Physiology & Behavior, Vol. 17, pp. 181-186. Pergamon Press and Brain Research Publ., 1976. Printed in the U.S.A.
The Effect of Medial Thalamic Lesions on Emotionality, Activity, and Discrimination Learning in the Rat ANN E. WARING AND L A R R Y W. MEANS 2
East Carolina University, Greenville, N C 27834 (Received 8 September 1975)
WARING, A. E. AND L. W. MEANS. The effect o f medial thalamic lesions on emotionality, activity, and discrimination learning in the rat. PHYSIOL. BEHAV. 17(2) 181-186, 1976.- Three experiments were conducted to examine the effects of medial thalamic lesions on emotionality, open-field activity, and discrimination learning. The first study revealed that rats with large medial thalamie lesions are significantly less responsive to capture and to handling than are sham-operated rats. The second study failed to produce any significant differences in open-field activity. A third study revealed that rats with large medial thalamic lesions, and with both small anterior and posterior medial thalamic lesions are impaired on the acquisition of an appetitive visual-tactile discrimination task, with the deficit being greatest in the large lesion group. It was concluded that the medial thalamus plays a role in the neural mediation of certain emotional responses and is critical in the acquisition of complex appetitive tasks. Medial thalamus
Emotionality
Activity
Discrimination
CHANGES in emotionality, activity, and acquisition and retention have been observed to follow lesions of the dorsomedial nucleus of the thalamus (MD) in both humans and infrahuman species. Rats with MD lesions have been observed to be tamer than normal animals [12,21], to freeze less in novel exploration, and to display less emotionality, as evidenced by less defecation [10,21]. The animals, however, exhibit increased freezing in response to aversive stimuli, resulting in deficits in one-way [ 13, 18, 19] and two-way avoidance [1,13]. No deficits are noted in passive avoidance [7,18]. Inconsistent results in activity have been noted; increases have been noted in a bar press situation [8], in the open field [6], and in a nonaversive situation [ 18,20]. Decreases have been found in running wheel activity [5] and spontaneous activity [4]. Several studies have demonstrated no changes in maze exploration [5,12], cage activity [5], cage emergence, and closed field exploration [7]. Impairments in rats with MD lesions have been demonstrated on acquisition of visual discrimination [2,3], visual-tactile discrimination [ 12], visual discrimination reversal, tactile discrimination and reversal [16], and complex spatial discrimination [22]. The rats are also impaired on go, no-go alternation tasks [ 11 ] and go, no-go visual-auditory discrimination tasks [9].
The present study was designed to examine the effects of both large and small medial thalamic lesions on emotionality, activity, and acquisition of a visual-tactile discrimination task. Relatively large lesions were centered on the MD for one group, while small anterior or posterior medial thalamic lesions were produced in the other two groups. The small lesions were an attempt to destroy the anterior or posterior portions of tissue destroyed by the large lesions, and were included to permit a more precise determination of the medial thalamic structures necessary for normal behavior. G E N E R A L METHOD
Animals The same 39 male Long-Evans rats, approximately 110 days old at the time of surgery, were used in all 3 experiments. They were housed individually and maintained on a 14-hr-light, 10-hr-dark cycle. Water was continuously available.
Surgical and Histological Procedure Thirty-one rats received bilateral lesions of the medial thalamus, while 8 rats received sham-operations. The animals were anesthetized with 40 mg/kg pentobarbital
t This paper is based on an MA thesis submitted by AEW to East Carolina University. The authors wish to thank Larry Hayes and John Whisnant for their assistance and Karl Wuensch for his helpful comments. 2Requests for reprints should be sent to Larry W. Means, Department of Psychology, East Carolina University, Greenville, N. C. 27834. 181
182
(
WARING AND MEANS
.
) 1,
) FIG. 1. Reconstruction of the largest and smallest lesions of Group A (left column), Group P (center column), and Group C (right column). (Nembutal) and received 0.20 ml of Bicillin. Each animal was placed in the stereotaxic with the top of the incisor bar elevated 5.0 mm above the ear bar, and lesions were made by passing 2.0 rnA anodal current through a stainless steel electrode that was insulated with Epoxylite except for the tip. Ten of the rats received small bilateral lesions of the anterior medial thalamus (Group A). The lesions were made by passing current for 8 sec with the tip of the electrode placed at coordinates 0.6 mm behind bregma, 1.0 mm lateral to the midline, and 6.2 mm below the top surface of the skull. Eight rats received small bilateral lesions of the posterior medial thalamus (Group P). These lesions also were formed by passing current for 8 sec, with the coordinates being 1.8 mm behind bregma, 1.0 mm lateral to the midline, and 6.2 mm below the skull surface. Thirteen animals received large bilateral lesions of the medial thalamus (Group C). These animals had current passed for 15 sec with the coordinates being 1.2 mm behind bregma, 1.0 mm lateral to the midline, and 6.2 mm below the skull surface. Eight animals received sham-operations (Group S), which involved the same surgical procedure except the electrode was lowered only 5.0 mm below the surface of the skull and no current was applied. At the completion of the behavioral testing all rats were
sacrificed with an overdose of Nembutal, the animals were perfused with Formalin, and the brains were extracted and sectioned at 50 u while frozen. Every fourth section throughout the extent of the lesion was photographed using 35 mm Kodak High Contrast Copy Film. The extent of lesion damage was determined by projecting the negatives onto corresponding plates from Pellegrino and Cushman's [14] stereotaxic atlas. The lesions were traced onto copies of plates and a grid was used to determine the per cent damage to each structure. Figure 1 shows reconstructions of the largest and smallest lesions in each group. Group A lesions were centered on the anterior portion of the MD and destroyed bilaterally a mean of 38% of the MD. In most animals in Group A the lesions also invaded the midline nuclei, the anteroventral nucleus, the habenulointerpeduncular tract, and the stria medullaris. Group P lesions, which were on the posterior border of the MD, resulted in a mean bilateral destruction of the MD of only 6 per cent. Most of the animals in this group had extensive damage of the habenula and some damage to the pretectal area, parafascicular nucleus, paraventricular nucleus, and stria medullaris. The Group C lesions were centered on the MD and bilaterally destroyed a mean of 44 per cent of the MD. Lesions in this
MEDIAL THALAMUS AND BEHAVIOR
183
group also destroyed the midline nuclei and invaded the habenula, anterodorsal nucleus, pretectal area, and stria medullaris. Twelve animals received minimal bilateral damage to t h e hippocampus, averaging approximately 1.0 percent. Note, that as intended, there was considerable overlap of the small lesions of Groups A & P with the relatively large lesions of Group C.
Anterior
¢ "
:
Posterior
.~*
--"
Central
e---e
Sham
3.5
3.0
d
2.5
General Procedure 2.0
All animals were handled 15 min daily for 3 days prior to surgery, and then presurgery emotionality and activity testing was done. Following surgery they were allowed to recuperate for 14 days and then were once again handled 15 min daily for 3 days. At this time, postsurgery emotionality and activity testing were conducted. Immediately following these tests food deprivation was begun, with animals being maintained throughout the remainder of the experiment at 85% of their ad lib body weights. EXPERIMENT 1: EMOTIONALITY
1.5 IJJ
1.0
.5 I
!
Pre-operative
Post-operative
FIG. 2. Mean preoperative and postoperative emotionality scores for all groups (Experiment i).
Method Apparatus. A modified version of the emotionality rating scale constructed by Tryon, Tryon, and Kuznets [17] was used. The scale included t h e following 6 components: (a) attack or flight reaction to a lead pencil held directly in front of the animal, (b) startle or flight reaction to a light tap on the animal's back with a lead pencil, (c) resistance to capture, (d) muscular tension and resistance to handling, (e) vocalization reaction when captured and handled, (f) urination and/or defecation when captured and handled. Each component was given a rating from 0 - 2 , with 0 being no reaction, 1 being a moderate reaction, and 2 being an extreme reaction. Procedure. After 3 days of handling, both pre- and postoperatively, each animal was carried in his home cage to a table in a quiet room. Each rat then had a pencil placed in front of him, was tapped on the back, was picked up, and was held for 7 sec. Two independent observers rated each animal on all 6 components and a total preoperative and postoperative score were obtained for each animal. Correlations between the observers were calculated for both pre- and postoperative scores (preoperative r = .89; postoperative r = .97). Results and Discussion The results of Experiment I (see Fig. 2) reveal that the emotionality scores of all 3 brain-damaged groups were decreased following surgery, while the scores of Group S remained the same. A Kruskal-Wallis analysis of variance run on the difference scores between pre- and postoperative scores indicated that the groups differed significantly, and subsequent tests (all a posteriori tests reported in this paper were done with the ManmWhitney procedure) showed that the only significant difference was between Group C and Group S, (p
The Effect of Medial Thalamic Lesions on Emotionality, Activity, and Discrimination Learning in the Rat ANN E. WARING AND L A R R Y W. MEANS 2
East Carolina University, Greenville, N C 27834 (Received 8 September 1975)
WARING, A. E. AND L. W. MEANS. The effect o f medial thalamic lesions on emotionality, activity, and discrimination learning in the rat. PHYSIOL. BEHAV. 17(2) 181-186, 1976.- Three experiments were conducted to examine the effects of medial thalamic lesions on emotionality, open-field activity, and discrimination learning. The first study revealed that rats with large medial thalamie lesions are significantly less responsive to capture and to handling than are sham-operated rats. The second study failed to produce any significant differences in open-field activity. A third study revealed that rats with large medial thalamic lesions, and with both small anterior and posterior medial thalamic lesions are impaired on the acquisition of an appetitive visual-tactile discrimination task, with the deficit being greatest in the large lesion group. It was concluded that the medial thalamus plays a role in the neural mediation of certain emotional responses and is critical in the acquisition of complex appetitive tasks. Medial thalamus
Emotionality
Activity
Discrimination
CHANGES in emotionality, activity, and acquisition and retention have been observed to follow lesions of the dorsomedial nucleus of the thalamus (MD) in both humans and infrahuman species. Rats with MD lesions have been observed to be tamer than normal animals [12,21], to freeze less in novel exploration, and to display less emotionality, as evidenced by less defecation [10,21]. The animals, however, exhibit increased freezing in response to aversive stimuli, resulting in deficits in one-way [ 13, 18, 19] and two-way avoidance [1,13]. No deficits are noted in passive avoidance [7,18]. Inconsistent results in activity have been noted; increases have been noted in a bar press situation [8], in the open field [6], and in a nonaversive situation [ 18,20]. Decreases have been found in running wheel activity [5] and spontaneous activity [4]. Several studies have demonstrated no changes in maze exploration [5,12], cage activity [5], cage emergence, and closed field exploration [7]. Impairments in rats with MD lesions have been demonstrated on acquisition of visual discrimination [2,3], visual-tactile discrimination [ 12], visual discrimination reversal, tactile discrimination and reversal [16], and complex spatial discrimination [22]. The rats are also impaired on go, no-go alternation tasks [ 11 ] and go, no-go visual-auditory discrimination tasks [9].
The present study was designed to examine the effects of both large and small medial thalamic lesions on emotionality, activity, and acquisition of a visual-tactile discrimination task. Relatively large lesions were centered on the MD for one group, while small anterior or posterior medial thalamic lesions were produced in the other two groups. The small lesions were an attempt to destroy the anterior or posterior portions of tissue destroyed by the large lesions, and were included to permit a more precise determination of the medial thalamic structures necessary for normal behavior. G E N E R A L METHOD
Animals The same 39 male Long-Evans rats, approximately 110 days old at the time of surgery, were used in all 3 experiments. They were housed individually and maintained on a 14-hr-light, 10-hr-dark cycle. Water was continuously available.
Surgical and Histological Procedure Thirty-one rats received bilateral lesions of the medial thalamus, while 8 rats received sham-operations. The animals were anesthetized with 40 mg/kg pentobarbital
t This paper is based on an MA thesis submitted by AEW to East Carolina University. The authors wish to thank Larry Hayes and John Whisnant for their assistance and Karl Wuensch for his helpful comments. 2Requests for reprints should be sent to Larry W. Means, Department of Psychology, East Carolina University, Greenville, N. C. 27834. 181
182
(
WARING AND MEANS
.
) 1,
) FIG. 1. Reconstruction of the largest and smallest lesions of Group A (left column), Group P (center column), and Group C (right column). (Nembutal) and received 0.20 ml of Bicillin. Each animal was placed in the stereotaxic with the top of the incisor bar elevated 5.0 mm above the ear bar, and lesions were made by passing 2.0 rnA anodal current through a stainless steel electrode that was insulated with Epoxylite except for the tip. Ten of the rats received small bilateral lesions of the anterior medial thalamus (Group A). The lesions were made by passing current for 8 sec with the tip of the electrode placed at coordinates 0.6 mm behind bregma, 1.0 mm lateral to the midline, and 6.2 mm below the top surface of the skull. Eight rats received small bilateral lesions of the posterior medial thalamus (Group P). These lesions also were formed by passing current for 8 sec, with the coordinates being 1.8 mm behind bregma, 1.0 mm lateral to the midline, and 6.2 mm below the skull surface. Thirteen animals received large bilateral lesions of the medial thalamus (Group C). These animals had current passed for 15 sec with the coordinates being 1.2 mm behind bregma, 1.0 mm lateral to the midline, and 6.2 mm below the skull surface. Eight animals received sham-operations (Group S), which involved the same surgical procedure except the electrode was lowered only 5.0 mm below the surface of the skull and no current was applied. At the completion of the behavioral testing all rats were
sacrificed with an overdose of Nembutal, the animals were perfused with Formalin, and the brains were extracted and sectioned at 50 u while frozen. Every fourth section throughout the extent of the lesion was photographed using 35 mm Kodak High Contrast Copy Film. The extent of lesion damage was determined by projecting the negatives onto corresponding plates from Pellegrino and Cushman's [14] stereotaxic atlas. The lesions were traced onto copies of plates and a grid was used to determine the per cent damage to each structure. Figure 1 shows reconstructions of the largest and smallest lesions in each group. Group A lesions were centered on the anterior portion of the MD and destroyed bilaterally a mean of 38% of the MD. In most animals in Group A the lesions also invaded the midline nuclei, the anteroventral nucleus, the habenulointerpeduncular tract, and the stria medullaris. Group P lesions, which were on the posterior border of the MD, resulted in a mean bilateral destruction of the MD of only 6 per cent. Most of the animals in this group had extensive damage of the habenula and some damage to the pretectal area, parafascicular nucleus, paraventricular nucleus, and stria medullaris. The Group C lesions were centered on the MD and bilaterally destroyed a mean of 44 per cent of the MD. Lesions in this
MEDIAL THALAMUS AND BEHAVIOR
183
group also destroyed the midline nuclei and invaded the habenula, anterodorsal nucleus, pretectal area, and stria medullaris. Twelve animals received minimal bilateral damage to t h e hippocampus, averaging approximately 1.0 percent. Note, that as intended, there was considerable overlap of the small lesions of Groups A & P with the relatively large lesions of Group C.
Anterior
¢ "
:
Posterior
.~*
--"
Central
e---e
Sham
3.5
3.0
d
2.5
General Procedure 2.0
All animals were handled 15 min daily for 3 days prior to surgery, and then presurgery emotionality and activity testing was done. Following surgery they were allowed to recuperate for 14 days and then were once again handled 15 min daily for 3 days. At this time, postsurgery emotionality and activity testing were conducted. Immediately following these tests food deprivation was begun, with animals being maintained throughout the remainder of the experiment at 85% of their ad lib body weights. EXPERIMENT 1: EMOTIONALITY
1.5 IJJ
1.0
.5 I
!
Pre-operative
Post-operative
FIG. 2. Mean preoperative and postoperative emotionality scores for all groups (Experiment i).
Method Apparatus. A modified version of the emotionality rating scale constructed by Tryon, Tryon, and Kuznets [17] was used. The scale included t h e following 6 components: (a) attack or flight reaction to a lead pencil held directly in front of the animal, (b) startle or flight reaction to a light tap on the animal's back with a lead pencil, (c) resistance to capture, (d) muscular tension and resistance to handling, (e) vocalization reaction when captured and handled, (f) urination and/or defecation when captured and handled. Each component was given a rating from 0 - 2 , with 0 being no reaction, 1 being a moderate reaction, and 2 being an extreme reaction. Procedure. After 3 days of handling, both pre- and postoperatively, each animal was carried in his home cage to a table in a quiet room. Each rat then had a pencil placed in front of him, was tapped on the back, was picked up, and was held for 7 sec. Two independent observers rated each animal on all 6 components and a total preoperative and postoperative score were obtained for each animal. Correlations between the observers were calculated for both pre- and postoperative scores (preoperative r = .89; postoperative r = .97). Results and Discussion The results of Experiment I (see Fig. 2) reveal that the emotionality scores of all 3 brain-damaged groups were decreased following surgery, while the scores of Group S remained the same. A Kruskal-Wallis analysis of variance run on the difference scores between pre- and postoperative scores indicated that the groups differed significantly, and subsequent tests (all a posteriori tests reported in this paper were done with the ManmWhitney procedure) showed that the only significant difference was between Group C and Group S, (p
