BEHAVIORAL BIOLOGY 15, 479-484 (1975), Abstract No. 5168

BRIEF REPORT Distractibility and Reactivity under Different Response Conditions Following Hippocampal Lesions in Rats 1

JOHN W. GUSTAFSON 2

Department of Psychological Sciences, Purdue University, West Lafayette, Indiana 47907 In order to evaluate appropriate measures for distractibility and reactivity, rats with dorsal hippocampal lesions were compared with sham operated controls on measures of responsiveness to a distracting stimulus that was presented under three conditions of ongoing operant or consummatory activity. The distractor was a compound auditory-visual stimulus delivered twice in each of three daily sessions, in each instance following (a) the second response of a fixed-ratio sequence; (b) the sixth response of a fixed-ratio sequence; or (c)5 min of licking for sucrose solution. The duration of distraction was lower among lesioned subjects than among controls under all three response conditions and lower for both groups of subjects under the latter two conditions than under the first. The lesion effect was more pronounced as a reduction in exploration following distraction than as a reduction in orienting activity. In a subsequent test, tentative evidence was obtained for a lesion-induced decrement in dishabituation.

Reduced distractibility has been frequently observed among rats with hippocampal lesions (Wickelgren and Isaacson, 1963; Raphelson, Isaacson, and Douglas, 1965; Kaplan, 1968; Crowne and Riddell, 1969; Riddell, 1969). Because the interval of distraction appears to be closely correlated with orienting activity, this evidence has been considered in connection with hippocampal involvement in processes of orienting and attention that have generated major theoretical interest (Douglas, 1967; Kimble, 1968; Pribram and McGuinness, 1975). Both the behavioral and cardiac components of the orienting response may be altered by hippocampal lesions (Rogozea and Ungher, 1968; Crowne and Riddell, 1969; Hendrickson, Kimble, and Kimble, 1969; Sanwald, Porzio, Deane, and Donovick, 1970), but distractibility is only indirectly a measure of orienting activity, inasmuch as exploration or even the 1This research was supported in part by an XL Grant from Purdue University to J. W. Gustafson. 2Susan A. Hoppe contributed surgical assistance during the research and helpful criticism during the preparation of this report. 479 Copyright © 1975 by Academic Press, Inc. All rights of reproduction in any form reserved.

480

JOHN W. GUSTAFSON

startle response (Kaplan, 1968) may contribute to the distraction interval. In clarification, some investigators (Douglas and Pribram, 1969; Isaacson, 1974; Senba and lwahara, 1974) have emphasized the distinction between distraction by a novel stimulus and the ensuing, often exploratory, reaction to it. This reactivity, like distraction, is sensitive to hippocampal damage (Karmos and Grast)~an, 1962; Rogozea and Ungher, 1968; Sengstake, 1968). The present study was initiated to determine the apparent correspondence between hippocampal lesion effects as they are revealed by measures of orienting and of distractibility. Since lesion effects on orienting vary with the animal's behavioral activity at the time of stimulus presentation (Hendrickson et al., 1969), distractibility was assessed during three different conditions of ongoing background activity. Forty-two male rats of the Holtzman strain, weighting between 325 and 476 g at the beginning of training, received either bilateral electrolytic lesions of the dorsal hippocampus or sham operations without passage of current. All animals were anesthetized with pentobarbital sodium, 40 mg/kg ip, and were mounted for stereotaxic surgery with ear bars placed under the zygomatic arch to avoid damage to the ossicles. After surgery, 2 weeks with free access to food and water were allowed for recovery. The time between surgery and the beginning of behavioral training varied from 3 to 5 weeks among animals. Testing for distractibility was conducted with food-deprived subjects using a Foringer operant chamber that was housed in a sound-attenuating enclosure. Animals were observed through a peephole in the door of the enclosure, with the aid of a house light mounted on the frame of the operant chamber. White noise was delivered during testing at an intensity of 91 db (re: 0.0002 dynes/cru 2), measured within the operant chamber. Two tasks were employed for testing distractibility. In the first, each subject was shaped to lever-press for pellet rewards (45-rug Noyes pellets) in l or 2 days of training. In daily 15-ruin sessions thereafter, with house illuruination and white noise present, the schedule of reinforcement was altered at 2-day intervals from continuous reinforcement to FR-2, -4, -6, and -8. In all following sessions, reinforcement was delivered on an FR-8 schedule. Testing for distractibility was begun after 2 days of training on an FR-8 schedule. Five minutes from the beginning of the session, and again at 10 rain, the distractor was presented. This stimulus consisted of momentary, simultaneous interruptions of both the house-light illumination and the white noise, continuing at 1-sec intervals for a period of 4 sec. The method of distraction was chosen because i t reliably interrupted lever-pressing without eliciting a startle response. After the distractor was presented for the second time within a session, each subject was allowed to bar-press freely until the end of the session. In the second task used for testing distractibility, subjects were trained in the Foringer chamber to lick 10% sucrose solution from a drinking tube

HIPPOCAMPAL LESIONS AND DISTRACTIBILITY

481

that replaced the feeder. Free licking was permitted in ten consecutive daily sessions of 15 rain each. Beginning with the following session, distraction testing was conducted in the same manner as for the lever-pressing task. In three consecutive sessions of testing for distractibility, distraction was measured as the interval between onset of the distractor and the second lick or lever response to follow. The effectiveness of distraction was measured for each hippocampallesioned and control subject under one of three conditions of ongoing operant responding. In the Early Distractor condition, the distractor was triggered by the second response of an FR-8 sequence, at the designated 5-rain intervals. In the Late Distractor condition, the distractor was triggered by the sixth response in the FR-8 sequence. In the Licking condition, the distractor was triggered by a lick response at the designated 5-rain intervals. Under each condition, seven lesioned and seven control subjects were tested. Following the recommendation of Thompson and Spencer (1966) for the identification of habituation, a test of dishabituation was performed at the conclusion of testing for distractibility with subjects in the Early Distractor condition. Hippocampal-lesioned and control subjects were tested for 1 or 2 days, continuing the procedure for testing of distractibility, until the distraction interval for each subject fell to less than 10 sec for both presentations of the distractor within a session. In the following session, the first presentation of the distractor was preceded by the delivery of a 0.5-sec signal from a 2800-Hz Sonalert alarm that was triggered by the sixth lever-press in the FR-8 sequence preceding the distractor. Five minutes later, and in two subsequent sessions, the distractor was presented alone. The delay between the Sonalert signal and the distractor was always less than 1 rain. Histological analysis was performed with 40/~m sections stained with cresyl echt violet. The behavioral data for two subjects of the Early Distractor group were discarded because the lesioned brains were not available for histological examination. In place of these subjects, two additional subjects were prepared and tested during ongoing testing of other groups. Distractibility was consistently lower among lesioned subjects than among controls. As Fig. 1 illustrates, the magnitude of the reduction in distractibility was pronounced in the Early condition, moderate in the Late condition, and negligible in the Licking condition (Groups effect, ANOVAR: F ( 1 , 36)= 9.60; P < 0.01). The nature of this lesion effect was clarified by observation of subjects during presentation of the distractor. Although all but two subjects reacted to the first presentation of the distractor with arrested activity for 10 sec or more, usually with the head oriented initially in the direction of the distractor, the lesioned subjects showed little subsequent tendency to explore the walls of the chamber that separated them from the light and speaker. Among control subjects, exploration accounted for a large proportion of the measured periods of distraction. The exploration was often

482

JOHN W. GUSTAFSON

150I I 75 ', EARLY

.~ 25

o.,.

LATE

LICKING

',

1

2

3

1

2

3

1

2

3

SESSIONS Fig. 1. Distraction intervals (D.I.) under three response conditions, with two trials per session. Filled symbols: hippocampal lesion group. Unfilled symbols: control group. accompanied by rearing or sniffing at floor bars in the front of the chamber. Measurements of the interval of distraction were so rarely contaminated by episodes of grooming and face washing that no correction of the data was made for this activity. Group differences in lever-pressing or licking that preceded testing for distractibility were examined for their possible contributions to the duration of distraction in subsequent testing. However, mean response totals for each subject in the two sessions preceding distraction were only weakly correlated with initial intervals of distraction (Early and Late conditions, r = - 0 . 2 8 ; Licking, r = 0.24). In t tests for these values of r, neither approached significance. Distractibility varied for all groups across Early, Late, and Licking conditions. Following confirmation by analysis of variance of an overall effect of response condition upon distractibility (F(2, 36)=4.12; P < 0 . 0 5 ) , firsttrial intervals of distraction in the Early condition were shown to differ significantly (Newman-Keuls test, P < 0.05) from first-trial performance means in the Late and Licking conditions. Distraction diminished rapidly after the first presentation of the distractor. Over all conditions, the decline in the duration of distraction with repetition was reflected in a significant Trials effect ( F ( 5 , 180)=37.63; P < 0.01), but group differences in the rate of decline were not confirmed statistically. The results of the tests for dishabituation, shown in Table 1, suggest tentatively that the foregoing decline in distractibility was the result of habituation. Distractibility among control subjects rose perceptibly after presentation of the Sonalert signal, but this effect was short-lived and did not achieve statistical significance. In tests for dishabituation, lesioned subjects showed little distractibility, and the dishabituation test for these subjects consequently failed to provide a criterion for habituation. Histological reconstruction of the lesions (Fig. 2) revealed consistent bilateral damage within the dorsal hippocampus. The reduced distractibility during lever pressing among lesioned subjects is consistent with earlier findings. However, in contrast with previous observa-

HIPPOCAMPAL LESIONS AND DISTRACTIBILITY

483

TABLE 1 Intervals of Distraction (Seconds) for Each Subject in the Dishabituation Test Trials

Hippocampal subjects

Mean Sham operates

Mean

Pre-1

Pre-2

3

Dishaba

Post-1

Post-2

6

1

2

1

1

3

3

1 1

6 5 2

4 10 3

3 6 4

3 52 b 1

2 4 6

1

3

2

2

2

3

5

3

2 (9) c

3

5 3 l0

6 4 3

6 6 34

5 6 5

2 6 6

1

9

11

5

2

2

4

4

2

1

4

5

12

5

5

aTrial immediately following presentation of dishabituation stimulus. blnterval occupied by grooming and face washing. CMean intervals excluding and including the extreme score. tions (Crowne and Riddell, 1969; Hendrickson et al., 1969), the behavioral orienting response appeared to have been affected slightly, if at all, by hippocampal lesions. Rather, a pronounced reduction in exploratory reactions to the distractor underlay the reduced distractibility o f lesioned subjects. While a reduction in exploratory reactivity appears to be at variance with reports o f increased exploration among hippocampally lesioned rats in novel surroundings (Nadel, 1968), it should be noted that subjects in the present experiments had received lengthy exposure to the testing chamber before presentation of the distractor, and subsequent exploration must have been triggered with some process of orienting to the distractor. Anterior Section

Middle Posterior S e c t i o n Section

Modal Lesion Maximal Lesion Fig. 2. Reconstruction of hippocampal lesions.

484

JOHN W. GUSTAFSON

The present findings emphasize the utility o f distinguishing between measures of "distraction" and "reactivity" to a novel stimulus. The distinctive nature o f lesion effects upon orienting and upon exploration is indicated by the appearance of minimal lesion effects on exploration during consummatory behavior in the present experiment, whereas lesion effects on orienting were maximal under this condition in the experiments of Hendrickson et al., (1969).

REFERENCES Crowne, D. P., and Riddell, W. I. (1969). Hippocampal lesions and the cardiac component of the orienting response in the rat. J. Comp. PhysioL Psychol. 69, 748-755. Douglas, R. J. (1967). The hippocampus and behavior. Psychol. Bull. 67, 416-442. Douglas, R. J., and Pribram, K. H. (1969). Distraction and habituation in monkeys with limbic lesions. J. Comp. Physiol. Psychol. 69,473-480. Hendrickson, C. W., Kimble, R. J., and Kimble, D. P. (1969). Hippocampal lesions and the orienting response. J. Comp. Physiol. Psychol. 67, 220-227. Isaacson, R. L. (1974). "The Limbic System." New York: Plenum. Kaplan, J. (1968). Approach and inhibitory reactions in rats after bilateral hippocampal damage. J. Comp. Physiol. Psychol. 65, 274-281. Karmos, G., and Grasty~n, E. (1962). Influence of hippocampal lesions on simple and delayed conditioned reflexes. Acta Physiol. Acad. ScL Hung. 21, 215-224. Kimble, D. P. (1968). Hippocampus and internal inhibition. Psychol. Bull. 70, 285-295. Nadel, L. (1968). Dorsal and ventral hippocampal lesions and behavior. Physiol. Behav. 3, 891-900. Pribram, K. H., and MeGuinness, D. (1975). Arousal, activation and effort in the control of attention. PsychoL Rev. 82, 116-149. Raphelson, A. C., Isaacson, R. L., and Douglas, R. J. (1965). The effect of distracting stimuli on the runway performance of the limbic damaged rats. Psychon. Scl. 3, 483-484. Riddell, W., Rothblat, L., and Wilson, W. A., Jr. (1969). Auditory and visual distraction in hippocampectomized rats. J. Comp. Physiol. Psychol. 67, 216-219. Rogozea, R., and Ungher, J. (1968). Changes in orienting activity of cat induced by chronic hippocampal lesions. Exp. Neurol. 21, 176-186. Sanwald, J. C., Porzio, N. R., Deane, G. E., and Donovick, P. J. (1970). The effects of septal and dorsal hippocampal lesions on the cardiac component of the orienting response. Physiol. Behav. 5,883-888. Senba, K., and Iwahara, S. (1974). Effects of medial septal lesions on the hippocampal electrical activity and the orienting response to auditory stimulation in drinking rats. Brain Res. 66, 309-320. Sengstake, C. B. (1968). Habituation and activity patterns of rats with large hippocampal lesions under various drive conditions. J. Comp. Physiol. PsychoL 65, 504-506. Thompson, R. F., and Spencer, W. A. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 173, 16-43. Wickelgren, W. O., and Isaacson, R. L. (1963). Effect of the introduction of an irrelevant stimulus on runway performance of the hippocampectomized rat. Nature (London] 200, 48-50.

Distractibility and reactivity under different response conditions following hippocampal lesions in rats.

BEHAVIORAL BIOLOGY 15, 479-484 (1975), Abstract No. 5168 BRIEF REPORT Distractibility and Reactivity under Different Response Conditions Following Hi...
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