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Effect of septal lesions on response to frustrative nonreward
Physiology and Behavior, Vol. 8, pp. 909-913, Brain Research Publications Inc., 1972. Printed in Great Britain.
Effect of Septal Lesions on Response to Frustrative Nonreward' P A U L D. M A B R Y s A N D D U D L E Y F. P E E L E R
University of Mississippi Medical Center, Jackson, Mississippi 39216, U.S.A. (Received 22 N o v e m b e r 1971)
MABRY,P. D. AND D. F. PEELER. Effect of septal lesions on response to frta'trative nonreward. PHYSIOL.BEHAV. 8 (5) 909-913, 1972.--Male albino rats, septal-lesioned and control, were subjected to frustrative nonreward in the Amsel double runway. Results revealed that the magnitude of the frustration effect with both running and starting speed measures was not affected by septal lesions. This finding was interpreted as supporting McCleary's inhibitory-deficit hypothesis of septal lesion effects. Septum
Frustration
Inhibition
Rat
Runway
FINDINGS of studies concerned with septal function generally point to an inhibitory role for the septum in the organization of brain function. Electrical stimulation in the subcallosalseptal area has been shown to produce inhibition of ongoing responses [9]. Destruction of the septum, on the other hand, markedly weakens response inhibition. For instance, passive avoidance responding is significantly impaired by septal ablation [12, 14]. Similarly, conditioned emotional response, with the lever pressing measure, is attenuated following septal lesions [3, 8], and discriminated instrumental punishment is less effective in suppressing responding [8]. Other types of measures requiring inhibitory capacity are also influenced by septal ablation. Resistance to extinction of an instrumental response reinforced with food or water is significantly increased [4, 15], and response to the negative stimulus in performance of a preoperatively learned discrimination is significantly elevated [15]. In addition, septal lesions produce decreased efficiency on D R L reinforcement schedules [7] and on fixed interval schedules [6]. The perseveration of septal animals subsequent to withdrawal of reward [4, 6, 7, 15] deserves special attention. Amsel [1] has proposed a conditioned frustration hypothesis to explain the inhibition of learned responses that follows retraction of positive reinforcement. Given Amsel's formulation, septal lesions might increase resistance to extinction by reducing the frustration elicited by nonreward. McCleary [13], on the other hand, has maintained that septal lesions interfere with a general capacity for response inhibition, as reflected in a range of problems. Simply stated, the septal extinction effect could result from either a change in some property of the inhibitory, conditioned-frustration stimulus (st) or a change in the effectiveness of that stimulus in controlling behavior. The present investigation seeks to enhance interpretation of septal lesion effects by determining the influence
of the septum on the frustration reaction. Specifically, it examines the response of septal-lesioned rats to frustrative nonreward in the Amsel [2] double runway. METHOD
Animals Sixteen experimentally naive, male albino rats of the Wistar strain were employed. They were adult animals between 150 and 200 days of age at the time of testing. All were housed individually with free access to food and water until the beginning of experimental adaptation. Assignment of animals to lesion and control groups (n = 8 each) was at random.
Surgery and Histology The rats were anesthetized with sodium pentobarbital (40 mg/kg) supplemented by atropine sulphate (0.5 mg/kg). They were then placed in a Kopf stereotaxic instrument with the tooth bar set at a position 5 mm above the interaural plane. Holes were drilled in the skull at a point 2 mm anterior to bregrna and 0.75 mm lateral to the midline, and a stainlesssteel electrode (0.5 mm in dia.) was lowered into the septum, 6 mm below the dura. Bilateral lesions were produced electrolyticaUy by passing a 2 mA anodal current through the uninsulated, 0.5 mm tip of the electrode for 20 sec. The sham-operated control animals received the same treatment, except that no lesions were made. Every animal was allowed at least 30 days for postoperative recovery. At the conclusion of experimental testing, the rats were deeply anesthetized and then perfused with physiological saline followed by 10% formalin. After the brains had been removed and allowed to fix in a formalin solution, they were sliced into 75 t~ sections by the frozen tissue technique. The
IThis research was supported by PHS Training Grant No. NB-05411. SPresent address: Department of Psychology, Princeton University, Princeton, New Jersey 08540. 909
910
sections were then stained with cresyl violet tbr microscopic verification of lesion locus.
.4pparatus The testing compartment was a two-stage runway composed of five components arranged in the following order: start box, Runway 1, Goal Box 1, Runway 2, and Goal Box 2. All portions of the apparatus, with the exception of Goal Box 2, were 7.5 cm wide with 12 cm high walls. The first four components had the following lengths: start box, 22.5 cm; Runway 1, 105 cm; Goal Box 1, 30 cm; and Runway 2, 300 cm. Goal Box 2 measured 20 × 25 × 30 cm. Exit doors from the start box and Goal Box 1 and entrance doors to Goal Box 1 and Goal Box 2 were of the guillotine type and operable only by the experimenter through a pulley system. The entire apparatus was constructed from plywood and painted neutral gray, except for the interior of Goal Box 2 which was painted fiat black. Food was provided in a metal cup in Goal Box 2, while an indenture in the floor served as food trough in Goal Box 1. Starting and running speeds were measured in Runway 2 with photocell circuits. One photocell was stationed 60 cm beyond Goal Box 1 and another, 60 cm in front of the entrance to Goal Box 2. In addition, a photocell was positioned over the exit door of Goal Box 1. Starting speed was measured by an electric timer wired to start when the photocell on the door of Goal Box 1 was activated by opening of the door and stop when the first photocell in Runway 2 was activated. Running speed was docked from the time between activation of the two runway photocells. A second electric timer recorded this interval.
Procedure Before formal training began, both lesioned and shamoperated animals underwent 14 days of adaptation to the experimental environment. The first two days were allotted for initial adjustment to the 22-hr food deprivation schedule used in training and testing. From this point on, the rats received only enough food to maintain them at 8 0 ~ body weight. (Water was continuously available in the home cage.) The next 10 days were spent in adapting the animals to handling by the experimenter. Each rat was handled for 10 min each day during this period. The last 2 days of adaptation (Days 13 and 14) were spent in the experimental apparatus. The animals were given 15 min daily (30 min total for the 2 days) to explore the entire two-stage assembly. During training, each animal was run three times a day in the experimental apparatus with 30 min between each trial. The 22-hr food deprivation schedule was still in effect, and food was available in both goal boxes. For each trial, the rat was placed in the start box. Three sec later, the exit door was raised; the rat traversed Runway 1, entered Goal Box 1, and ate the food pellet. Thirty sec after entry into Goal Box 1, the exit door was opened; the rat negotiated Runway 2, entered Goal Box 2, and consumed another food pellet. At the completion of this experimental Sexluence, the animal was returned to its home cage until time for the next trial. The entire training period lasted 15 days (45 trials). Performance had stabilized for each group at the end of this period. The experimental test was conducted during the last 12 days of the experiment. The animals were again run three times a day (36 trials total) under 22-hr food deprivation. The procedure in this phase of the experiment differed from
MABRY A N D PkI-~Lt~R
that of the training phase in one respect. During testing, half of the trials (18) were reward trials and half were frustration trials. On reward trials, food was available in both goal boxes, as in training. On frustration trials, however, food was omitted from Goal Box 1, and the rat was confined there for 10 sec before being allowed to continue on to Goal Box 2. Reward trials and frustration trials were programmed in the following sequence to control for any effects of order of presentation: F R F RFR F F R R R F FRR RFF FRF RFR F F R R R F F R R RFF. Starting and running speed measures were taken on each trial. A between-subject comparison was made to determine the effect of septal lesions. For the test of frustrative nonreward, each animal served as his own control. As a check for differences within the 12 day test period, successive trial blocks (12 trials per block) were formed, with each block containing 6 reward and 6 frustration trials
RESULJS
Histology General findings of the histological examination revealed that the septum was either damaged or completely destroyed in every lesioned animal. The lateral septal nucleus was interrupted or destroyed bilaterally in each of the 20 preparations, whereas, the medial septal nucleus received damage in 19 of the 20 preparations. A reconstruction of representative lesions is shown in Fig. 1. A number of other structures adjacent to the septum were also damaged minimally and inadvertently by the lesioning process. Those most often affected were: the anterior hippocampal continuation, the corpus callosum, the medial parolfactorial area, and the fornix.
Affective Behavior All lesioned animals displayed the characteristic hyperirritability that follows septal damage. After prolonged recovery and adaptation, however, the animals became quite docile and remained so throughout the course of the experiment. Introduction of frustrative nonreward did not disinhibit the rage reaction.
Running Speed Frustration is measured in the double runway as an increased starting speed from Goal Box 1 and an increase in running speed in Runway 2 on those trials in which reinforcement is omitted from Goal Box I. Table I presents mean running speeds under the various experimental conditions. An analysis of variance on blocked data revealed no significant differences between trial blocks, The data in Table 1 are therefore collapsed across the entire test period. As expected, a rather large overall frustration effect was obtained with running scores ( F = 105,00; dr--1, 14; p <0.01). The absence of an interaction between brain damage and reinforcement conditions ( F ~ 2 . 0 0 ; d f = 1, 14; p >0.05) indicates, however, that septal animals were just as frustrated by nonreinforcement as their sham-operated controls. An additional finding was that septal lesions produced a decrease in running speed in Runway 2 regardless of reinforcement conditions (F~-- 9.09; d f = 1, 14; p<0.01). An analysis of running speed during the training phase revealed a similar decrement (F = 5.25; df~- 1, 14; p<0.05):
SEPTAL LESIONS AND FRUSTRATION
911
14
18
19
2d
A
B i
i
FIG. 1. Reconstruction of septal lesions showing the extent of the largest (A) and smallest (B) lesions. (Plates are from the Ktinig and Klippel [10] Atlas.)
912
MABRY AND PEEkkR TABLE 1 MEAN RUNNING SPEEDS (I/sEC) IN RUNWAY 2
Treatment
Reward
Frustration
(Combined)
Septal
0.237530
0.311526
0.274528
Unlesioned
0.320513
0.429185
0.374849
(Combined)
0.279022
0.370356
Starting Speed The speed with which animals left Goal Box 1 was also differentially affected by reinforcement conditions. When food was omitted from Goal Box 1, the rats started significantly faster than on reward trials (F--~ 16.93; df~-- 1, 14; p < 0.01). Furthermore, the presence of septal lesions did not significantly alter this frustration effect (F .... 3.17; dJ '-~ 1, 14; p > 0.05). These data, collapsed across trial blocks, are shown in Table 2. (As before, there were no significant differences between blocks.) Although septal lesions produced an overall decrement in running speed, starting speed was not dampened. The starting speed of septal animals across all conditions did not differ significantly from that of sham-operated controls ( F ~ 1.98; d f ~ 1, 14;p > 0.05).
DISCUSSION
The results of the present experiment suggest that the frustration reaction is not dependent on septal function. The finding of a normal facilitatory effect of frustrative nonreward with septal animals indicates that the primary frustration reaction remains undisturbed. Furthermore, since conditioned frustration (rf) should not differ qualitatively from primary frustration, it is unlikely that the properties of conditioned frustration are altered by septal lesions. The failure to demonstrate an alteration in frustration suggests that the perseveration of septal animals following withdrawal of reward is not due to a change in the aversiveness of st. Lesioned rats responded to frustrative nonreward with as much vigor as did unlesioned controls. Instead, it appears that septal animals simply have a diminished ability to inhibit high probability responses, as hypothesized by McCleary [13]. The punishment afforded by sr after reward withdrawal in instrumental situations seems to be as impotent in suppressing responding as electric shock has proven to be. The present results are not in accord with those of Caplan [5] demonstrating an increase in frustration in the operant box after septal lesions. This state of affairs indicates that
there may be an interaction between the lesion effect and the runway measure. For instance, in the double runway, normal animals may be forced by the structure of the situation to make the experimental response [18], thus masking the perseveration of septal animals. On the other hand, the structure of the operant chamber provides many avenues of escape from the frustrating situation (e.g., exploration, grooming, etc.) which may lower the baseline provided by controls. Such a structural difference between the two situations would tend to accentuate any apparent frustration effect found in the operant box as compared with the runway. It should be noted that findings with septal animals with respect to frustration are quite similar to those involving hippocampal preparations. Hippocampals yield higher rates of lever pressing than controls when positive reinforcement is withdrawn in the operant chamber [17], but do not differ from controls in the double runway test [18]. Furthermore, hippocampal animals show the same selective decrement in runway performance that was found with septals [18]. These results underscore the relationship in function between septum and hippocampus, and bolster the notion that differences in response measures may account for the discrepancy in frustration data for septal animals. The finding that septal lesions produce slower running speeds, but not starting speeds, should be examined. Reduction in running speed as a function of septal lesions has also been reported in another study [19]. Wolfe et al. [19] found that septal rats ran more slowly, but consumed a greater amount of water reward than controls. Such results suggest that the slower running may not be due to a motivational deficit. Furthermore, the fact that animals in the present experiment ran more slowly but started just as quickly as controls discourages a motivational explanation. It is possible that septal lesions precipitate some sort of motor interference or deficit. For instance, animals in the present study displayed a heightened tendency to jump (startle) in response to any unexpected stimulus change. Similar findings have been reported by others [11, 16]. Such a disposition might produce response tendencies that are antagonistic to running but not to starting speed in the runway.
TABLE 2 MEANSTARTINGSPEEDS(I/sEC) EROM GoALBox1
Treatment
Reward
Frustration
(Combined)
Septal
0.342466
0.621118
0.481792
Unlesioned
0.400000
0.649351
0.524676
(Combined)
0.371233
0.635235
SEPTAL LESIONS A N D F R U S T R A T I O N
913 REFERENCES
1. Amsel, A. The role of frustrative nonreward in non-continuous reward situations. Psychol. Bull. 55: 102-119, 1958. 2. Amsel, A. and J. Roussel. Motivational properties of frustration: I. Effect on a running response of the addition of frustration to the motivational complex. J. exp. Psychol. 43: 363-368, 1952. 3. Brady, J. V. and W. J. H. Nauta. Subcortical mechanisms in emotional behavior: The duration of affective changes following septal and habenular lesions in the albino rat. J. comp. physiol. Psychol. 48: 412-420, 1955. 4. Butters, N. and H. E. Rosvold. Effect of septal lesions on resistance to extinction and delayed alternation in monkeys. J. comp. physiol. Psychol. 66: 389-395, 1968. 5. Caplan, M. Effects of withheld reinforcement on timing behavior of rats with limbic lesions. J. comp. physiol. Psychol. 71: 119-135, 1970. 6. Ellen, P. and E. W. Powell. Temporal discrimination in rats with rhinencephalic lesions. Expl Neurol. 6: 538-547, 1962. 7. Ellen, P., A. S. Wilson, and E. W. Powell. Septal inhibition and timing behavior in the rat. Expl Neurol. 10: 120-132, 1964. 8. Harvey, J. A., C. E. Lints, L. E. Jacobson and H. F. Hunt. Effects of lesions in the septal area on conditioned fear and discriminated instrumental punishment. J. comp. physiol. Psychol. 59: 37-48, 1965. 9. Kaada, B. R. Somatomotor autonomic and electrocortigraphic responses to electrical stimulation of "rhinencephalic" and other structures in primates, cats, and dogs. Acta physiol. scand. 24: Suppl. 83, 1951. 10. K/Snig, J. F. R. and R. A. Klippel. The Rat Brahe. Baltimore: Williams & Wilkins, 1963.
11. Lints, C. E. and J. A. Harvey. Altered sensitivity to footshock and decreased brain content of serotonin following brain lesions in the rat. J. comp. physiol. Psychol. 67: 23-31, 1969. 12. McCleary, R. A. Response specificity in the behavioral effects of limbic system lesions in the cat. d. comp. physiol. Psychol. 54: 605-613, 1961. 13. McCleary, R. A. Response-modulating functions of the limbic system: Initiation and suppression. In: Progress in Physiological Psychology, edited by E. Stellar and J. M. Sprague. New York: Academic Press, 1966, pp. 210-266. 14. McNew, J. J. and R. Thompson. Role of the limbic system in active and passive avoidance conditioning in the rat. J. comp. physiol. Psychol. 61: 173-180, 1966. 15. Schwartzbaum, J. S., M. H. Kellicutt, T. M. Spieth and J. B. Thompson. Effects of septal lesions in rats on response inhibition associated with food reinforced behavior. J. comp. physiol. Psychol. 58: 217-224, 1964. 16. Seggie, J. Effect of somatosensory stimulation on affective behavior of septal rats. J. comp. physiol. Psychol. 66: 820--822, 1968. 17. Swanson, A. M. and R. Isaacson. Hippocampal ablation and performance during withdrawal of reinforcement. J. comp. physiol. Psychol. 64: 30-35, 1967. 18. Swanson, A. M. and R. L. Isaacson. Hippocampal lesions and the frustration effect in rats. J. comp. physiol. Psychol. 68"562-567, 1969. 19. Wolfe, J. W., J. F. Lubar and J. R. Ison. Effects of medial cortical lesions on appetitive instrumental conditioning. Physiol. Behav. 2: 239-244, 1967.
Effect of Septal Lesions on Response to Frustrative Nonreward' P A U L D. M A B R Y s A N D D U D L E Y F. P E E L E R
University of Mississippi Medical Center, Jackson, Mississippi 39216, U.S.A. (Received 22 N o v e m b e r 1971)
MABRY,P. D. AND D. F. PEELER. Effect of septal lesions on response to frta'trative nonreward. PHYSIOL.BEHAV. 8 (5) 909-913, 1972.--Male albino rats, septal-lesioned and control, were subjected to frustrative nonreward in the Amsel double runway. Results revealed that the magnitude of the frustration effect with both running and starting speed measures was not affected by septal lesions. This finding was interpreted as supporting McCleary's inhibitory-deficit hypothesis of septal lesion effects. Septum
Frustration
Inhibition
Rat
Runway
FINDINGS of studies concerned with septal function generally point to an inhibitory role for the septum in the organization of brain function. Electrical stimulation in the subcallosalseptal area has been shown to produce inhibition of ongoing responses [9]. Destruction of the septum, on the other hand, markedly weakens response inhibition. For instance, passive avoidance responding is significantly impaired by septal ablation [12, 14]. Similarly, conditioned emotional response, with the lever pressing measure, is attenuated following septal lesions [3, 8], and discriminated instrumental punishment is less effective in suppressing responding [8]. Other types of measures requiring inhibitory capacity are also influenced by septal ablation. Resistance to extinction of an instrumental response reinforced with food or water is significantly increased [4, 15], and response to the negative stimulus in performance of a preoperatively learned discrimination is significantly elevated [15]. In addition, septal lesions produce decreased efficiency on D R L reinforcement schedules [7] and on fixed interval schedules [6]. The perseveration of septal animals subsequent to withdrawal of reward [4, 6, 7, 15] deserves special attention. Amsel [1] has proposed a conditioned frustration hypothesis to explain the inhibition of learned responses that follows retraction of positive reinforcement. Given Amsel's formulation, septal lesions might increase resistance to extinction by reducing the frustration elicited by nonreward. McCleary [13], on the other hand, has maintained that septal lesions interfere with a general capacity for response inhibition, as reflected in a range of problems. Simply stated, the septal extinction effect could result from either a change in some property of the inhibitory, conditioned-frustration stimulus (st) or a change in the effectiveness of that stimulus in controlling behavior. The present investigation seeks to enhance interpretation of septal lesion effects by determining the influence
of the septum on the frustration reaction. Specifically, it examines the response of septal-lesioned rats to frustrative nonreward in the Amsel [2] double runway. METHOD
Animals Sixteen experimentally naive, male albino rats of the Wistar strain were employed. They were adult animals between 150 and 200 days of age at the time of testing. All were housed individually with free access to food and water until the beginning of experimental adaptation. Assignment of animals to lesion and control groups (n = 8 each) was at random.
Surgery and Histology The rats were anesthetized with sodium pentobarbital (40 mg/kg) supplemented by atropine sulphate (0.5 mg/kg). They were then placed in a Kopf stereotaxic instrument with the tooth bar set at a position 5 mm above the interaural plane. Holes were drilled in the skull at a point 2 mm anterior to bregrna and 0.75 mm lateral to the midline, and a stainlesssteel electrode (0.5 mm in dia.) was lowered into the septum, 6 mm below the dura. Bilateral lesions were produced electrolyticaUy by passing a 2 mA anodal current through the uninsulated, 0.5 mm tip of the electrode for 20 sec. The sham-operated control animals received the same treatment, except that no lesions were made. Every animal was allowed at least 30 days for postoperative recovery. At the conclusion of experimental testing, the rats were deeply anesthetized and then perfused with physiological saline followed by 10% formalin. After the brains had been removed and allowed to fix in a formalin solution, they were sliced into 75 t~ sections by the frozen tissue technique. The
IThis research was supported by PHS Training Grant No. NB-05411. SPresent address: Department of Psychology, Princeton University, Princeton, New Jersey 08540. 909
910
sections were then stained with cresyl violet tbr microscopic verification of lesion locus.
.4pparatus The testing compartment was a two-stage runway composed of five components arranged in the following order: start box, Runway 1, Goal Box 1, Runway 2, and Goal Box 2. All portions of the apparatus, with the exception of Goal Box 2, were 7.5 cm wide with 12 cm high walls. The first four components had the following lengths: start box, 22.5 cm; Runway 1, 105 cm; Goal Box 1, 30 cm; and Runway 2, 300 cm. Goal Box 2 measured 20 × 25 × 30 cm. Exit doors from the start box and Goal Box 1 and entrance doors to Goal Box 1 and Goal Box 2 were of the guillotine type and operable only by the experimenter through a pulley system. The entire apparatus was constructed from plywood and painted neutral gray, except for the interior of Goal Box 2 which was painted fiat black. Food was provided in a metal cup in Goal Box 2, while an indenture in the floor served as food trough in Goal Box 1. Starting and running speeds were measured in Runway 2 with photocell circuits. One photocell was stationed 60 cm beyond Goal Box 1 and another, 60 cm in front of the entrance to Goal Box 2. In addition, a photocell was positioned over the exit door of Goal Box 1. Starting speed was measured by an electric timer wired to start when the photocell on the door of Goal Box 1 was activated by opening of the door and stop when the first photocell in Runway 2 was activated. Running speed was docked from the time between activation of the two runway photocells. A second electric timer recorded this interval.
Procedure Before formal training began, both lesioned and shamoperated animals underwent 14 days of adaptation to the experimental environment. The first two days were allotted for initial adjustment to the 22-hr food deprivation schedule used in training and testing. From this point on, the rats received only enough food to maintain them at 8 0 ~ body weight. (Water was continuously available in the home cage.) The next 10 days were spent in adapting the animals to handling by the experimenter. Each rat was handled for 10 min each day during this period. The last 2 days of adaptation (Days 13 and 14) were spent in the experimental apparatus. The animals were given 15 min daily (30 min total for the 2 days) to explore the entire two-stage assembly. During training, each animal was run three times a day in the experimental apparatus with 30 min between each trial. The 22-hr food deprivation schedule was still in effect, and food was available in both goal boxes. For each trial, the rat was placed in the start box. Three sec later, the exit door was raised; the rat traversed Runway 1, entered Goal Box 1, and ate the food pellet. Thirty sec after entry into Goal Box 1, the exit door was opened; the rat negotiated Runway 2, entered Goal Box 2, and consumed another food pellet. At the completion of this experimental Sexluence, the animal was returned to its home cage until time for the next trial. The entire training period lasted 15 days (45 trials). Performance had stabilized for each group at the end of this period. The experimental test was conducted during the last 12 days of the experiment. The animals were again run three times a day (36 trials total) under 22-hr food deprivation. The procedure in this phase of the experiment differed from
MABRY A N D PkI-~Lt~R
that of the training phase in one respect. During testing, half of the trials (18) were reward trials and half were frustration trials. On reward trials, food was available in both goal boxes, as in training. On frustration trials, however, food was omitted from Goal Box 1, and the rat was confined there for 10 sec before being allowed to continue on to Goal Box 2. Reward trials and frustration trials were programmed in the following sequence to control for any effects of order of presentation: F R F RFR F F R R R F FRR RFF FRF RFR F F R R R F F R R RFF. Starting and running speed measures were taken on each trial. A between-subject comparison was made to determine the effect of septal lesions. For the test of frustrative nonreward, each animal served as his own control. As a check for differences within the 12 day test period, successive trial blocks (12 trials per block) were formed, with each block containing 6 reward and 6 frustration trials
RESULJS
Histology General findings of the histological examination revealed that the septum was either damaged or completely destroyed in every lesioned animal. The lateral septal nucleus was interrupted or destroyed bilaterally in each of the 20 preparations, whereas, the medial septal nucleus received damage in 19 of the 20 preparations. A reconstruction of representative lesions is shown in Fig. 1. A number of other structures adjacent to the septum were also damaged minimally and inadvertently by the lesioning process. Those most often affected were: the anterior hippocampal continuation, the corpus callosum, the medial parolfactorial area, and the fornix.
Affective Behavior All lesioned animals displayed the characteristic hyperirritability that follows septal damage. After prolonged recovery and adaptation, however, the animals became quite docile and remained so throughout the course of the experiment. Introduction of frustrative nonreward did not disinhibit the rage reaction.
Running Speed Frustration is measured in the double runway as an increased starting speed from Goal Box 1 and an increase in running speed in Runway 2 on those trials in which reinforcement is omitted from Goal Box I. Table I presents mean running speeds under the various experimental conditions. An analysis of variance on blocked data revealed no significant differences between trial blocks, The data in Table 1 are therefore collapsed across the entire test period. As expected, a rather large overall frustration effect was obtained with running scores ( F = 105,00; dr--1, 14; p <0.01). The absence of an interaction between brain damage and reinforcement conditions ( F ~ 2 . 0 0 ; d f = 1, 14; p >0.05) indicates, however, that septal animals were just as frustrated by nonreinforcement as their sham-operated controls. An additional finding was that septal lesions produced a decrease in running speed in Runway 2 regardless of reinforcement conditions (F~-- 9.09; d f = 1, 14; p<0.01). An analysis of running speed during the training phase revealed a similar decrement (F = 5.25; df~- 1, 14; p<0.05):
SEPTAL LESIONS AND FRUSTRATION
911
14
18
19
2d
A
B i
i
FIG. 1. Reconstruction of septal lesions showing the extent of the largest (A) and smallest (B) lesions. (Plates are from the Ktinig and Klippel [10] Atlas.)
912
MABRY AND PEEkkR TABLE 1 MEAN RUNNING SPEEDS (I/sEC) IN RUNWAY 2
Treatment
Reward
Frustration
(Combined)
Septal
0.237530
0.311526
0.274528
Unlesioned
0.320513
0.429185
0.374849
(Combined)
0.279022
0.370356
Starting Speed The speed with which animals left Goal Box 1 was also differentially affected by reinforcement conditions. When food was omitted from Goal Box 1, the rats started significantly faster than on reward trials (F--~ 16.93; df~-- 1, 14; p < 0.01). Furthermore, the presence of septal lesions did not significantly alter this frustration effect (F .... 3.17; dJ '-~ 1, 14; p > 0.05). These data, collapsed across trial blocks, are shown in Table 2. (As before, there were no significant differences between blocks.) Although septal lesions produced an overall decrement in running speed, starting speed was not dampened. The starting speed of septal animals across all conditions did not differ significantly from that of sham-operated controls ( F ~ 1.98; d f ~ 1, 14;p > 0.05).
DISCUSSION
The results of the present experiment suggest that the frustration reaction is not dependent on septal function. The finding of a normal facilitatory effect of frustrative nonreward with septal animals indicates that the primary frustration reaction remains undisturbed. Furthermore, since conditioned frustration (rf) should not differ qualitatively from primary frustration, it is unlikely that the properties of conditioned frustration are altered by septal lesions. The failure to demonstrate an alteration in frustration suggests that the perseveration of septal animals following withdrawal of reward is not due to a change in the aversiveness of st. Lesioned rats responded to frustrative nonreward with as much vigor as did unlesioned controls. Instead, it appears that septal animals simply have a diminished ability to inhibit high probability responses, as hypothesized by McCleary [13]. The punishment afforded by sr after reward withdrawal in instrumental situations seems to be as impotent in suppressing responding as electric shock has proven to be. The present results are not in accord with those of Caplan [5] demonstrating an increase in frustration in the operant box after septal lesions. This state of affairs indicates that
there may be an interaction between the lesion effect and the runway measure. For instance, in the double runway, normal animals may be forced by the structure of the situation to make the experimental response [18], thus masking the perseveration of septal animals. On the other hand, the structure of the operant chamber provides many avenues of escape from the frustrating situation (e.g., exploration, grooming, etc.) which may lower the baseline provided by controls. Such a structural difference between the two situations would tend to accentuate any apparent frustration effect found in the operant box as compared with the runway. It should be noted that findings with septal animals with respect to frustration are quite similar to those involving hippocampal preparations. Hippocampals yield higher rates of lever pressing than controls when positive reinforcement is withdrawn in the operant chamber [17], but do not differ from controls in the double runway test [18]. Furthermore, hippocampal animals show the same selective decrement in runway performance that was found with septals [18]. These results underscore the relationship in function between septum and hippocampus, and bolster the notion that differences in response measures may account for the discrepancy in frustration data for septal animals. The finding that septal lesions produce slower running speeds, but not starting speeds, should be examined. Reduction in running speed as a function of septal lesions has also been reported in another study [19]. Wolfe et al. [19] found that septal rats ran more slowly, but consumed a greater amount of water reward than controls. Such results suggest that the slower running may not be due to a motivational deficit. Furthermore, the fact that animals in the present experiment ran more slowly but started just as quickly as controls discourages a motivational explanation. It is possible that septal lesions precipitate some sort of motor interference or deficit. For instance, animals in the present study displayed a heightened tendency to jump (startle) in response to any unexpected stimulus change. Similar findings have been reported by others [11, 16]. Such a disposition might produce response tendencies that are antagonistic to running but not to starting speed in the runway.
TABLE 2 MEANSTARTINGSPEEDS(I/sEC) EROM GoALBox1
Treatment
Reward
Frustration
(Combined)
Septal
0.342466
0.621118
0.481792
Unlesioned
0.400000
0.649351
0.524676
(Combined)
0.371233
0.635235
SEPTAL LESIONS A N D F R U S T R A T I O N
913 REFERENCES
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