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Effects of cortical ablations upon recovery from the septal syndrome in hooded rats
PhyMology and Behavior. Vol. 5, pp. 879-882. Pergamon Press, 1970. Printed in Great Britain
Effects of Cortical Ablations Upon Recovery from the Septal Syndrome in Hooded Rats' JAY D. GLASS A N D 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 19 February 1970)
GLASS,J. D. ANDG. J. THOMAS.Effects of corticalablations upon recoveryfrom the septalsyndrome in hoodedrats. PHYSIOL. BEHAV. g(8)879-882, 1970.--Thehyper-reactivity of the septal syndrome was produced in adult male Long-Evans rats by electrolytic lesions in the septal region. Various groups of the rats with septal lesions were handled postoperatively for either 5 or 18 days or left unhandled for 18 days. The operated control group was also not handled. Following these handling periods, the septal syndrome was found to have declined in both handled groups, and the animals were at normal reactivity levels. The unhandled group with septal lesions still displayed the syndrome. Neocortical ablations did not reinstate the syndrome in either handled group, nor did they change the reactivity level of the unhandled groups. The septal syndrome in another group of rats was reduced to normal levels by handling for 21 postoperative days. Spreading depression, induced by application of 25~o KCI to the neocortex, did not reinstate the septal syndrome. These results differ from and restrict the generality of previous findings. Recovery of function
Septalsyndrome
Cortical ablations
THE PROBLEMof discovering neural mechanisms mediating recovery of function following brain damage is a basic problem in brain research. The phenomenon of recovery from lesionproduced deficits clearly occurs in humans [5], and there are many instances of recovery of function in animals, yet very little is known of its mechanisms. In this study the role of neocortex in mediating recovery from the septal syndrome [2] was used to investigate the problem of the neuroanatomical factors in recovery. Cytawa and Teitelbaum [4] reported that elimination of cortical function by spreading depression reinstated the spontaneously ablated emotional syndrome which had been caused by previous septal lesions. Further evidence for the cortical control hypothesis was presented by Yutzey et al. [11 ] who showed that if rats were given simultaneous septal lesions and cortical ablations, the expected spontaneous recovery from the septal syndrome did not occur. If cortical ablations could be shown to reinstate the septal syndrome in a "calmed" rat with septal lesions, it was felt that this demonstration would represent additional support for a theory of cortical mediation of recovery. The cortical ablations that we produced had no effect, so we repeated the essential features of the study by Cytawa and Teitelbaum [4]. METHOD
Subjects Thirty-two male hooded, Long-Evans rats, weighing 300400 g at the beginning of the study, were used in the experiments. They were obtained from a local animal dealer, and
this stock could be characterized as more nervous than the usual laboratory rat. The rats were housed individually and received food and water ad lib throughout the experiment.
Operations Fifteen rnin prior to the induction of anesthesia all animals received 1.6 mg of atropine sulfate i.p. to reduce secretions in airways. Anesthesia was induced by sodium pentobarbital supplemented with chloral hydrate given i.p. according to procedures proposed by Valenstein [10]. Following surgery 40,000 units of antibiotic (DistryciUin, Squibb) were given intramuscularly. Septal lesion. After being placed in the stereotaxic instrument, the head was leveled by adjusting bregma and lambda to equal height. Electrolytic lesions were produced by passing 2.0 mA anodal current for 20 sec through the uninsulated tip of a stereotaxically guided stainless-steel electrode. Bilateral lesions were produced at a depth of 5.4 mm below the skull by inserting the electrode through two small holes located 0.8 mm anterior to bregma and 0.5 mm on either side of the midline. The operated control groups underwent identical surgical procedures without inserting the electrode into the brain. Cortical ablation. Using clean technique, the neocortex was exposed by removal of the dorsal part of the skull while the rats were anesthetized as described above. The ablations were performed by the combined techniques of aspiration through a finely drawn glass tip, and by scraping a piece of a roll of dental cotton across the surface of the brain. Scraping off the pia mater and superficial blood vessels with compressed cotton to produce cortical ablations was suggested to
1This investigation was supported by grants MH 08034 and MH 13581. We are indebted to Jean A. Conlon for preparing the histological sections. 879
880 tts by Dr. Clinton N. Woolsey. Later examination of histological sections showed that the neocortex had degenerated completely under the scraped area. Typically, the dorsal surface of the cortex was ablated by scraping with dental cotton, and aspiration was used to extend the cortical lesions under the bone laterally and ventrally toward the rhinal fissure. Spreading depression. The rats were anesthetized as described above, and two 4-ram dia. holes were trephined through the skull approximately 3 mm from each side of the midline and 1 mm behind bregma, Two 1 cm long plastic tubes were placed over the two openings in the skull and held in place by two stainless-steel screws in the skull and acrylic plastic (Cranioplast). Each tube was filled with sterile physiological saline-soaked cotton which was resoaked every day during the course of the experiment. On the test day, the cotton was removed, two drops of 25% KCI were placed into each tube, and clean pieces of cotton were inserted.
Procedure All animals received 3 days of handling by the experimenter prior to surgery. Then the animals were divided into six groups roughly equated for reactivity to handling. Groups 5H, 18H, 18NH and 21H received septal lesions and two groups (C-AB and C-SD) received control operations. The N of each group is shown in Table 1 and Fig. 2. Three days following the production of septal lesions in the cortical ablation experiment, all groups were rated for reactivity. Then group 5H received 5 days of handling, group 18H received 18 days of handling, group 18NH was not handled for 18 days, and the control group (C-AB) was left unhandled. After the appropriate handling period, all groups received bilateral cortical ablations. Five days were allowed for recovery from the operation, and then the animals were rated for the septal syndrome. In the spreading depression experiment, 3 days following the septal operation all animals were rated, then groups 21H and C-SD received 21 days of handling. After the 21-day period KC1 was applied to the cortex of both groups and the animals were rated every 10 min for the first 2 hr and every 20 min during the third hour following the application of the KC1. In order to determine if the application of KCI did institute spreading depression, 30 min after the KCI was applied the rats were tested for front-leg placing reactions, and they were also placed on a grid to determine if their feet would dangle through the grid bars. Loss of placing and failure to support themselves with their feet on top of the grid bars were taken as positive signs that the KCI had produced spreading depression [1 ]. The handling procedure involved placing the animal in a large cardboard box once a day for a period of 3 min during which it was stroked with a gloved hand, and attempts were made to grasp and pick up the animal. The reactivity ratings were made on a 4-point scale applied to each of three reactions. The scale was 0, no reaction through 3, a violent reaction. Each animal's daily score was the sum of its rating scores on three reaction tests: touching the face with a stick, tapping the rump with a stick, and picking up the rat with the gloved hand. Reliability of ratings was checked by independent ratings of two experimenters on several occasions. It was found that the two experimenters rated the animals almost identically, so the presented emotionality scores are the sums of the ratings by one experimenter. The procedure is a modification of that.*described by Thomas et al. [9].
GLASS ANt) 1ttOIMAb Histoh~gy After the final rating period the animals were anesthetized with an overdose of sodium pentobarbital and perfused through the heart with 0.9% saline followed by 100.,, formalin. The brains were removed from the skulls and placed in 10% formalin for further fixation for several days. They were then embedded in celloidin, and 48-!z thick frontal sections were cut. Every third section was saved, stained with cresyl violet, and mounted. RESULq'S
Anatomical Microscopic examination of the histological sections showed large septal lesions which ablated most of the medial and lateral septal nuclei with moderate damage to the triangular nucleus and nucleus acumbens. Recent evidence (e.g. Hamilton et al. [6]) points towards a relationship of specific behavioral alterations with lesions restricted to specific regions or nuclei within the septal area. However, the septal syndrome of hyper-reactivity seems to be associated only with large lesions of the septal region. Our septal lesions were all large and no variations in them could be related to severity of the septal syndrome. The cortical lesions were also evaluated by microscopic examination. The largest and smallest lesions were reconstructed on Lashley diagrams and are shown in Fig. 1. Behavioral The results from the cortical ablation experiment are presented in Table 1. It may be seen by comparing the preseptal and postseptal columns that the septal lesions causeda significant (no overlap) increase in rated reactivity in all experimental groups. The operated control animals (C-AB) that did not receive septal lesions showed no significant change in reactivity. The handling given groups 5H and 18H produced a large decrease in reactivity level in all animals. The effect of handling is seen by the scores in the column labeled precortical ablation. There was no overlap in the scores of the handled and unhandled rats that had septat lesions. As may be seen from comparing the column labeled precortical ablation with the column labeled posteortical ablation, the subsequent cortical ablation did not reinstate the septal syndrome in either group. Reactivity level of group 18NH was not significantly affected by a period of 18 days with no handling. After the 18-day period, cortical ablation did not significantly alter the group's high reactivity level. The cortical ablations had no effect upon the reactivity level of the nonseptal and nonhandled control group. The results from the spreading depression experiment are presented in Fig. 2. The bar graphs on the left illustrate the effects of septal ablation on emotionatity ratings. As expected, the septal lesions caused a large increase in rated reactivity level in the experimental group, and the control operation had no significant effect upon reactivity level (no overlap). The 21 days of handling of the experimental group produced a marked decline in reactivity in all hyper-reactive rats. It is clear from the curves of average ratings shown in the righ t hand portion of Fig. 2 that following the 21-day handting period, the application of KCI to induce spreading depression did not reinstate the septal syndrome. The grid test and absence of the visual placing reaction showed that the KC! produced severe bilateral spreading depression within 30-45 min after application in all animals,
CORTICAL ABLATIONS A N D SEPTAL S Y N D R O M E RECOVERY
.~----~._.
I
---
881
---_
.__
-;".. .::; -
"-
il
-
~"-~'-~
~;"
-----I
ii !
--
!
-7-_
-
-
, I! q ---:I~:9-'.-"-."
FIG. 1. Schematic diagrams to illustrate the cortical lesions. The pictures on the left (A) show the largest lesions. Below are Lashley diagrams of the ablated cortex and above is a tracing of a frontal section to show the depth of the lesions. The diagrams on the right (B) similarly depict the smallest cortical lesions. Abbreviations: BP, basic peduncle; CC, corpus callosum; F, fornix; MTT, mammillo-thalamic tract; V, ventricle.
6'5 6'0
,~S'
[]
o Control N=5
[]
i
5'5 5'0
Septol N = 5
4'5 4"0 3'5 "t
.= 5 ~E
3"0 2"5 2'0 1"5 I'0 0'5 r/A
Pro op.
, . ~ ..
7ost op.
Post hand
o. ~,,~,-. -'-. -.=,~,,~,,.o/~ 0
.----.__.
20 40 60 80 I00 120 140 160 180 Post application of KCL, rain
FIG. 2. Mean reactivity ratings. The bar graphs on the left indicate the typical increase in reactivity produced by septal lesions and the subsequent decrease in emotionality occasioned by handling. On the right are graphs showing mean reactivity as a function of time after induction of spreading depression.
I--
832
~ILAS5 AND !tlONIA5 TABLE 1 MEAN REACTIVITY RATINGS FOR CORTICAL ABLATION EXPERIMENT
Group
N
Preseptal
Postseptal
Precortical Ablation
Postcortical Ablation 1.5 0.7 4.2 0.5
5H
7
0.1
5.4
0.1
18H
5
0
5.0
1.0
18NH C-AB
6 4
0 0
4.9 --
4.3 0.3
DISCUSSION
Neither cortical ablations nor spreading depression reinstated the septal syndrome of hyperemotionality that had been attenuated by daily handling. The results are, in part, contrary to the findings o f Cytawa and Teitelbaum [4]. They found that in a spontaneously recovered animal, the application of KCI to the cerebral cortex reinstated the behavioral syndrome produced by septal lesions. Also, contrary to previous findings [2, 4], our animals did not recover spontaneously. In order to determine the effect of cortical ablations, we had to handle our animals to lower their reactivity levels. It is possible that the septal syndrome returned after the cortical ablation but subsided during the 5.day postablation recovery period. However, that seems unlikely because of the persistence o f the syndrome in the stock of rats used in our experiment. It is also possible that the neocortical ablations produced by scraping the surface left normally functioning tissue at the time of behavioral testing and that only later did it degenerate to produce the complete absence of neocortical neurons in the ablated regions. However, it is not plausible to believe that the remaining cortical tissue in the ablated areas could function normally after the trauma of scraping of its superficial layers and depriving it of its blood supply. It seems likely that the septal area does not have the same function in all mammals (Carlson and Thomas [3]). Ablation
of the septal area (an easily homologized structure in the mammalian brain) does not result in homologous emotional alterations in different animals. Sodetz et aL [8] have described large differences between species with regard to effects of septal lesions on emotionality. Some species showed n o hyperreactivity following septal lesions. King [7] has shown a strong interaction between the natural temperament o f an animal and behavioral effects of septal lesions. The higher the preoperative emotional level of the animal, then the higher its emotional level is following a septal lesion. We have found in other experiments (unpublished) that the hooded rats we used are a very nervous and excitable stock. They adapt slowly to handling and to new environments. We do not find it surprising therefore that the septal syndrome in our hooded rats was extremely persistent. We hypothesize that the behavioral effects of septal lesions are related in part, to the species-typical temperamental characteristics of the animal, and, that within the L o n g Evans strain, stock differences in temperament in hooded rats account for the failure of our rats with septal lesions to decrease spontaneously over time in reactivity. Effects of removal of cortical control (either by partial ablation or spreading depression) on the septal syndrome may be specific to rats that spontaneously (without handling) decline in reactivity level after septal lesions.
REFERENCES 1. Albert, D. J. The effect of spreading depression on the consolidation of learning. Neuropsychologia 4: 49--64, 1966. 2. Brady, J. V. and W. H. Nauta. Subcortical mechanisms in emotional behavior: Affective changes following septal forebrain lesions in the albino rat. J. comp. physiol. Psychol. 46: 339-346, 1953. 3. Carlson, N. R. and G. J. Thomas. Maternal behavior of mice with limbic lesions. J. comp. physiol. Psychol. 66: 731-737, 1968. 4. Cytawa, J. and P. Teitelbaum. Spreading depression and recovery of subcortical functions. Acta Biol. exp. (Warsaw) 27: 343-353, 1967. 5. Denny-Brown, D. The nature of apraxia. J. herr. ment. Dis. 126: 9-32, 1958. 6. Hamilton, L. W., J. E. Kelsey and S. P. Grossman. Variations in behavioral inhibition following different septal lesions in rats. J. comp. physiol. Psychol. 70: 79-86, 1970.
7. King, F. A. Relationship of the "septal syndrome,' to genetic differences in emotionality in the rat. Psychol. Rep. 5: 11-17, 1959. 8. Sodetz, F. J., E. S. Matalka and B. N. Bunnell. Septal ablation and affective behavior in the Golden Hamster, Psyehonom. Sci. 7: 189-190, 1967. 9. 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. Psychot. 52: 527-532, 1959. 10. Valenstein, E. S. A note on anesthetizing rats and guinea pigs. J. exp. Analysis Behav. 4: 6, 1961. 11. Yutzey, D. A., D. R. Meyer and P. M, Meyer, Effects of simultaneous septal and nee- or limbic-cortical lesions upon emotionality in the rat. Brain Res. 5: 452-458, I967.
Effects of Cortical Ablations Upon Recovery from the Septal Syndrome in Hooded Rats' JAY D. GLASS A N D 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 19 February 1970)
GLASS,J. D. ANDG. J. THOMAS.Effects of corticalablations upon recoveryfrom the septalsyndrome in hoodedrats. PHYSIOL. BEHAV. g(8)879-882, 1970.--Thehyper-reactivity of the septal syndrome was produced in adult male Long-Evans rats by electrolytic lesions in the septal region. Various groups of the rats with septal lesions were handled postoperatively for either 5 or 18 days or left unhandled for 18 days. The operated control group was also not handled. Following these handling periods, the septal syndrome was found to have declined in both handled groups, and the animals were at normal reactivity levels. The unhandled group with septal lesions still displayed the syndrome. Neocortical ablations did not reinstate the syndrome in either handled group, nor did they change the reactivity level of the unhandled groups. The septal syndrome in another group of rats was reduced to normal levels by handling for 21 postoperative days. Spreading depression, induced by application of 25~o KCI to the neocortex, did not reinstate the septal syndrome. These results differ from and restrict the generality of previous findings. Recovery of function
Septalsyndrome
Cortical ablations
THE PROBLEMof discovering neural mechanisms mediating recovery of function following brain damage is a basic problem in brain research. The phenomenon of recovery from lesionproduced deficits clearly occurs in humans [5], and there are many instances of recovery of function in animals, yet very little is known of its mechanisms. In this study the role of neocortex in mediating recovery from the septal syndrome [2] was used to investigate the problem of the neuroanatomical factors in recovery. Cytawa and Teitelbaum [4] reported that elimination of cortical function by spreading depression reinstated the spontaneously ablated emotional syndrome which had been caused by previous septal lesions. Further evidence for the cortical control hypothesis was presented by Yutzey et al. [11 ] who showed that if rats were given simultaneous septal lesions and cortical ablations, the expected spontaneous recovery from the septal syndrome did not occur. If cortical ablations could be shown to reinstate the septal syndrome in a "calmed" rat with septal lesions, it was felt that this demonstration would represent additional support for a theory of cortical mediation of recovery. The cortical ablations that we produced had no effect, so we repeated the essential features of the study by Cytawa and Teitelbaum [4]. METHOD
Subjects Thirty-two male hooded, Long-Evans rats, weighing 300400 g at the beginning of the study, were used in the experiments. They were obtained from a local animal dealer, and
this stock could be characterized as more nervous than the usual laboratory rat. The rats were housed individually and received food and water ad lib throughout the experiment.
Operations Fifteen rnin prior to the induction of anesthesia all animals received 1.6 mg of atropine sulfate i.p. to reduce secretions in airways. Anesthesia was induced by sodium pentobarbital supplemented with chloral hydrate given i.p. according to procedures proposed by Valenstein [10]. Following surgery 40,000 units of antibiotic (DistryciUin, Squibb) were given intramuscularly. Septal lesion. After being placed in the stereotaxic instrument, the head was leveled by adjusting bregma and lambda to equal height. Electrolytic lesions were produced by passing 2.0 mA anodal current for 20 sec through the uninsulated tip of a stereotaxically guided stainless-steel electrode. Bilateral lesions were produced at a depth of 5.4 mm below the skull by inserting the electrode through two small holes located 0.8 mm anterior to bregma and 0.5 mm on either side of the midline. The operated control groups underwent identical surgical procedures without inserting the electrode into the brain. Cortical ablation. Using clean technique, the neocortex was exposed by removal of the dorsal part of the skull while the rats were anesthetized as described above. The ablations were performed by the combined techniques of aspiration through a finely drawn glass tip, and by scraping a piece of a roll of dental cotton across the surface of the brain. Scraping off the pia mater and superficial blood vessels with compressed cotton to produce cortical ablations was suggested to
1This investigation was supported by grants MH 08034 and MH 13581. We are indebted to Jean A. Conlon for preparing the histological sections. 879
880 tts by Dr. Clinton N. Woolsey. Later examination of histological sections showed that the neocortex had degenerated completely under the scraped area. Typically, the dorsal surface of the cortex was ablated by scraping with dental cotton, and aspiration was used to extend the cortical lesions under the bone laterally and ventrally toward the rhinal fissure. Spreading depression. The rats were anesthetized as described above, and two 4-ram dia. holes were trephined through the skull approximately 3 mm from each side of the midline and 1 mm behind bregma, Two 1 cm long plastic tubes were placed over the two openings in the skull and held in place by two stainless-steel screws in the skull and acrylic plastic (Cranioplast). Each tube was filled with sterile physiological saline-soaked cotton which was resoaked every day during the course of the experiment. On the test day, the cotton was removed, two drops of 25% KCI were placed into each tube, and clean pieces of cotton were inserted.
Procedure All animals received 3 days of handling by the experimenter prior to surgery. Then the animals were divided into six groups roughly equated for reactivity to handling. Groups 5H, 18H, 18NH and 21H received septal lesions and two groups (C-AB and C-SD) received control operations. The N of each group is shown in Table 1 and Fig. 2. Three days following the production of septal lesions in the cortical ablation experiment, all groups were rated for reactivity. Then group 5H received 5 days of handling, group 18H received 18 days of handling, group 18NH was not handled for 18 days, and the control group (C-AB) was left unhandled. After the appropriate handling period, all groups received bilateral cortical ablations. Five days were allowed for recovery from the operation, and then the animals were rated for the septal syndrome. In the spreading depression experiment, 3 days following the septal operation all animals were rated, then groups 21H and C-SD received 21 days of handling. After the 21-day period KC1 was applied to the cortex of both groups and the animals were rated every 10 min for the first 2 hr and every 20 min during the third hour following the application of the KC1. In order to determine if the application of KCI did institute spreading depression, 30 min after the KCI was applied the rats were tested for front-leg placing reactions, and they were also placed on a grid to determine if their feet would dangle through the grid bars. Loss of placing and failure to support themselves with their feet on top of the grid bars were taken as positive signs that the KCI had produced spreading depression [1 ]. The handling procedure involved placing the animal in a large cardboard box once a day for a period of 3 min during which it was stroked with a gloved hand, and attempts were made to grasp and pick up the animal. The reactivity ratings were made on a 4-point scale applied to each of three reactions. The scale was 0, no reaction through 3, a violent reaction. Each animal's daily score was the sum of its rating scores on three reaction tests: touching the face with a stick, tapping the rump with a stick, and picking up the rat with the gloved hand. Reliability of ratings was checked by independent ratings of two experimenters on several occasions. It was found that the two experimenters rated the animals almost identically, so the presented emotionality scores are the sums of the ratings by one experimenter. The procedure is a modification of that.*described by Thomas et al. [9].
GLASS ANt) 1ttOIMAb Histoh~gy After the final rating period the animals were anesthetized with an overdose of sodium pentobarbital and perfused through the heart with 0.9% saline followed by 100.,, formalin. The brains were removed from the skulls and placed in 10% formalin for further fixation for several days. They were then embedded in celloidin, and 48-!z thick frontal sections were cut. Every third section was saved, stained with cresyl violet, and mounted. RESULq'S
Anatomical Microscopic examination of the histological sections showed large septal lesions which ablated most of the medial and lateral septal nuclei with moderate damage to the triangular nucleus and nucleus acumbens. Recent evidence (e.g. Hamilton et al. [6]) points towards a relationship of specific behavioral alterations with lesions restricted to specific regions or nuclei within the septal area. However, the septal syndrome of hyper-reactivity seems to be associated only with large lesions of the septal region. Our septal lesions were all large and no variations in them could be related to severity of the septal syndrome. The cortical lesions were also evaluated by microscopic examination. The largest and smallest lesions were reconstructed on Lashley diagrams and are shown in Fig. 1. Behavioral The results from the cortical ablation experiment are presented in Table 1. It may be seen by comparing the preseptal and postseptal columns that the septal lesions causeda significant (no overlap) increase in rated reactivity in all experimental groups. The operated control animals (C-AB) that did not receive septal lesions showed no significant change in reactivity. The handling given groups 5H and 18H produced a large decrease in reactivity level in all animals. The effect of handling is seen by the scores in the column labeled precortical ablation. There was no overlap in the scores of the handled and unhandled rats that had septat lesions. As may be seen from comparing the column labeled precortical ablation with the column labeled posteortical ablation, the subsequent cortical ablation did not reinstate the septal syndrome in either group. Reactivity level of group 18NH was not significantly affected by a period of 18 days with no handling. After the 18-day period, cortical ablation did not significantly alter the group's high reactivity level. The cortical ablations had no effect upon the reactivity level of the nonseptal and nonhandled control group. The results from the spreading depression experiment are presented in Fig. 2. The bar graphs on the left illustrate the effects of septal ablation on emotionatity ratings. As expected, the septal lesions caused a large increase in rated reactivity level in the experimental group, and the control operation had no significant effect upon reactivity level (no overlap). The 21 days of handling of the experimental group produced a marked decline in reactivity in all hyper-reactive rats. It is clear from the curves of average ratings shown in the righ t hand portion of Fig. 2 that following the 21-day handting period, the application of KCI to induce spreading depression did not reinstate the septal syndrome. The grid test and absence of the visual placing reaction showed that the KC! produced severe bilateral spreading depression within 30-45 min after application in all animals,
CORTICAL ABLATIONS A N D SEPTAL S Y N D R O M E RECOVERY
.~----~._.
I
---
881
---_
.__
-;".. .::; -
"-
il
-
~"-~'-~
~;"
-----I
ii !
--
!
-7-_
-
-
, I! q ---:I~:9-'.-"-."
FIG. 1. Schematic diagrams to illustrate the cortical lesions. The pictures on the left (A) show the largest lesions. Below are Lashley diagrams of the ablated cortex and above is a tracing of a frontal section to show the depth of the lesions. The diagrams on the right (B) similarly depict the smallest cortical lesions. Abbreviations: BP, basic peduncle; CC, corpus callosum; F, fornix; MTT, mammillo-thalamic tract; V, ventricle.
6'5 6'0
,~S'
[]
o Control N=5
[]
i
5'5 5'0
Septol N = 5
4'5 4"0 3'5 "t
.= 5 ~E
3"0 2"5 2'0 1"5 I'0 0'5 r/A
Pro op.
, . ~ ..
7ost op.
Post hand
o. ~,,~,-. -'-. -.=,~,,~,,.o/~ 0
.----.__.
20 40 60 80 I00 120 140 160 180 Post application of KCL, rain
FIG. 2. Mean reactivity ratings. The bar graphs on the left indicate the typical increase in reactivity produced by septal lesions and the subsequent decrease in emotionality occasioned by handling. On the right are graphs showing mean reactivity as a function of time after induction of spreading depression.
I--
832
~ILAS5 AND !tlONIA5 TABLE 1 MEAN REACTIVITY RATINGS FOR CORTICAL ABLATION EXPERIMENT
Group
N
Preseptal
Postseptal
Precortical Ablation
Postcortical Ablation 1.5 0.7 4.2 0.5
5H
7
0.1
5.4
0.1
18H
5
0
5.0
1.0
18NH C-AB
6 4
0 0
4.9 --
4.3 0.3
DISCUSSION
Neither cortical ablations nor spreading depression reinstated the septal syndrome of hyperemotionality that had been attenuated by daily handling. The results are, in part, contrary to the findings o f Cytawa and Teitelbaum [4]. They found that in a spontaneously recovered animal, the application of KCI to the cerebral cortex reinstated the behavioral syndrome produced by septal lesions. Also, contrary to previous findings [2, 4], our animals did not recover spontaneously. In order to determine the effect of cortical ablations, we had to handle our animals to lower their reactivity levels. It is possible that the septal syndrome returned after the cortical ablation but subsided during the 5.day postablation recovery period. However, that seems unlikely because of the persistence o f the syndrome in the stock of rats used in our experiment. It is also possible that the neocortical ablations produced by scraping the surface left normally functioning tissue at the time of behavioral testing and that only later did it degenerate to produce the complete absence of neocortical neurons in the ablated regions. However, it is not plausible to believe that the remaining cortical tissue in the ablated areas could function normally after the trauma of scraping of its superficial layers and depriving it of its blood supply. It seems likely that the septal area does not have the same function in all mammals (Carlson and Thomas [3]). Ablation
of the septal area (an easily homologized structure in the mammalian brain) does not result in homologous emotional alterations in different animals. Sodetz et aL [8] have described large differences between species with regard to effects of septal lesions on emotionality. Some species showed n o hyperreactivity following septal lesions. King [7] has shown a strong interaction between the natural temperament o f an animal and behavioral effects of septal lesions. The higher the preoperative emotional level of the animal, then the higher its emotional level is following a septal lesion. We have found in other experiments (unpublished) that the hooded rats we used are a very nervous and excitable stock. They adapt slowly to handling and to new environments. We do not find it surprising therefore that the septal syndrome in our hooded rats was extremely persistent. We hypothesize that the behavioral effects of septal lesions are related in part, to the species-typical temperamental characteristics of the animal, and, that within the L o n g Evans strain, stock differences in temperament in hooded rats account for the failure of our rats with septal lesions to decrease spontaneously over time in reactivity. Effects of removal of cortical control (either by partial ablation or spreading depression) on the septal syndrome may be specific to rats that spontaneously (without handling) decline in reactivity level after septal lesions.
REFERENCES 1. Albert, D. J. The effect of spreading depression on the consolidation of learning. Neuropsychologia 4: 49--64, 1966. 2. Brady, J. V. and W. H. Nauta. Subcortical mechanisms in emotional behavior: Affective changes following septal forebrain lesions in the albino rat. J. comp. physiol. Psychol. 46: 339-346, 1953. 3. Carlson, N. R. and G. J. Thomas. Maternal behavior of mice with limbic lesions. J. comp. physiol. Psychol. 66: 731-737, 1968. 4. Cytawa, J. and P. Teitelbaum. Spreading depression and recovery of subcortical functions. Acta Biol. exp. (Warsaw) 27: 343-353, 1967. 5. Denny-Brown, D. The nature of apraxia. J. herr. ment. Dis. 126: 9-32, 1958. 6. Hamilton, L. W., J. E. Kelsey and S. P. Grossman. Variations in behavioral inhibition following different septal lesions in rats. J. comp. physiol. Psychol. 70: 79-86, 1970.
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