Physiology and Behavior, Vol. 9, pp. 269-2?2, Brain Research Publications Inc., 19"/2. Printed in Oreat Britain.

BRIEF COMMUNICATION

Successive Position Reversals in Rats with Septal and/or Fronto-Polar Lesions'

B. S R E B R O ~ A N D I. D I V A C 3

Nencki Institute o f Experimental Biology, Warsaw, Poland

(Received 30 Augus t 1971)

SREBRO, B. AND I . DIVAC. Successive position reversals in rats with septal and or fronto-polar lesions. PHYSIOL. BEHAV. 9 (2) 269-272, 1972.--Emotionality and ability to reverse a position habit were examined in rats with septal lesions and/ or frontal pole ablations. Ablation of the frontal poles alone or superimposed on septal lesion facilitated the first two out of eight position reversals. Septal lesions strongly impaired all eight reversals and lead to "septal rage" which was enhanced when frontal poles were additionally ablated.

Septal lesion Fronto-polar ablation Emotionality Successive reversals

LARGE septal lesions in rats affected motivational [8, 16] and emotional [1, 20] aspects of behavior, and impaired position reversals [17, 19]. Ablations of the frontal poles in rats affected neither emotional behavior [23] nor reversals of position habit [6, 14], but facilitated other kinds of reversals [3, 4, 11]. Addition of neocortical ablations to septal lesions enhanced and prolonged septal hyperemotionality [23].

The present study examined whether the septal impairment in successive position reversals would be enhanced by super- imposed fronto-polar ablations, analogously to the effect of the combined lesions on emotional behavior.

METHOD

Subjects

Thirty adult male Wistar rats of the Nencki strain were used. The animals were housed in groups of three or four in a cage. Once daily, just after testing, they were given rodent pellets ad lib for one hr. Water was always available. The animals were randomly divided into four groups, three received brain les ions: fronto-polar cortex (F), n - - - -8 ; septum (S), n = 8; fronto-polar cortex and septum (FS), n = 8; and the fourth was unoperated control (N), n = 6.

Apparatus

A modification of the Thompson and Bryant [18] dis- crimination box was used. A transparent guillotine door when lifted allowed entrance from the start compartment into the choice area which was separated from the goal boxes

by two gray doors hinged on a horizontal bar. These doors had a blocking device and both goal boxes contained the food trays for a reward. A piece of cookie about 0.2 g was the reward throughout the study.

Procedure

Preoperatively all animals were adapted to the apparatus with the goal-doom removed. On the first day the rats were left in the discrimination box for about 5 min in groups of three or four. On subsequent days the rats were run indi- vidually. Food was offered in both goal boxes. The pre- operative shaping ended when an animal accomplished two successive runs in 10 see or less. Ten trials were given daily throughout the experiment.

Two weeks after surgery shaping was resumed. On the first day there were no doors in front of the goal boxes. These were introduced on the second day, first lifted and then gradually lowered in seven equal steps from horizontal to vertical position. Two successive runs accomplished in 10 sec or less resulted in lowering the door one step. After the rats finished the last step of pretraining with the hinged doors in the vertical position, the reward was placed for every animal only on the left side (the "correct" one). The in- correct door was locked. An approach to it was recorded as a vicarious trial, and touching it as an error. No corrections were allowed; when an error was made the rat was immedi- ately removed from the apparatus. The criterion for acquisi- tion of the initial position habit and all consecutive reversals

1This study was supported by Foreign Research Agreement No. 287707 of U.S. Dept. of Health, Education and Welfare under PL480. The authors thank Hanna Kosmal for her help in histological verification of the lesions, and Ala Boguslawska for technical assistance, Dr. Holger Ursin and Mr. Hugh Allen are appreciated for their help with the manuscript.

2Present address: Institute of Physiology, 5000 Bergen, Norway. aPresent address: Institute of Neurophysiology, 2100 Copenhagen, Denmark.

269

270 SREBRO AND DIVAC

was no more than two errors in twenty runs (90 ~o of correct choices for two consecutive days). Eight successive position reversals were given to all subjects.

Surgery and Histology The operations were performed in clean conditions under

60 mg]kg pentobarbital. The fronto-polar ablations were made by suction and septal lesions by passing 2rnA anodal current for 15 see through a stainless steel electrode 0.5 mm in diameter, insulated except for the 0.5 mm tip made conical by polishing. The coordinates were according to De Groot [5,] A = + 1.7, L = +0.5 from bregma and V = --5.5 mm from the skul l . The combined lesions were made in one session, septal preceding the fronto-polar.

On days 1, 3, 5 and 10 of the two-weeks postoperative recovery the animals were given a battery of three tests for an estimate of hyperemotionality. The tests were modified after Brady and Nauta [1]. Resistance to handling, reaction to an approaching object (pencil), and startle to a tap at the rump were evaluated. Within each test, reactions were ranged from absence, rated zero, to fierce struggling, magnet-like following of the object, and a high jump to the tap, rated 3.

After the last reversal, all operated animals were sacrificed and perfused, the brains were removed and embedded in paraffin. Coronal sections 10 ~ thick were cut. Every 5th section in the zone of lesions and every 20th outside that zone were stained by the Kltiver-Barrera method. The largest and the smallest lesions of each group are presented in Fig. 1.

RESULTS

The effects of septal, fronto-polar and combined ablations on learning of the initial position habit and eight successive reversals are presented in Fig. 2. There were no group differences during acquisition of the initial position habit as well as in the preliminary training. Analysis of variance showed that septal damage significantly impaired ability to reverse the position habit throughout the training (p <0.001). (For the analysis of variance 2 x 2 table for disproportionate sub-class members was used. The scores from two suc- cessive reversals were added and transformed into ~ / ~ +1) [22]. Rats with septal lesions approached the previously correct door over many trials and in a stereotyped manner. Direct approaches to the correct door increased in frequency only shortly before the reversal criterion was attained. Animals with septal lesions made significantly more vicarious trials during all reversals (p <0.001).

Analysis of variance also revealed significant facilitation of the two first reversals taken together in animals with fronto-polar ablations CO<0.01). Individual comparisons (Mann-Whitney two-tailed U test) revealed that during the first two reversals the FS group made significantly fewer errors than S group, both in errors to criterion and in errors to the first correct choice in a reversal CO<0.01) ; the F group made fewer errors to the first correct choice in a reversal than did the N group CO<0.05). In the very first reversal, however, the F group was significantly better than the N group in both measures Co <0.01).

Differences in emotionality were observed in all three tests. Rats with septal lesions were resistant to handling, followed in a magnet-like manner a pencil waved in front of their snout, and jumped to the tap at the rump. They also engaged in longlasting fights in their cages. Fronto-polar ablations increased and prolonged this septal lesion effect, but had no detectable effect by itself on emotionality. No animal in the

F group or the N group displayed fierce struggling, magnet- like following or jump to the tap at the rump.

DISCUSSION

Ablation of the frontal poles in rats enhanced and p r o longed septal hyperemotionality and at the same time diminished the deficit in reversal of a position habit caused by septal lesions. This dissociation suggests that the deficit in position reversal ability is not related to the hypere- motionality produced by septal damage.

In the present study an enhancement of the septal emotion- ality was observed after neocortical ablations much smaller than those reported earlier [23]. A similar effect has also been obtained with ablations of other neocortical regions [24].

The facilitation of the reversal learning seems to be an effect of fronto-polar ablation in the rat rather than an interaction resulting from the combination of lesions.

FRONTO- POLAR

SEPTAL AND FRONTO-POLAR

FIG. l. Maximal (stripped) and minimal (dark) extent of the lesions for the septal group, fronto-polar, and combined fronto-

polar and septal.

SEPTAL AND OR FRONTO-POLAR LESIONS 271

MEAN ERROR

60

50

40

30

tl

"~O NORMAL CONTROL

-,.& F R O N T O - P O L A R ABLATION

--o SEPTAL LESION

- - ~ F R O N T O - P O L A R AND

SEPTAL ABLATION

, . , \

10 ~ . ",%.__

ACQ 1 2 3 4 5 6 7 8

REVERSALS

FIG. 2. Mean errors in initial acquisition and eight successive reversals of a position habit for all experimental groups.

Facilitation of visual discrimination reversal [4, 11 ] and maze reversal [3] after fronto-polar ablations in rats was unexpected when first reported. The facilitation of position reversals was not regularly observed [6] and the conditions under which it occurs are not known.

The faster reversal of a position discrimination reported here would be difficult to explain if the frontal poles in rat continued to be considered as prefrontal cortex, since an impairment is usually seen after comparable lesions in monkeys [15] and carnivores [21]. Recently, Leonard [12] provided data which could explain the puzzling absence of the " f ron ta l syndrome" after polar ablations in the rat. Analysis of connections suggested that prefrontal cortex (defined as the projections field of the dorsomedial thalamic nucleus) is located on the anteromedial and inferolateral surface of the rostral part of the rat brain. The area of the frontal pole, on the other hand, was found to resemble the premotor cortex of other mammals.

A deficit in a single reversal of a position habit after septal lesions has been reported both in rats [19] and in cats [25]. In the present study, rats with septal lesions showed an impairment in a series of position reversals. Their perfor- mance improved significantly during the course of training.

It has been suggested that the spatial reversal deficit in the monkey after ablations within the frontal region results

ERRORS

100

80

60

40

20

I~/J ERRORS TO FIRST CORRECT CHOICE

--]ERRORS TO CRITERION

£ /

;..

L

No r,',a, F .to-S ta, polar

Fronto- polar and septal

FIG. 3. Errors to first correct choice and to criterion in the first two reversals (combined) for all experimental groups. The standard

errors of the means are indicated.

either from difficulties with reversal or from failure to use spatial/positional cues [15]. The same deficit in rats with septal lesions cannot be attributed to a general difficulty in reversal learning since such animals are not impaired in a reversal of visual discriminations [13, 17]. It is more likely that rats with septal lesions are not able to use spatial/ positional cues as efficiently as normals. This suggestion is supported by the impaired performance of the rats with septal lesions in maze learning [2], spontaneous alternation [7] and in a resolution of approach-avoidance conflict [10].

An alternative explanation of the impairment in position reversal is possible. It was found that highly motivated normal rats are impaired in successive reversals of spatial discrimination when they receive a small reward [9]. The performance of those animals resemble the impairment seen in animals with septal lesions in the present study. It is possible, therefore, that septal lesions produce an impairment in the position reversal ability by changing the incentive value of positive reinforcement. Similar explanation has been offered for other deficits following septal lesions [8, 16]. Such motivational dysfunction, however, does not exlude the possibility of concurrent impairment in the ability to use spatial/positional cues.

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272 SREBRO AND DIVAC

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