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Failure to reactivate the septal syndrome in rats
Physiology and Behavior, Vol. 6, pp. 599-601. P¢rsamon Prass, 1971. Printed in Great Britain
BRIEF COMMUNICATION Failure to Reactivate the Septal Syndrome in Rats I G E O F F R E Y R. H A M M O N D
Department of Psychology AND G A R T H J. T H O M A S
Center for Brain Research, University of Rochester, Rochester, New York, U.S.A. (Received 24 August 1970) HAMMOND,G. R. AND G. J. THOMAS. Failureto reactivate the septal syndrome in rats. PHYSIOL.BF.nAv. 6 (5) 599-601, 1971.--Electrolytic lesions in the septal region of albino rats produced the expected septal hyper-reactivity syndrome. Following abatement of the syndrome with daily handling, attempts were made to restore the hyper-reactivity with three techniques: abrupt reward decrement in an instrumental responding situation (frustration); exposure to both moderate and intense electric foot shock; and exposure to intense startle-eliciting tonal bursts. The treatments failed to elevate reactivity of the rats with septal lesions above control levels. Data from the instrumental responding situation provided support for the hypothesis of enhanced incentive properties of rewarding stimuli by septal lesions. Septal syndrome
Reactivity
Appetitive behavior
THE HYPEREMOTIONALITYdisplayed by laboratory rats following lesions in the septal region spontaneously abates with time and has been used as a model system for studying the role of neocortex in recovery of function [3]. The generality of the hypothesis about the role of the cortex in recovery of function is somewhat disputed by the evidence of Glass and Thomas [4], but there remains the clear implication that some stimuli (or their associated emotional states) that ordinarily play a role in regulating normal behavior, might bring about a resurgence of the syndrome. This study examined the effects on calmed rats with septal lesions of three treatments that seemed likely to induce a return of the syndrome; abrupt reward decrement following acquisition of an instrumental running response (frustration), exposure to emotion-arousing stimuli (footshock), and exposure to startle-eliciting acoustic stimuli. METHOD
Animals The animals were eight male albino rats (Holtzman) that weighed 445--480 g at the time of surgery and were housed individually throughout the experiment.
Surgery and Histology Large septal lesions were produced electrolytically and bilaterally by the passage of 3 mA anodal current through a
stereotaxically guided stainless-steel electrode in four rats. Four control rats underwent identical surgical procedures except the electrode was not lowered into the brain. Surgical procedures were identical (except for current level) to those described previously [4]. At the conclusion of the experiment frozen stained sections were made of three of the rat brains (one rat was lost to histology) to verify the lesions in the septal area.
Behavioral Procedures The animals were handled daily and also rated for reactivity on a series of tests employed by Thomas et al. [5]. The handling rapidly reduced the hyperemotionality of the septal syndrome. In the first phase of behavioral testing following abatement of the syndrome, all rats were placed on a 23-hr food deprivation regimen for 4 days, and then run in a straight runway (painted black and 239 cm long × 9 cm wide × l0 cm high) for a reward of fifteen 45-rag Noyes sucrose pellets. Intertrial intervals were about 5 rain. Following 42 acquisition trials (10 trials per day for 4 days except on Day 1 when two trials were given) reward magnitude was shifted down to one 45-mg pellet for all rats for a total of 18 shift trials. Reactivity was rated at the midpoint of the daily acquisition session, and subsequently, after each shift trial. Ratings were made while the animal was in the goal box immediately following consumption of the reward.
XThis investigation was supported by Grant No. MH 13581 from the National Institute of Mental Health and NSF Grant GB 14814. We thank James R. Ison for advice and the use of equipment during the course of the study and Jean A. Conlon for preparing the histological sections. 599
600
HAMMOND AND THOMAS
Following the completion of runway training all rats were successively exposed to moderate (0.3 mA, 10 sec) and then intense (1.0 mA, 10 sec) electric foot shock delivered in a Foringer shock chamber. Reactivity ratings were made while the animals were in the shock chamber before any shock was delivered and immediately following each of the two shock exposures, which were spaced 5 min apart. The rats were kept in a holding box during the 5-min interval. The startle treatment was administered 5 days after the shock treatment. It consisted of the delivery of 10 irregularly timed (average interval was 45 sec) tonal bursts of sufficient intensity (117 dB re 0.0002 dynes per cm 2) to elicit a startle response. For more detailed description of the equipment, see [2]. Again, the animals were rated for reactivity immediately following exposure to the tonal bursts.
17/102, p<0.001) as expected; however, post-shift group differences failed to reach statistical significance despite a tendency for the experimental rats to show less disruption of approach behavior (Fig. 2, curves on the righ0. The presumed frustration engendered by the downx~ard shift in reward magnitude clearly did not reinstate the septal syndrome.
4" • SEPTAL(N=4 ) © CONTROL(N=4) 3-
2-
RESULTS
As can be seen in the left part of Fig. 1, the animals with soptal lesions showed the expected increase in postoperative reactivity which declined over days, returning to control levels at about 2 weeks. A Mann-Whitney U test carried out on the sums of the ratings over Days 1-14 indicated a reliable difference betwean the experimental and control groups (p<0.05, two tailed). When the septal syndrome was at its height, there was no overlap in reactivity scores between experimental and control rats.
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i
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i
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23456789 INITIAL ACQUISITION (TRIALS)
SHIFT (BLOCKS)
FIG. 2. Mean speed of running as a function of trials. The left part of the figure shows the initial 10 acquisition trials. The right part of the figure shows response speeds following the reward shift (blocks of two trials on the abscissa). • [] SEPTAL(N=4)
5
0 ~ CONTROL(N=4)
_~ 3 ~-.
0
?~, ,o-o~,, ?~,~ ,'~:
Pie op.
I 2 3 4 5 6 13
POST-OR RATINGS
;~
jO0
Post shift
Pos~ Post Post shock shock startle (low) (high) TESTS
FIG. 1. Mean reactivity ratings. The graph on the left shows the expected enhanced reactivity in rats following septal lesions and the subsequent dvclin© of reactivity with handling. The bar graphs on the fight show mean reactivity ratings following the various behavioral manipulations.
Reward Decrement The results of the three manipulations that were used in an attempt to restore the syndrome following its abatement wore all without effect. The abrupt decrement in reward magnitude failed to elevate reactivity at all (right side of Fig. 1). Analysis of shift behavior in terms of running speeds showed a significant main effect of Trials (F = 5.95, d f =
The septal lesions did have a striking effect on runway performance during early trials of initial acquisition as can be seen in the left-hand portion of Fig. 2. An analysis of variance of total speed scores over the first 10 acquisition trials in the runway revealed reliable main effects of Groups (F = 52.14, df= 1/6, p < 0.001), Trials (F = 10.84, df= 9/54, p<0.001), and a reliable Groups × Trials interaction (F = 7.68, dr= 9/54, p<0.001). Inspection of the left part of Fig. 2 shows that whereas the control rats showed no appreciable improvement during the first few trials, the experimental rats demonstrated continuous trial-by-trial improvement beginning with the second trial in the runway. By the end of acquisition training, however, these group differences had disappeared with both experimental and control rats performing at a common asymptote (see first points on graph to the right, Fig. 2).
Exposure to Foot Shock While successive exposure to two shock intensities led to increasing reactivity in the experimental rats, tbese increases were not significantly different from those noted in the controls and cannot be taken as evidence of a selective reinstatement of the septal syndrome (see right side of Fig. 1).
Exposure to Startle-evoking Stimuli Again, as in the case of reward decrement and unescapable electric foot shock, no return of hyper-reactivity was detected (s¢¢ fight siti¢ of Fig. 1). The experimental rats showed normal
REACTIVATION OF SEPTAL SYNDROME
601
amplitudes of startle reactions, which also demonstrated that they did not have any significant hearing deficit. DISCUSSION
The results of the behavioral tests indicate clearly that frustration, painful stimulation, and intense startle-producing stimuli are not in themselves sufficient to reactivate the septal syndrome following its decline. These findings imply that the recovery of function evidenced by the decline of the syndrome represents a fairly stable behavioral change that is
not easily disrupted by emotion-provoking stimulation. The procedures used in this study failed to identify what events (if any) do have the capacity to induce a return of the hyper-responsiveness of the septal syndrome. The finding that the rats with septal lesions showed more rapid acquisition of the approach response during early training in the runway than the control rats is of interest. This superior initial-trials performance supports the hypothesis that septal lesions in rats act to exaggerate the incentive properties of positively rewarding stimuli [1] which, in this case, led to a more powerful incentive control of behavior.
REFERENCES 1. Beatty, W. W. and J. S. Schwartzbaum. Consummatory behavior for sucrose following septal lesions in the rat. J. comp. physiol. PsychoL 65: 93-102, 1968. 2. Buckland, G,, J. Buckland, C. Jamieson and J. R. Ison. Inhibition of startle response to acoustic stimulation produced by visual prestimulation. J. comp. physiol. PsychoL 67: 493-496, 1969. 3. Cytawa, J. and P. Teitelbaum. Spreading depression and recovery of subcortical functions. Acta Biol. exp. (Warsaw) 27: 343-353, 1967.
4. Glass, J. D. and G. J. Thomas. Effects of cortical ablations upon recovery from the septal syndrome in hooded rats. Physiol. Behav. 5: 879-882, 1970. 5. Thomas, G. J., R. Y. Moore, J. A. Harvey and H. F. Hunt. Relations between the behavioral syndrome produced by lesions in the septal region of the forebrain and maze learning in the rat. J. comp. physiol. Psychol. 52: 527-532, 1959.
BRIEF COMMUNICATION Failure to Reactivate the Septal Syndrome in Rats I G E O F F R E Y R. H A M M O N D
Department of Psychology AND G A R T H J. T H O M A S
Center for Brain Research, University of Rochester, Rochester, New York, U.S.A. (Received 24 August 1970) HAMMOND,G. R. AND G. J. THOMAS. Failureto reactivate the septal syndrome in rats. PHYSIOL.BF.nAv. 6 (5) 599-601, 1971.--Electrolytic lesions in the septal region of albino rats produced the expected septal hyper-reactivity syndrome. Following abatement of the syndrome with daily handling, attempts were made to restore the hyper-reactivity with three techniques: abrupt reward decrement in an instrumental responding situation (frustration); exposure to both moderate and intense electric foot shock; and exposure to intense startle-eliciting tonal bursts. The treatments failed to elevate reactivity of the rats with septal lesions above control levels. Data from the instrumental responding situation provided support for the hypothesis of enhanced incentive properties of rewarding stimuli by septal lesions. Septal syndrome
Reactivity
Appetitive behavior
THE HYPEREMOTIONALITYdisplayed by laboratory rats following lesions in the septal region spontaneously abates with time and has been used as a model system for studying the role of neocortex in recovery of function [3]. The generality of the hypothesis about the role of the cortex in recovery of function is somewhat disputed by the evidence of Glass and Thomas [4], but there remains the clear implication that some stimuli (or their associated emotional states) that ordinarily play a role in regulating normal behavior, might bring about a resurgence of the syndrome. This study examined the effects on calmed rats with septal lesions of three treatments that seemed likely to induce a return of the syndrome; abrupt reward decrement following acquisition of an instrumental running response (frustration), exposure to emotion-arousing stimuli (footshock), and exposure to startle-eliciting acoustic stimuli. METHOD
Animals The animals were eight male albino rats (Holtzman) that weighed 445--480 g at the time of surgery and were housed individually throughout the experiment.
Surgery and Histology Large septal lesions were produced electrolytically and bilaterally by the passage of 3 mA anodal current through a
stereotaxically guided stainless-steel electrode in four rats. Four control rats underwent identical surgical procedures except the electrode was not lowered into the brain. Surgical procedures were identical (except for current level) to those described previously [4]. At the conclusion of the experiment frozen stained sections were made of three of the rat brains (one rat was lost to histology) to verify the lesions in the septal area.
Behavioral Procedures The animals were handled daily and also rated for reactivity on a series of tests employed by Thomas et al. [5]. The handling rapidly reduced the hyperemotionality of the septal syndrome. In the first phase of behavioral testing following abatement of the syndrome, all rats were placed on a 23-hr food deprivation regimen for 4 days, and then run in a straight runway (painted black and 239 cm long × 9 cm wide × l0 cm high) for a reward of fifteen 45-rag Noyes sucrose pellets. Intertrial intervals were about 5 rain. Following 42 acquisition trials (10 trials per day for 4 days except on Day 1 when two trials were given) reward magnitude was shifted down to one 45-mg pellet for all rats for a total of 18 shift trials. Reactivity was rated at the midpoint of the daily acquisition session, and subsequently, after each shift trial. Ratings were made while the animal was in the goal box immediately following consumption of the reward.
XThis investigation was supported by Grant No. MH 13581 from the National Institute of Mental Health and NSF Grant GB 14814. We thank James R. Ison for advice and the use of equipment during the course of the study and Jean A. Conlon for preparing the histological sections. 599
600
HAMMOND AND THOMAS
Following the completion of runway training all rats were successively exposed to moderate (0.3 mA, 10 sec) and then intense (1.0 mA, 10 sec) electric foot shock delivered in a Foringer shock chamber. Reactivity ratings were made while the animals were in the shock chamber before any shock was delivered and immediately following each of the two shock exposures, which were spaced 5 min apart. The rats were kept in a holding box during the 5-min interval. The startle treatment was administered 5 days after the shock treatment. It consisted of the delivery of 10 irregularly timed (average interval was 45 sec) tonal bursts of sufficient intensity (117 dB re 0.0002 dynes per cm 2) to elicit a startle response. For more detailed description of the equipment, see [2]. Again, the animals were rated for reactivity immediately following exposure to the tonal bursts.
17/102, p<0.001) as expected; however, post-shift group differences failed to reach statistical significance despite a tendency for the experimental rats to show less disruption of approach behavior (Fig. 2, curves on the righ0. The presumed frustration engendered by the downx~ard shift in reward magnitude clearly did not reinstate the septal syndrome.
4" • SEPTAL(N=4 ) © CONTROL(N=4) 3-
2-
RESULTS
As can be seen in the left part of Fig. 1, the animals with soptal lesions showed the expected increase in postoperative reactivity which declined over days, returning to control levels at about 2 weeks. A Mann-Whitney U test carried out on the sums of the ratings over Days 1-14 indicated a reliable difference betwean the experimental and control groups (p<0.05, two tailed). When the septal syndrome was at its height, there was no overlap in reactivity scores between experimental and control rats.
J )
i
)
i
i
a
i
23456789 INITIAL ACQUISITION (TRIALS)
SHIFT (BLOCKS)
FIG. 2. Mean speed of running as a function of trials. The left part of the figure shows the initial 10 acquisition trials. The right part of the figure shows response speeds following the reward shift (blocks of two trials on the abscissa). • [] SEPTAL(N=4)
5
0 ~ CONTROL(N=4)
_~ 3 ~-.
0
?~, ,o-o~,, ?~,~ ,'~:
Pie op.
I 2 3 4 5 6 13
POST-OR RATINGS
;~
jO0
Post shift
Pos~ Post Post shock shock startle (low) (high) TESTS
FIG. 1. Mean reactivity ratings. The graph on the left shows the expected enhanced reactivity in rats following septal lesions and the subsequent dvclin© of reactivity with handling. The bar graphs on the fight show mean reactivity ratings following the various behavioral manipulations.
Reward Decrement The results of the three manipulations that were used in an attempt to restore the syndrome following its abatement wore all without effect. The abrupt decrement in reward magnitude failed to elevate reactivity at all (right side of Fig. 1). Analysis of shift behavior in terms of running speeds showed a significant main effect of Trials (F = 5.95, d f =
The septal lesions did have a striking effect on runway performance during early trials of initial acquisition as can be seen in the left-hand portion of Fig. 2. An analysis of variance of total speed scores over the first 10 acquisition trials in the runway revealed reliable main effects of Groups (F = 52.14, df= 1/6, p < 0.001), Trials (F = 10.84, df= 9/54, p<0.001), and a reliable Groups × Trials interaction (F = 7.68, dr= 9/54, p<0.001). Inspection of the left part of Fig. 2 shows that whereas the control rats showed no appreciable improvement during the first few trials, the experimental rats demonstrated continuous trial-by-trial improvement beginning with the second trial in the runway. By the end of acquisition training, however, these group differences had disappeared with both experimental and control rats performing at a common asymptote (see first points on graph to the right, Fig. 2).
Exposure to Foot Shock While successive exposure to two shock intensities led to increasing reactivity in the experimental rats, tbese increases were not significantly different from those noted in the controls and cannot be taken as evidence of a selective reinstatement of the septal syndrome (see right side of Fig. 1).
Exposure to Startle-evoking Stimuli Again, as in the case of reward decrement and unescapable electric foot shock, no return of hyper-reactivity was detected (s¢¢ fight siti¢ of Fig. 1). The experimental rats showed normal
REACTIVATION OF SEPTAL SYNDROME
601
amplitudes of startle reactions, which also demonstrated that they did not have any significant hearing deficit. DISCUSSION
The results of the behavioral tests indicate clearly that frustration, painful stimulation, and intense startle-producing stimuli are not in themselves sufficient to reactivate the septal syndrome following its decline. These findings imply that the recovery of function evidenced by the decline of the syndrome represents a fairly stable behavioral change that is
not easily disrupted by emotion-provoking stimulation. The procedures used in this study failed to identify what events (if any) do have the capacity to induce a return of the hyper-responsiveness of the septal syndrome. The finding that the rats with septal lesions showed more rapid acquisition of the approach response during early training in the runway than the control rats is of interest. This superior initial-trials performance supports the hypothesis that septal lesions in rats act to exaggerate the incentive properties of positively rewarding stimuli [1] which, in this case, led to a more powerful incentive control of behavior.
REFERENCES 1. Beatty, W. W. and J. S. Schwartzbaum. Consummatory behavior for sucrose following septal lesions in the rat. J. comp. physiol. PsychoL 65: 93-102, 1968. 2. Buckland, G,, J. Buckland, C. Jamieson and J. R. Ison. Inhibition of startle response to acoustic stimulation produced by visual prestimulation. J. comp. physiol. PsychoL 67: 493-496, 1969. 3. Cytawa, J. and P. Teitelbaum. Spreading depression and recovery of subcortical functions. Acta Biol. exp. (Warsaw) 27: 343-353, 1967.
4. Glass, J. D. and G. J. Thomas. Effects of cortical ablations upon recovery from the septal syndrome in hooded rats. Physiol. Behav. 5: 879-882, 1970. 5. Thomas, G. J., R. Y. Moore, J. A. Harvey and H. F. Hunt. Relations between the behavioral syndrome produced by lesions in the septal region of the forebrain and maze learning in the rat. J. comp. physiol. Psychol. 52: 527-532, 1959.