- Email: [email protected]
Two self-shaping methods for intracranial self-stimulation in rats
Physiology & Behavior, Vol. 18, pp. 721-723. Pergamon Press and Brain Research Publ., 1977. Printed in the U.S.A.
BRIEF COMMUNICATION Two Self-Shaping Methods for Intracranial Self-Stimulation in Rats G. T. POLLARD, N. E. HARTO, K. W. ROHRBACH AND J. L. HOWARD Wellcome Research Laboratories, Research Triangle Park, N.C. (Received 1 June 1976) POLLARD, G. T., N. E. HARTO, K. W. ROHRBACH AND J. L. HOWARD. Two self-shaping methods for intracranial self-stimulation in rats. PHYSIOL. BEHAV. 18(4) 721-723, 1977. - Shaping an animal for intracranial self-stimulation (ICSS) by manual reinforcement of successive approximations to the desired response can be tedious and time-consuming and may produce inappropriate behaviors. To test alternative shaping methods, rats were implanted with bipolar electrodes aimed at the medial forebrain bundle; one group was shaped manually, another group was allowed to acquire the bar-press response for food reward before implantation and then ICSS was substituted for food, and a third group was allowed to shape themselves spontaneously for ICSS through exploratory behavior. It was concluded that spontaneous shaping produces stable responders with less investment of time and expertise than do the other two methods. Intracranial self-stimulation
Medial forebrain bundle
Operant conditioning
SHAPING an animal for intracranial self-stimulation (ICSS) by manual reinforcement of successive approximations to the desired response can be tedious and time-consuming and may produce inappropriate or stimulus-bound behaviors. The early literature on ICSS suggested that manual shaping was unnecessary in many experimental situations, that rats would in fact shape themselves during exploratory behavior. Olds [3 ] connected the stimulus switch to a large pedal placed in such a way that the rat would press it spontaneously 10 to 50 times per hour while exploring a light source; this method yielded rewarded response rates of 500 to 7000 [4] for the first hour of self-shaping. Yet manual shaping is still used, and shaping periods of up to 15 daily sessions have been reported for rats implanted in dorsal brain stem and hypothalamus [ 2]. To explore the relative efficiency of various shaping procedures, one group of rats was allowed to shape themselves essentially by the Olds method and another group was allowed to acquire the desired response by bar-pressing for food, after which ICSS was substituted for the food reward. These self-shaped groups were compared to each other and to a group of rats shaped manually to determine whether the different shaping procedures produced differences in time required for achieving stable response rates. METHOD
Animals and Surgery Male Long-Evans rats ( 2 8 0 - 4 8 0 g) from Blue Spruce 721
Farms, Altamont, N.Y., were anesthetized with sodium pentobarbital (50 mg/kg IP), placed in a Kopf stereotaxic apparatus, and implanted with a bipolar electrode aimed at the left medial forebrain bundle at the level of the lateral hypothalamus according to coordinates derived from Pellegrino and Cushman [5] - 0.5 mm posterior and 1.6 mm lateral to Bregma, and 8 .8 - 9 .1 mm below skull surface.
Apparatus and Procedure Sine wave stimulation at 60 Hz was provided by a Microtronics constant current source and brought to the animal through a mercury commutator. Each stimulus was 250 msec in duration for the spontaneous and food-pretrained groups, 300 msec for the manually-shaped group; this difference in train duration was considered to be of little or no significance, since it has been shown that a 500 msec train produces only a slight increase in preference in a choice test and a slight decrease in bar-pressing rate when compared to a 250 msec train [1]. Intensities used in shaping were in general 50 #A for the manually-shaped and food-pretrained groups; a variable intensity schedule with a mean of 60 btA was used for the spontaneous group. Testing was carried out in a Coulbourn enclosure with a single bar. Criterion for stability in bar-pressing rate was consistency within 20 percent of the mean number of responses on 3 consecutive days at the same intensity. For those animals on a variable intensity schedule, the intensity one step below maximum was selected for criterion purposes. For rats conditioned to bar-press for food, Coulbourn
722
POLLARD, HARTO, ROHRBACH AND HOWARD
operant chamber equipped with a single bar, pellet dispenser (Noyes 45 mg pellets), and water bottle was used. Rats were placed in the chamber on a continuous reinforcement (CRF) schedule. After 30 min had elapsed, if the rat had performed 30 responses, he was switched to a fixed ratio 2 schedule; if he had not performed 30 responses, he remained on the CRF schedule for another 30 min. Once the rat had entered the ratio portion of the schedule, his performance was evaluated every 15 min; if he received 15 reinforcements in 15 min, his ratio of responses to reinforcement was incremented by 1. All behavior events were programmed, and data acquired, via a NOVA 2/10 computer and an Interact interface. Manually-shaped group. Thirteen naive rats were implanted and allowed an average of 10 days to recover from surgery. They were given daily shaping sessions 1 0 - 4 0 min in duration. After being shaped to bar-press at 50/IA, most animals were run on a variable intensity schedule, 1 hr per session, one session per day, with all intensities set at 50/aA for the first session; intensities were varied step-wise (e.g., 4 0 - 6 0 /2A) for the second session, and by the third or fourth session most animals were being run on the intensities at which they eventually stabilized, 3 0 - 7 0 or 4 0 - 8 0 /2A. Two priming stimuli at the middle intensity were delivered at the beginning of each 1-hr session, and each change in intensity (every 2 rain) was signaled by a priming stimulus at that intensity. Food-pretrained group. Nineteen naive rats were given an average of 3.1 12-hr sessions, one session per night, on a CRF/progressive ratio schedule with food reward;criterion was ratio 9. After implantation and an average recovery period of 7 days, each animal was placed in the selfstimulation chamber with intensity set at 50/IA, given two priming stimuli, and monitored visually until he began to bar-press repeatedly or 10 min had elapsed, after which a 10-min scored interval was begun. Criterion was 100 responses in 10 min. On succeeding days identical 10-min runs were given, one per day, except that runs were preceded by 4 rain in the test chamber with cue lights and stimulator turned off, then 6 min in which responses were rewarded but not recorded. Animals were not routinely starved before self-shaping. Spontaneously-shaped group. Eleven naive rats were implanted and allowed an average of 10 days to recover from surgery. Each animal was placed in the self-stimulation chamber for 12 consecutive hours with 10 priming
stimuli at the beginning of each hour and 1 priming stimulus to signal the change of intensity every 2 min; one of the 11 failed to reach criterion during the first session and was given a second 12-hour training session. Animals were then placed on a daily 20-rain schedule consisting of two consecutive 10-rain variable intensity blocks at 4 0 - 8 0 /2A preceded by 4 min with stimulator and cue lights turned off. On succeeding days intensities for the 20 rain sessions were reduced to 30 70 or 2 0 - 6 0 /IA in most cases. RESULTS AND DISCUSSION Mean times required for shaping and stabilizing of responsive animals are given in Table 1. Two of the 8 responsive rats in the manually-shaped group of 13 became stimulus-bound to manually-delivered electrical stimulation. That is, the animals would not self-start or restart after time-outs, although they were excited and exhibited gnawing behavior during shaping and would self-stimulate at high rates when given extra priming stimuli. Histological examination showed electrode placement to be correct. Eight of the 19 rats pretrained on food reached ICSS self-shape criterion in the first session, two in the second session, two in the third, and another in the fifth after being starved. The remaining 6 animals, having failed to respond after starvation and manual stimulation, were discarded. Of the 1 1 rats in the spontaneous group, 2 shaped themselves within the first hour, 4 in the second, 3 in the third, and 1 in the seventh. The remaining rat reached criterion in the sixth hour of the second nightly session; although he did eventually stabilize at the low response rate, he was judged marginally useful and his data are excluded from Table 1. We found no significant differences among groups in performance after stabilizing. The three groups, trained at different times for different ultimate uses, were required to stabilize on somewhat different schedules; thus strict comparisons among groups would be inappropriate. However, for two reasons, we feel that shaping method accounts for a significant amount of the observed difference in stabilizing times. First, the manually-shaped group had the longest stabilizing sessions (1 hour) incorporating both single and variable intensity programs, yet they required more stabilizing time than did
TABLE 1 TIMES REQUIRED FOR SHAPING A N D STABILIZING OF RESPONSIVE RATS ( M E A N S _+ SE)
Group Manually-shaped (N = 6) Food-pretrained, self-shaped (N = 13) Spontaneously self-shaped (N = 10)
No. days pretraining (food)
--
2.6 _+ 0.2 --
No. shaping days
Shaping time (hrs)
2.0 ___0.3 1.8 _+ 0.3
0.7*
1.0 +_ 0 . 0
*Estimated by the experimenter who shaped the animals.
No. stabilizing days
Percent of implanted rats reaching stability 46
0.6 _+ 0.1
11.5 _+ 1.9 6.8 _+ 1.2
2.6 +_ 0.5
3.4 +_ 0.2
91
68
TWO SELF-SHAPING METHODS F O R ICSS
723
the groups with shorter sessions (16 minutes of single intensity for food pretrained, 20 minutes of variable intensity for spontaneous). Second, stabilizing times for some manually-shaped rats mentioned in the literature are of the same order as times required by our manually-shaped group. Furthermore, shaping method may account for some of the difference in percentage of implanted animals which self-stimulated; the possibility is worth considering that self-shaping not only eliminates the sort of stimulusbound behavior described but also increases the probability
that a rat will in fact acquire the bar-press response for ICSS. In summary, self-shaping produced reliable responders more efficiently than did manual shaping, and without requiring the time and effort of a skilled shaper. Thus for routine production spontaneous self-shaping seems the method of choice. As for the food-pretraining method, which requires 2 or 3 days on CRF/progressive ratio before beginning ICSS, it was a first step away from manual shaping and can be dismissed for most purposes.
REFERENCES 1. Beyra, M. The measurement of reinforcing brain stimulation. Brain Res. 70: 467-479, 1974. 2. Ellman, J., R. F. Ackermann, J. Bodnar, F. Jackler and S. Steiner. Comparison of behaviors elicited by electrical brain stimulation in dorsal brain stem and hypothalamus of rats. J. cornp, physiol. Psychol. 88: 816-828, 1975. 3. Olds, J. Self-stimulation of the brain: its use to study local effects of hunger, sex, and drugs. Science 127: 315-324, 1958.
4. Olds, J., R. P. Travis and R. C. Schwing. Topographic organization of hypothalamic self-stimulation functions. J. comp. physiol. Psychol. 53: 23-31, 1960. 5. Pellegrino, L. J. and A. J. Cushman. A Stereotaxic Atlas o f the Rat Brain. New York: Appleton-Century-Crofts, 1967.
BRIEF COMMUNICATION Two Self-Shaping Methods for Intracranial Self-Stimulation in Rats G. T. POLLARD, N. E. HARTO, K. W. ROHRBACH AND J. L. HOWARD Wellcome Research Laboratories, Research Triangle Park, N.C. (Received 1 June 1976) POLLARD, G. T., N. E. HARTO, K. W. ROHRBACH AND J. L. HOWARD. Two self-shaping methods for intracranial self-stimulation in rats. PHYSIOL. BEHAV. 18(4) 721-723, 1977. - Shaping an animal for intracranial self-stimulation (ICSS) by manual reinforcement of successive approximations to the desired response can be tedious and time-consuming and may produce inappropriate behaviors. To test alternative shaping methods, rats were implanted with bipolar electrodes aimed at the medial forebrain bundle; one group was shaped manually, another group was allowed to acquire the bar-press response for food reward before implantation and then ICSS was substituted for food, and a third group was allowed to shape themselves spontaneously for ICSS through exploratory behavior. It was concluded that spontaneous shaping produces stable responders with less investment of time and expertise than do the other two methods. Intracranial self-stimulation
Medial forebrain bundle
Operant conditioning
SHAPING an animal for intracranial self-stimulation (ICSS) by manual reinforcement of successive approximations to the desired response can be tedious and time-consuming and may produce inappropriate or stimulus-bound behaviors. The early literature on ICSS suggested that manual shaping was unnecessary in many experimental situations, that rats would in fact shape themselves during exploratory behavior. Olds [3 ] connected the stimulus switch to a large pedal placed in such a way that the rat would press it spontaneously 10 to 50 times per hour while exploring a light source; this method yielded rewarded response rates of 500 to 7000 [4] for the first hour of self-shaping. Yet manual shaping is still used, and shaping periods of up to 15 daily sessions have been reported for rats implanted in dorsal brain stem and hypothalamus [ 2]. To explore the relative efficiency of various shaping procedures, one group of rats was allowed to shape themselves essentially by the Olds method and another group was allowed to acquire the desired response by bar-pressing for food, after which ICSS was substituted for the food reward. These self-shaped groups were compared to each other and to a group of rats shaped manually to determine whether the different shaping procedures produced differences in time required for achieving stable response rates. METHOD
Animals and Surgery Male Long-Evans rats ( 2 8 0 - 4 8 0 g) from Blue Spruce 721
Farms, Altamont, N.Y., were anesthetized with sodium pentobarbital (50 mg/kg IP), placed in a Kopf stereotaxic apparatus, and implanted with a bipolar electrode aimed at the left medial forebrain bundle at the level of the lateral hypothalamus according to coordinates derived from Pellegrino and Cushman [5] - 0.5 mm posterior and 1.6 mm lateral to Bregma, and 8 .8 - 9 .1 mm below skull surface.
Apparatus and Procedure Sine wave stimulation at 60 Hz was provided by a Microtronics constant current source and brought to the animal through a mercury commutator. Each stimulus was 250 msec in duration for the spontaneous and food-pretrained groups, 300 msec for the manually-shaped group; this difference in train duration was considered to be of little or no significance, since it has been shown that a 500 msec train produces only a slight increase in preference in a choice test and a slight decrease in bar-pressing rate when compared to a 250 msec train [1]. Intensities used in shaping were in general 50 #A for the manually-shaped and food-pretrained groups; a variable intensity schedule with a mean of 60 btA was used for the spontaneous group. Testing was carried out in a Coulbourn enclosure with a single bar. Criterion for stability in bar-pressing rate was consistency within 20 percent of the mean number of responses on 3 consecutive days at the same intensity. For those animals on a variable intensity schedule, the intensity one step below maximum was selected for criterion purposes. For rats conditioned to bar-press for food, Coulbourn
722
POLLARD, HARTO, ROHRBACH AND HOWARD
operant chamber equipped with a single bar, pellet dispenser (Noyes 45 mg pellets), and water bottle was used. Rats were placed in the chamber on a continuous reinforcement (CRF) schedule. After 30 min had elapsed, if the rat had performed 30 responses, he was switched to a fixed ratio 2 schedule; if he had not performed 30 responses, he remained on the CRF schedule for another 30 min. Once the rat had entered the ratio portion of the schedule, his performance was evaluated every 15 min; if he received 15 reinforcements in 15 min, his ratio of responses to reinforcement was incremented by 1. All behavior events were programmed, and data acquired, via a NOVA 2/10 computer and an Interact interface. Manually-shaped group. Thirteen naive rats were implanted and allowed an average of 10 days to recover from surgery. They were given daily shaping sessions 1 0 - 4 0 min in duration. After being shaped to bar-press at 50/IA, most animals were run on a variable intensity schedule, 1 hr per session, one session per day, with all intensities set at 50/aA for the first session; intensities were varied step-wise (e.g., 4 0 - 6 0 /2A) for the second session, and by the third or fourth session most animals were being run on the intensities at which they eventually stabilized, 3 0 - 7 0 or 4 0 - 8 0 /2A. Two priming stimuli at the middle intensity were delivered at the beginning of each 1-hr session, and each change in intensity (every 2 rain) was signaled by a priming stimulus at that intensity. Food-pretrained group. Nineteen naive rats were given an average of 3.1 12-hr sessions, one session per night, on a CRF/progressive ratio schedule with food reward;criterion was ratio 9. After implantation and an average recovery period of 7 days, each animal was placed in the selfstimulation chamber with intensity set at 50/IA, given two priming stimuli, and monitored visually until he began to bar-press repeatedly or 10 min had elapsed, after which a 10-min scored interval was begun. Criterion was 100 responses in 10 min. On succeeding days identical 10-min runs were given, one per day, except that runs were preceded by 4 rain in the test chamber with cue lights and stimulator turned off, then 6 min in which responses were rewarded but not recorded. Animals were not routinely starved before self-shaping. Spontaneously-shaped group. Eleven naive rats were implanted and allowed an average of 10 days to recover from surgery. Each animal was placed in the self-stimulation chamber for 12 consecutive hours with 10 priming
stimuli at the beginning of each hour and 1 priming stimulus to signal the change of intensity every 2 min; one of the 11 failed to reach criterion during the first session and was given a second 12-hour training session. Animals were then placed on a daily 20-rain schedule consisting of two consecutive 10-rain variable intensity blocks at 4 0 - 8 0 /2A preceded by 4 min with stimulator and cue lights turned off. On succeeding days intensities for the 20 rain sessions were reduced to 30 70 or 2 0 - 6 0 /IA in most cases. RESULTS AND DISCUSSION Mean times required for shaping and stabilizing of responsive animals are given in Table 1. Two of the 8 responsive rats in the manually-shaped group of 13 became stimulus-bound to manually-delivered electrical stimulation. That is, the animals would not self-start or restart after time-outs, although they were excited and exhibited gnawing behavior during shaping and would self-stimulate at high rates when given extra priming stimuli. Histological examination showed electrode placement to be correct. Eight of the 19 rats pretrained on food reached ICSS self-shape criterion in the first session, two in the second session, two in the third, and another in the fifth after being starved. The remaining 6 animals, having failed to respond after starvation and manual stimulation, were discarded. Of the 1 1 rats in the spontaneous group, 2 shaped themselves within the first hour, 4 in the second, 3 in the third, and 1 in the seventh. The remaining rat reached criterion in the sixth hour of the second nightly session; although he did eventually stabilize at the low response rate, he was judged marginally useful and his data are excluded from Table 1. We found no significant differences among groups in performance after stabilizing. The three groups, trained at different times for different ultimate uses, were required to stabilize on somewhat different schedules; thus strict comparisons among groups would be inappropriate. However, for two reasons, we feel that shaping method accounts for a significant amount of the observed difference in stabilizing times. First, the manually-shaped group had the longest stabilizing sessions (1 hour) incorporating both single and variable intensity programs, yet they required more stabilizing time than did
TABLE 1 TIMES REQUIRED FOR SHAPING A N D STABILIZING OF RESPONSIVE RATS ( M E A N S _+ SE)
Group Manually-shaped (N = 6) Food-pretrained, self-shaped (N = 13) Spontaneously self-shaped (N = 10)
No. days pretraining (food)
--
2.6 _+ 0.2 --
No. shaping days
Shaping time (hrs)
2.0 ___0.3 1.8 _+ 0.3
0.7*
1.0 +_ 0 . 0
*Estimated by the experimenter who shaped the animals.
No. stabilizing days
Percent of implanted rats reaching stability 46
0.6 _+ 0.1
11.5 _+ 1.9 6.8 _+ 1.2
2.6 +_ 0.5
3.4 +_ 0.2
91
68
TWO SELF-SHAPING METHODS F O R ICSS
723
the groups with shorter sessions (16 minutes of single intensity for food pretrained, 20 minutes of variable intensity for spontaneous). Second, stabilizing times for some manually-shaped rats mentioned in the literature are of the same order as times required by our manually-shaped group. Furthermore, shaping method may account for some of the difference in percentage of implanted animals which self-stimulated; the possibility is worth considering that self-shaping not only eliminates the sort of stimulusbound behavior described but also increases the probability
that a rat will in fact acquire the bar-press response for ICSS. In summary, self-shaping produced reliable responders more efficiently than did manual shaping, and without requiring the time and effort of a skilled shaper. Thus for routine production spontaneous self-shaping seems the method of choice. As for the food-pretraining method, which requires 2 or 3 days on CRF/progressive ratio before beginning ICSS, it was a first step away from manual shaping and can be dismissed for most purposes.
REFERENCES 1. Beyra, M. The measurement of reinforcing brain stimulation. Brain Res. 70: 467-479, 1974. 2. Ellman, J., R. F. Ackermann, J. Bodnar, F. Jackler and S. Steiner. Comparison of behaviors elicited by electrical brain stimulation in dorsal brain stem and hypothalamus of rats. J. cornp, physiol. Psychol. 88: 816-828, 1975. 3. Olds, J. Self-stimulation of the brain: its use to study local effects of hunger, sex, and drugs. Science 127: 315-324, 1958.
4. Olds, J., R. P. Travis and R. C. Schwing. Topographic organization of hypothalamic self-stimulation functions. J. comp. physiol. Psychol. 53: 23-31, 1960. 5. Pellegrino, L. J. and A. J. Cushman. A Stereotaxic Atlas o f the Rat Brain. New York: Appleton-Century-Crofts, 1967.