open-field behavior in rats - acta … neurobiol. exp. 1981, 41: 197-210 open-field behavior in rats...

ACTA NEUROBIOL. EXP. 1981, 41: 197-210

OPEN-FIELD BEHAVIOR IN RATS WITH FRONTOMEDIAL CORTICAL, NEOSTRIATAL

OR HIPPOCAMPAL LESIONS

Alicja MARKOWSKA and Irena EUKASZEWSKA

Department of Neurophysiolagy, Nencki Institute of Experimental Biology Pasteura 3, 02-093 Warsaw, Pdand

Key words: open-field behavior, dorsal prefrontal system, rats

Abstract. The effects of lesions in four structures corresponding to the main components of dorsal prefrontal system of the monkey were studied in a total of 165 rats. In a homogeneous open-field apparatus, rats with frontomedial cortical (FM) or anteromedial neostriatal (NC) lesions showed more ambulations than their respective sham operated controls. Posteroventral (VH) and anterodorsal (DH) hippocampal dam- ages did not affect ambulations. The introduction of a novel stimulus produced transient suppression of open-field activity in all lesioned and control groups. Exploratory responses to the stimulus, assessed by the number of direct contacts and the time spent near the stimulus, were fewer in rats with VH or DH lesions than in rats with FM or NC lesions, that in turn did not differ from controls in this respect. Fear, indicated by defecations during the entire open-field test and by prolonged activity suppression in response to the presence of the novel sltimulus, was observed in FM or VH lesioned rats, but not in those subjects with NC or DH lesions. Functional interrelations among these structures are discussed relative to their participation in a common functional system.

INTRODUCTION

Most research studies on the behavioral roles of principal structures in the "dorsal" prefrontal subsystem of the rat have found similar effects between dorsomedial prefrontal damage and anteromedial neo-

striatum destruction in such tasks as spontaneous alternation, delayed alternation or spatial reversal (6, 8, 9, 21, 28). However, our recent investigation has disclosed a functional dissociation between these structures in the regulation of emotional states evaluated by a multicategory scale (18). Nonneman et al. (19) have suggested that both major sub- fields of the rat's prefrontal cortex, dorsomedial and sulcal regions, are functionally related to the hippocampus. According to our previous report (18), the similarity of effects on emotional reactivity was stronger between dorsomedial prefrontal destruction and destruction of posteroventral than anterodorsal hippocampus.

To extend the generalization of our previous findings, it seemed desirable to examine the influence of the same lesions on emotionality assessed under different conditions, and for this purpose, the open-field test appeared appropriate. Emotionality (or fear) is widely assumed to underlie a large number of open-field parameters, among them defecation and ambulation. However, ambulation has also been thought to be indicative of exploration, or locomotor activity per se. Therefore, the present experiment included, beside the most widely used measures of defecation and ambulation, responses to a novel stimulus placed in the open-field apparatus to try to differentiate emotionality and ex-. ploration. The experiment used the same subjects that previously (18)' were employed in the emotionality rating by the multicategory scale, which provided an opportunity for closer comparison of the lesion effects on emotional reactivity evaluated under two different conditions.

METHOD

Subjects. The subjects were 165 male Wistar albino rats, approximately 100 days old at the time of the experiment. They were housed in groups of 5-7 with food and water available ad lib. The rats were maintained in the laboratory for 2 wk after their arrival from the animal breeding farm. During this time they were handled 5 min per day for 6 days prior to surgery in order to diminish individual differences in emotionality. About 40 rats were assigned to each of four surgical treatments: frontomedial cortical (FM), anteromedial neostriatal (NC), anterodorsal hippocampal (DH) and posteroventral hippocampal (VH). Within each treatment, the subjects were randomly divided into lesioned and control groups. The experiment was conducted successively, so that only one lesioned group and its control group were tested in a given time period. Prior to the present experiment, emotional reactivity had been tested, the results of which have been reported separately (18)- The present experiment started 1 day after emotionality testing.

Surgery and histology. All brain lesions were performed by stereotaxic coagulation (for details, see 18). The animals of the control groups. received an incision and skull holes were drilled, but no lesions were made. After behavioral testing, deeply anesthetized rats were perfused with a 10'310 formalin-solution. Their brains were frozen, sliced at 50 pm frontal sections, and stained following the Kliiver-Barrera method. The extents of the lesions were transfered to the standardized diagrams of Konig and Klippel (15).

Apparatus. Open-field test was conducted in 120 X 120 cm - square box with a wall height of 50 cm. The walls were constructed of plywood and painted light gray. The black plastic floor was divided by painted white lines into 36 squares, each 20 cm on a side. The only illumination in the testing room was from a 40 W light suspended 1 m above the center of the open-field.

Procedure. Beginning 11 days after surgery, all rats were given daily 3-min sessions in the open-field apparatus for 5 consecutive days. On Days 1 and 2 the apparatus was empty, while on Days 3, 4 and 5. the novel stimulus of a white plates 20 cm in diameter, was placed at the center of the field. On each session the subject was placed in the apparatus and the following observations were recorded: (i) the number of squares entered with all four paws, (ii) the amount of time-spent in the center of the apparatus on the inner squares not adjacent to the walls and (iii) the amount of defecatiodurination. Additionally, the numbers of contacts with the stimulus were counted on Days 3, 4 and 5. The field was wiped clean after each rat was tested.

RESULTS

Anatomy

Typical lesions are presented in Figure 1, while more details of t he histological results were presented elsewhere (18). Briefly, the frontomedial cortex (FM) was ablated from the frontal pole to the genu of the corpus callosum. The neostriatal lesions (NC) destroyed the region that receives projections from the frontomedial cortex. The hippocampal lesions were restricted to the anterodorsal (DH) or to the posteroventral portion (VH) of this structure.

Behavior

Locomotor activity. Figure 2 presents the mean numbers of crossings for all groups over the 5 days of testing, i.e., the two days in the empty open-field apparatus (Days 1 and 2) and the three days during the presentation of the novel stimulus (Days 3-5). The overall

analysis of variance (Treatments X Groups X Days) disclosed significant Day (F = 17.29, df = 4/628, P < 0.001) and Treatment effects ( F = 2.72, df = 31157, P < 0.05). Although the main effect of Groups was nonsignificant, the differential effects of various lesions were shown by a significant interaction between Treatments and Groups (F = 2.91, >df = 31157, P < 0.05). The Treatment and Group variables produced different changes in ambulations over testing days as indicated by significant Treatments X Days (F = 5.70, df = 121628, P < 0.001) and Groups X Days ( F = 9.03, df = 41628, P < 0.001) interactions. The nonsignificant triple interaction of Treatments X Groups X Days indicated a' similar time course of activity changes in all treatments and groups. As seen from Fig. 2 in all four control groups ambulations increased on the second day in the open-field apparatus. Introduction of the novel stimulus resulted in the lowering of activity level (Day 3) which increased again on subsequent days with presence of the stimulus.

Fig. 1. Represenbative destructions of the frontoanediall (FM), aeostriatal (NC), dorsal hippocampal (DH) and ventral hippocampal (VH) lesions.

Separate two-way analyses of variance performed for each treatment allowed more detailed comparisons between the lesioned and respective control groups. Under the F M treatment, a significant Day effect (F = = 5.49, df = 41160, P < 0.001) and Days X Groups interaction (F = 6.87, df = 41160, P < 0.001) were shown, which indicated different ambulation changes in the operated and control groups. In the empty open-field apparatus, the lesioned rats were more active than the sham lesioned controls (Duncan test, P < 0.05). On the first day of novel stimulus presentation (Day 3) both groups displayed similar decreases of activity with respect to Day 2 ( P < 0.01). Subsequently, the control rats showed a n increase of ambulations, while activity of the lesioned rats was

maintained at the level of Day 3, so that between groups differences vanished on Day 4. On Day 5, the control rats were more active than the lesioned subjects ( P (0.05). Rats with NC lesions showed different activity levels than their respective controls ( F = 8.13, d f = 1/42, P < < 0.01). Activity changed over days in both groups ( F = 7.70, df = = 4/168, P < 0.001), and the nonsignificant Groups X Days interaction reflected a similar course of changes. However, the Duncan tests indicat- led that the lesioned rats were more active than the controls in the empty open-field on Days 1 and 2 (P < 0.05 and P < 0.01, respectively).

B k k I I I I J I I I I J

t Q, D E DH

60

I I l l I I 1 I I 1 2 3 4 5 1 2 3 4 5

Days Fig. 2. Ambulation in the homogeneous open-field apparatus (Days 1, 2) and in the presence of the noyel stimulus (Days 3-5). Open circles, control group; filled

circles, merated groups.

The introduction of novel stimulus resulted in an activity decrease in both groups (P < 0.05). During succeeding days with the novel stimulus presentation the initial difference between groups disappeared. The lesioned and control groups of the DH treatment did not differ and

showed similar changes of activity across testing days, which was reflected by significant Day effect (F = 6.97, df = 4/152, P < 0.001), the nonsignificant effects of Groups (F < 1) and Groups X Days interaction (F< 1). Under this treatment the activity decrease in response to the introduction of the novel stimulus did not attain acceptable significance. In the VH treatment the main Group effect was not reliable, but differences among Days were significant ( F = 18.53, df = 41148, P < 0.001). As shown by Duncan tests, both groups were less active when the novel stimulus was placed in the apparatus (Day 3, P < 0.01). On Day 4 the lesioned rats showed a further decrease of activity ( P < 0.05) which remained approximately constant to Day 5. The control rats, after initial suppression ( P < 0.01), showed the typical increase of activity. These changes accounted for a Groups X Days interaction (F = 8.37, df = 41148, P < 0.001).

T i m e in center. Mean time spent within the central squares by each group across the 5 days of testing is presented in Fig. 3. The overall ANOVA (Treatments X Groups X Days) showed that all main effects

Days

Fi8g. 3. Time in the center of homogeneous open-gield (Days 1, 2) and Ln the presence of the novel stimulus (Days 3-5). Denotations as in Fig. 2.

were significant (F = 8.00, df = 31157, P < 0.001; F = 12.37, df = 11157, P < 0.001 and F = 84.12, d f = 41628, P < 0.001, respectively). Significant Treatments X Days (F = 4.73, df = 121628, P < 0.001) and Groups X X Days interactions (F = 5.22, df = 4/628, P < 0.001) reflected differential rates in time spent in the central squares by subjects from various treatments and groups across testing days. The remaining interactions were nonsignificant. These effects were further examined by two-way ANOVAs. In the FM treatment the Group effect (P> 0.1) was not reliable, but a significant effect of Days (F = 21.55, df = 41160, P < < 0.001) emerged, indicating that the amount of time in the center of the apparatus increased during successive days in both lesioned and control groups. The effect of novel stimulus presentation could not be satisfactorily evaluated, since the groups of the FM treatment showed similar increament of time in the center during the first two testing days as they did after introduction of the novel stimulus. The significant Groups X Days interaction (F = 2.42, df = 4/160, P < 0.05) was pro- bably due to between-group differences on Day 5. In the NC treatment, differences between the lesioned and control rats were nonsignificant (P > 0.1) as was the Groups X Days interaction (P 7 0.1). The time spent in the central squares by both groups increased across days (F = 19.97, df = 41168, P < 0.001), but this increase attained significance only after novel stimulus introduction (Duncan tests, Ps < 0.01). The lesioned and control rats of the DH treatment showed a similar trend of changes across testing days which was reflected by the effect of Days (F = 35.05, d f = 41152, P < 0.001) as well as the nonsignificance of the Groups X X Days interaction ( P > 0.1). The increase of time in the center was more pronounced in the DH control rats than in their lesioned counter- parts (Group effect, F = 4.81, df = 1/38, P < 0.05). However this difference was reliable only during presentation of the novel stimulus (Dun- can tests, Ps < 0.05). In the V H treatment, the Day effect was significant (F = 16.44, d f = 41148, P < 0.001), while Group effect was not (P > 0.1). The Groups X Days interaction reached significance (F = 2.56, d f =

= 41148, P < 0.05), which was the result of shorter time in the center of the apparatus on the part of the lesioned subjects during novel stimulus presentations.

Defecation and urination. Mean defecatiodurination scores for each surgical treatment across the 5 days of testing are presented in Fig. 4. The overall analysis of variance (Treatments X Groups X Days) indicated that all main effects were significant (F = 7.91, df = 31157, P < 0.001; F = 5.65, df = 11157, P < 0.05 and F = 29.68, df = 4/628, P < 0.001, respectively). The amount of fecal boluses and urination differed under various treatments on different days as indicated by a significant inter-

action between Treatments and Days ( F = 4.41, df = 12/628, P < 0.001). The nonsignificant Groups X Days interaction (P > 0.2) indicated a similar direction of changes in the lesioned and control groups. The significant triple interaction (F = 2.02, df = 12/628, P < 0.01) might be attributed to the lesion effects on the magnitude of changes. Two-way ANOVAs indicated no between-groups differences in the NC and DH t r e a t m e n t s ( F s < 1). In both treatments defecation and urination diminished during successive days in the open-field (Day effects; F = 9.34, df = 4/168, P < 0.001 and F = 8.46, df = 4/152, P < 0.001, respectively)..

Days

Fig. 4. Defecation/urinartion scores in the homogeneous qpen-field (Days 1, 2) a n 8 in the presence of the novel stimulus (Days 3-5). Denotations as in Fig. 2.

Interactions between Groups and Days were nonsignificant. No indications of response to novel stimulus presentation regarding defecation or urination were noted in the NC and DH treatments. In the FUM t r e a t m e n t , lesioned rats defecated and urinated more than controls ( F = = 5.33, df = 1/40, P < 0.05). The Day effect was significant (F = 2.74, df = 4/160, P<0.05), however no systematic changes in defecation/' /urination over days were observed. The interaction between Groups. and Days was nonsignificant ( F < 1). In the VH t r e a t m e n t the Group effect was nonsignificant (P> 0.2) in contrast to the Groups X Days

interaction which was highly significant (F = 4.70, df = 4/148, P < < 0.001). The lesioned and control groups did not differ in the empty open-field, while during presentation of the novel stimulus lesioned rats defecated and urinated more than controls (Duncan tests, P s < 0.05). Defecation and urination diminished in both groups during successive, days (F = 29.14, d f = 41148, P < 0.001).

Novel stimulus contacts. Figure 5 shows mean numbers of contacts with the novel stimulus for each treatment across the 3 days of testing. The overall ANOVA (Treatments X Groups X Days) showed significant

Days

Fig. 5. Direct contacts with the nwel stimulus. Denotations as in Fig. 2.

Group effect (F = 9.29, df = 11157, P < 0.01) and Groups X Treatments interaction (F = 2.69, d f = 31157, P < 0.05), which indicated that lesioned rats of the DH and VH treatments showed lower numbers of contacts than respective controls. The FM and NC treatments did not- influence this measure. The number of contacts increased across successive days in all treatments (F = 21.99, df = 2/314, P<0.001), and the time course of these changes was similar in all treatments and groups across testing days, as indicated by nonsignificant interactions related to time (Fs < 1).

DISCUSSION

In the homogenous opeq-field, FM and NC lesioned rats showed higher ambulations than their respective controls, while no group differences were observed under the DH and VH treatments. The increase of locomotor activity following frontomedial lesion is in accordance with the findings of previous studies in rats (4, 9, 14, 17). Regarding the influence of neostriatal lesion on locomotor activity, our results con- firm the reports of hyperactivity after this type of lesion (1, 13, 24). The failure of some authors (11, 25) to observe the influence of neostriatal lesion on open-field activity in rats might be explained by different localizatons of their lesions which missed the area receiving the efferents from the frontomedial cortex.

There is considerable disagreement concerning the involvement of hippocampus in open-field activity. Some investigators demonstrated an increase of ambulations evoked by destructions of the dorsal (3, 12) or ventral (16, 23) hippocampal regions, whereas others have reported no changes (2, 10). One important reason for these discrepancies might be attributed to the surgery - test interval. Kimble (12) has found that the hyperactivity in open-field peaks between 6 and 8 days after lesions and then begins to decline. The hyperactive period lasts until the 14th day. Our data were collected on 11 and 12 postoperative days, i.e., during the period of elevated activity as delineated by Kimble, however, no difference between the lesioned and control hippocampal groups was observed. This lack of a hippocampal effect might be due to a different postoperative time course of activity changes in our rats.

In view of the widely accepted negative relationship between the open-field ambulation and defecation; it seems pertinent to note that i n our experiment the brain lesions either had a similar effect on both measures (FM - increase, DH - no effect) or influenced only one measure (NC - ambulation, VH - defecation). These findings might indicate that ambulation' reflected the level of motor activity per se in our subjects, which was not necessarily related to emotionality. However, group means are a weak measure and individual scores would be re- quired to define the relationship between ambulations and defecations. Such a correlation was not done in our study.

The introduction of the new stimulus to the open-field apparatus (Day 3) elicited orienting response in all lesioned and control groups judging from the suppression of locomotion and from the increase of time spent in the central squares. On successive days with novel stimulus presentation ambulations increased after the initial suppresion in all control groups, as well as in the NC and DH lesioned groups,

whereas in the FM and VH lesioned groups, ambulations remained at the lowered level until the end of testing. Since only the lesioned FM and VH groups showed more defecation and urination in the open-field, it seems likely that they responded to novel stimulus with higher emotionality than other groups which was reflected in their persistence of locomotor suppression. This interpretation is consistent with our previous finding (18) indicating higher emotionality in the FM and VH lesioned groups than in the NC and DH lesioned groups, when tested by the multicategory scale.

Responses to novelty were not affected by FM or NC lesions since no significant differences were observed between the lesioned and control groups in the number of direct contacts with the novel stimulus and the time spent near it. In contrast, the VH and DH lesioned groups displayed lower responsiveness to the novel stimulus than their respective controls as indicated by both measures. Novel stimulation presu- mably evokes both an exploratory drive and fear, so that the common assumption is that emotionality and exploration, similar to ambulations are inversely related. The data of our previous (18) and present experi- ments provided no evidence for this relationship. Although the FM lesioned group was emotional while the NC was not, both groups were not deficient in responsiveness to novelty. On the other hand, lowered responsiveness was observed in emotional VH lesioned group as well as in the DH lesioned group, which showed much lower emotional reactivity. But again, the limitation imposed by group means requires caution when assessing the relations between particular measures. Mo- reover, the contribution of other factors (e.g., the level of ambulations in the empty open-field) may be also of importance. Whimbey and Denenberg (26) have shown that ambulations loaded positively on exploration. In tihis context, it is interesting to note that the unaffected level of novel stimulus exploration observed after FM and NC lesions was associated with increased ambulations on Days 1 and 2. In contrast, decreased stimulus exploration occurred after both hippocampal lesions which had no effect on initial ambulation.

Several investigators have suggested that due to poorer attention, hippocampal rats are less likely to attend to the relevant cues, parti- cularly nonsalient ones (for review see 20). This hypothesis might account for the lowered number of exploratory responses to the novel stimulus shown by the DH and VH lesioned groups. However, such an interpretation is not consistent with the lack of differences between the Dfi or VH lesioned subjects and their respective controls in the level of orienting responses to the introduction of the stimulus. Moreover, if the novel stimulus elicited fear responses in the VH lesioned rats it

6 - Acta Neurobiol. Exp. 2/81

had to be salient for them. It seems probable that lowered object exploration in the DH or VH lesioned groups might be attributed simply to the decrease of exploratory motivation following the hippocampal lesions, which has been reported in several papers (5, 22, 27).

The results of the present experiment provide further indications concerning functional relations among structures belonging to the dorsal prefrontal system. Similarities and differences of the effects of various lesions are summarized in Table I. As seen, a functional affinity between

Characteristics of changes'in open-field performance following different lesions. Upward arrows denote increase, downward arrows - decrease

of respective parameters.

Lesioned Arnbular groups empty op

the frontomedial cortex and the anteromedial part of the neostriatum, found in previous researches (6-9, 21, 28), is confirmed by the present data concerning the locomotor activity in the homogeneous open-field and the two measures of exploratory responses to the novel stimulus. However, fear responses evoked by the novel stimulus, which occurred in rats with frontmedlal, but not with neostriatal lesions dissociated the two groups. This finding supports our previous results (18) of differential effects of frontomedial and neostriatal lesions on emotionality. A similar pattern of relations was observed after dorsal and ventral hippocampal lesions, i.e., the effects of both types of lesion on activity in the empty open-field and on object exploration were alike, while fear responses were found only in rats with ventral hippocampal lesion.

The comparison between the frontomedial cortex - neostriatum couple of structures on the one hand, and the hippocampus on the other, reveals a clear dissociation in the behavior of lesioned rats in the homogeneous open-field and in exploratory responsiveness to a novel stimulus. However some functional correspondence between the ventral hippocampal region and the frontomedial cortex is provided by fear responses.

This investigation was supported by Project 10.4.1.01.2 of the Palish Academy of Sciences.

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Accepted 10 November 1980

open-field behavior in rats - acta … neurobiol. exp. 1981, 41: 197-210 open-field behavior in rats...

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