability of intertrial responses for this period of time. Thus, depending on the intensity relations between the CS and the background noise level, CS onset either increases or decreases the level of fear conditioned to the experimental situation and influences the proportion of short-latency avoidance responses which are considered as driven by the non-specific arousing effect of the CS onset [14]. Intertrial responding may be considered as an index of fear conditioned to the whole experimental situation. Data presented in this paper indicate that ITRs were more frequently performed after escape than after avoidance trials.
393 After avoidance trials the frequency of ITRs was higher in Group 2, in which the CS was not terminated by the avoidance response, than in Group 1, in which termination of the CS was response contingent on all trials. In spite of a higher level of fear conditioned to the experimental situation the CS onset in Group 2 did not elicit short-latency avoidance responses at any stage of training and testing. This provides further support for the notion that termination of the CS by the avoidance response is a necessary condition for acquisition of shortlatency responses. The effects of prefrontal lesions presented in this paper are concordant with those previously reported [40-44]. The between-group comparison showed that the smaller thc proportion of short-latency responses performed before lesions the more was the cumulative distribution of response latencies affected by the prefrontal operations. In neither group did the frequency of shortlatency avoidance responses recover after post-operative retraining. Data from the acquisition and post-operative stages of the experiment seem to indicate a lower response strength when CS termination was not contingent upon the avoidance response. However, the avoidance responses acquired under that procedure were more resistant to extinction than in the other group. Abolition of shock and introduction of a fixed duration CS in the extinction sessions was a greater change in the experimental procedure for Group I than for Group 2. The more rapid weakening of avoidance responding in Group I was presumably due to the punishing effect of the CS persisting after the instrumental response. Additionally the level of fear conditioned to the experimental situation, as indicated by ITR rate, was higher in Group 2 than in Group 1. Results of the present experiment demonstrate a strong effect of CS termination on several indices of avoidance behavior. Response-contingent CS termination resulted in more efficient avoidance responding a:,d a lowered level of fear conditioned to the experimental situation. Collectively the data are consonant with the hypothesis that the biological role of short-latency avoidance responses is to avoid fear conditioned to the discriminative CS. ACKNOWLEDGEMENTS
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