Operant discrimination of interoceptive urinary bladder stimulation in the monkey

Physiology and Behavior, Vol. 12, pp. 583-587. Brain Research Publications Inc., 1974. Printed in the U.S.A.

Operant Discrimination of Interoceptive Urinary Bladder Stimulation in the Monkey SUSAN S O L D O F F 3

Department of Psychology, California State College, Dominguez Hills, California 90747, U.S.A. AND H E N R Y SLUCKI 4

Department of Human Behavior, University of Southern California, School of Medicine, Los Angeles, California 90033, U.S.A. (Received 22 August 1973)

SOLDOFF, S. AND H. SLUCKI. Operant discrimination of interoceptive urinary bladder stimulation in the monkey. PHYSIOL. BEHAV. 12(4) 583-587, 1974. - The interoceptive stimulus of fluid in the urinary bladder of a female rhesus monkey was manipulated so as to function as a discriminative stimulus, such that lever-presses emitted in the absence of the stimulus (SD) were reinforced on FR 24, and those emitted in the presence of the stimulus (SA) were extinguished. Successful discrimination was achieved. Results were in agreement with those of previous research, in which stimulus onset was quickly discriminated but stimulus offset was not. Implications of visceral stimulus functions for basic psychophysiology and practical applications for the study and modification of behavior were considered. Operant discrimination Visceral perception

Interoceptive stimuli Biofeedback Urinary bladder Stimulus control Bladder control Toilet training

STIMULUS discrimination is established through differe n t i a l r e i n f o r c e m e n t contingencies. Most commonly, responses occurring only in the presence of a given stimulus are reinforced and extinguished in its absence. Thus, stimulus control is achieved when the discriminative stimulus (SD) sets the occasion for reliable responding and S a - the absence of SD - for its cessation. Until recently, studies of operant discrimination had utilized visual and auditory stimuli almost to the exclusion of all other Stimulus sources. This limitation for experimenting is due, in part, to methodological rather than theoretical considerations in that the reinforcement community - parents, experimenters, therapists, teachers, etc. - effectively arranges the management of contingencies for external (exteroceptive) stimuli but, lacking direct access to the individual's internal environment, cannot do so reliably for visceral (interoceptive) stimuli. Thus, the organism

Rhesus monkey

will perceive visceral stimuli only after reinforcement contingencies for responses to these internal events are established [ 16,18 ]. One very clear implication of the distinction and overlap between interoceptive and exteroceptive factors affecting behavior is the process of toilet training. At first, micturition occurs independently of any external factors, that is, regardless of place or time. When training is completed, however, the organism - discerning the presence of internal stimuli (urine in the bladder) - initiates a sequence or chain of responses postponing urination and terminating in the availability of an appropriate toilet facility. Thus, interoceptive discrimination of bladder stimuli has been achieved through the manipulation of appropriate and differential reinforcement contingencies - albeit with relative inefficiency [ 19 ]. Interoceptive conditioning was first demonstrated by

~This experiment was conducted in accordance with the American Psychological Association statement of "Guiding principles for the humane care and use of animals," December 15, 1962. 2We wish to express our gratitude to Robert W. Porter, M.D., Ph.D., for his generosity in allowing us the use of his laboratory, equipment and personnel at the Veterans Administration Hospital, Long Beach, California; to Nathan Fruehter, Frank B. McCoy, David F. Wright and Stephen K. Soldoff for assistance in the laboratory; and to William R. Christensen and Eleanor D. Kwong for photograph and manuscript preparation, respectively. 3This paper is based, in part, on research conducted by the first author, under the direction of the second author, in partial fulfillment of the Doctor of Philosophy degree at the University of Southern California. 4 Requests for reprints should be addressed to Henry Slucki. 583

584

SOLDOFF A N [ ) S I . [ ( K t

Soviet investigators using Pavlovian (respondent) techniques [1, 2, 12], and has been studied in the United States by operant conditioning procedures [ 3, 9, 13, 16, 17, 18 ]. The present experiment was designed to determine whether the interoceptive stimulus of fluid volume in the urinary bladder could be manipulated experimentally so as to function as a discriminative stimulus through differential reinforcement contingencies. METHOD

Animal An experimentally naive female rhesus monkey approximately four years of age, weighing 5.5 kg, was seated in a Foringer primate chair. She was maintained on a daily 22-hr food deprivation schedule, receiving a restricted regimen of approximately 50 g of laboratory monkey diet (Old Mother Hubbard Chimp Crackers) and half of an orange, half of an apple, and half of a banana 1/2 hr after the end of each experimental session, with ad lib access to water supplemented with Vi-Syneral multi-vitamin drops.

Apparatus The experimental chamber, previously described by Slucki et al. [16], was sound-attenuated, well-ventilated, and moderately illuminated. A one-way glass window allowed visual observation of behavior. The adjacent equipment room contained a Davis cumulative recorder, solidstate programmer, and the apparatus for bladder stimulation. Additional apparatus will be described below as applicable.

Procedure Operant conditioning. Reinforcement (Precision Food Pellets, P. J. Noyes Co.: dextrose 44.6 mg, starch 2.2 rag) was dispensed into a hopper near the monkey's chin. At the beginning of each daily experimental session a lever was placed 20 cm from the subject at waist level. A standard shaping procedure to bring about lever-pressing consisted of sequentially training the monkey: (a) to eat the pellets as quickly as they were delivered, (b) to move her paw closer and closer to the lever mechanism, and (c) gradually to press it more and more rapidly. After a relatively stable lever-pressing rate was achieved, an adjusting ratio schedule was instituted, requiring a greater number of responses for reinforcement. Eventually, a fixed ratio schedule requiring 24 responses for each pellet delivery (FR 24) was effected. Bladder stimulation and operant discrimination. After the response rate was stabilized, the daily procedure of bladder catheterization was introduced and continued throughout the experiment's duration. The bladder stimulus of Travenol normal saline, maintained at 37°C with heated water pumped through a condenser, was delivered and withdrawn at 2.5 cc/sec by a catheter (C. R. Bard, Foley, 14 French), using a pump, 50 cc glass syringe (B-D, Luer-lock) and polyethylene tubing (PE 100). The bladder pressure was monitored by a Beckman Dynograph through a transducer (Statham, Model P23Dc). The experimenter activated the pump manually by a toggle switch which automatically initiated the discrimination procedure and its appropriate contingencies. Lever-presses emitted after the actuation of the toggle switch for the syringe to begin feeding fluid to the bladder were extinguished (Sex), while those occurring after the actuation of the toggle switch for the

syringe to begin withdrawing fluid were reinforced on [ R 24 (SD). Thus, the SD consisted of (a) an empty bladder and (b) the time during which the fluid was being withdrawn; the S t` was (a) an experimentally specified volume of fluid in the bladder and (b) the time during which the fluid was being infused. St` duration was varied randomly from 2 to 30 min and SD from 0.5 to 6 rain. Daily sessions ranged from 30 rain to 2 hr. Discrimination training continued until the criterion of 10:1, SD/S/' response rate ratio, was exceeded. The amount of fluid infused was 20 cc initially and was incremented up to 40 cc in 10 cc steps whenever discrimination did not occur. After training at 40 cc the fluid quantity was reduced to 10 cc. Behavioral measures. The four dependent variables were:

(a}

SI) - - ratio Sex

=

Responses in S l)/minutes in SD Responses in St`/minutes in Sex

(b} Urinary bladder pressure change (PCD) = Mean pressure (mm Hg) over all St` segments of a daily session, based on one reading every 20 seconds, minus the mean pressure of the first SD of that session. (c) Response overshoot = Number of responses between S,a initiation and the first pause greater than 2 sec. (d) Response latency = Time in sec to first response following SD initiation. Daily routine. The daily routine consisted of: (a) prewarming the water-bath and saline and catheterizing the subject about 30 min prior to the experimental session, (b) preparing the infusion apparatus (including all necessary connections and calibrations), (c) preparing the behavioral control and recording apparatus, and (d) attaching the lever and pellet dispenser arrangement just prior to the initiation of the experimental run. Experimental precautions. The following precautions were taken to prevent bladder infections: (a) the catheter remained in the bladder for no longer than three hours daily, (b) the catheter was removed from the animal immediately after the termination of the experimental session and rinsed thoroughly, (c) the catheter was stored in a sterilizing solution of zephiran chloride, and (d) the syringe and tubing of the pump were flushed with fresh saline in preparation for the next experimental session at the end of each run. To minimize the effects of saline spray at a single locus on the bladder wall during stimulus presentation, a catheter with a two-holed tip and an infusion/withdrawal rate not exceeding 2.5 cc/sec were utilized~ RESULTS

The animal successfully discriminated 40 cc of fluid, since the criterion SD/SzX ratio of 10:1 was exceeded on three of five consecutive days. Overall means for SD/S A ratio, PCD, overshoot, and latency were calculated (Table 1). A Kruskat-Wallis one-way analysis of variance by ranks [ 14] was performed on each of the four measures (because of recorder failure at 20 cc, PC D comparisons of 30 cc and 40 cc only could be calculated). With the increase in volume from 20 to 30 to 40 cc, the animal shows significant trends for an increase in response ratio (p< 0.001 ), increase in PC D (p< 0.05 ), and decrease in overshoot (p<0.05), but with little corresponding change in latency. A typical sequence of behavior at 40 cc of fluid is shown in the cumulative record (Fig. 1). During the S D lever-pressing occurs at a steady rate followed by a small

OPERANT DISCRIMINATION OF URINARY BLADDER STIMULATION

585

TABLE 1 MEANS PER VOLUME AND CHI SQUARE FOR s D / s A RATIO, BLADDER PRESSURE, RESPONSE OVERSHOOT INTO S A AND TIME LATENCY INTO S D

Vol (cc) Measure

20

30

40

10

x ~*

p

s D / s A ratio

2.68

4.01

9.99

4.48

13.82

<0.001

-

54.23

57.39

49.58

6.27

<0.05

OS (#responses)

35.55

20.73

12.41

23.08

9.24

<0.02

LAT (sec)

14.40

15.60

12.00

12.60

1.98

PC D (mm Hg)

ns

*Statistical comparisons do not include the 10 cc values nor 20 cc for PC D (see text).

SO

Sa

SO

U~ UJ

Z 0 O. LU

0£

0 0

MIN /q/f/'////,,

~

//

~ " ' ~"~'~"~'~'~'~.....__

////////// .,,,~,J~,..,..,.~

1100ramHg

FIG. 1. Representative cumulative record (top) and corresponding bladder pressure record (bottom), once visceral discrimination has been established. The diagonal pips indicate reinforcement presented on FR .24 schedule. The bladder is empty for SD and the fluid stimulus for S a is 40 cc. Note the abrupt cessation of lever-pressing upon the introduction of fluid into the bladder (overshoot) and the longer latency between offset of the visceral stimulus and the resumption of lever-pressing.

586

SOLDOFF AND SI.UCKI

overshoot (less than 24 responses) after the onset of Sa. Pressing, which resumes shortly after SD is reintroduced, continues at a steady rate. The corresponding record shows the increase in bladder pressure at the beginning of Sa and the gradual reduction of this pressure as the bladder accommodates to the presence of the stimulus, presumably by smooth muscle relaxation through the sympathetic feedback system [6]. The large spikes which are riding on the basic bladder pressure curve are assumed to be skeletal muscle movement artifacts (Porter, Personal Communication, 1969). Spearman rank-order correlations [7] were performed for each amount of fluid volume on the following three comparisons: (a) time in each Sa segment versus the corresponding pressure change for the interval (PCI which in contrast to PCD, is computed as the mean pressure in each S A segment minus the mean pressure of the first SD of the daily session), (b) time in each S a segment versus the corresponding lever-pressing rate and (c) rate in each S A segment versus PC 1 (Table 2). There is a consistently significant relationship in all three comparisons: a decrease in PCI with an increase in time, an increase in rate with an increase in time, and an increase in rate with a decrease in PCI. It is apparent that 40 cc is the minimum fluid volume needed to provide the necessary PC D for discrimination to be established (Table 1). Since (a) the recordable pressure within the bladder varied due to contraction and relaxation (Fig. l) and (b) occasional FR extinction bursts (24 or more presses such that one reinforcement would be missed) were emitted during Sa, it may be that no discriminable difference exists between the pressure when the animal lever-pressed in S A and the resting pressure in SD. Thus, a more accurate description of threshold may be the pressure at that instant, rather than fluid volume specifications. Such threshold values were calculated as the mean pressure at the beginning of each FR burst in S A minus the mean pressure in the previous SD. The mean threshold value increases with the increase in volume but the standard deviation is highest at the lowest volumes (Table 3). DISCUSSION

The results of the present study clearly indicate that operant behavior may be brought under the control of an interoceptive stimulus originating in the urinary bladder [ 18]. They confirm our earlier findings that (1) visceral events may come to serve as SD's when appropriate reinforcement contingencies have been established and (2) the onset of visceral stimulation is discriminated earlier than its termination [9, 16, 17]. After unsuccessful attempts with fluid at 20 and 30 cc, discrimination was established easily with 40 cc. However, a test probe with 10 cc of fluid, after the behavioral criterion had been achieved, generated differential responding (Table 1, Column for 10 cc). Thus, through stimulus generalization an intensity that previously had not been discriminated gained a stimulus control function. This finding is virtually identical to our earlier report [9,17] in which extensive training failed to achieve discrimination of a visceral stimulus, increasing its intensity resulted in its establishment as an SD. Subsequent testing with the previously ineffective stimulus resulted in its being discriminated easily. In the present study, the SD consisted of an empty bladder or the condition of bladder emptying and the S A was the presence of fluid in the bladder; that is, stimulus ON

TABLE 2 C O R R E L A T I O N OF TIME (T), PRESSURE (P), ANI) RESPONSE RATE (R) DURING BLADDER STIMULATION (S A)

rS

Vol (cc)~c

N

T vs P

R vs P

T vs P

10

28

-0.35 t

-0.02

0.39-~

30

20

-0.81 *

-0.68*

0.76*

40

21

-0.68*

-0.47 t

0.54*

*p<0.01 tp<0.05 SNo pressure recordings taken at 20 cc (see text)

TABLE 3 MEANS AND STANDARD DEVIATIONS OF THRESHOLD B L A D D E R PRESSURE (mm Hg) VALUES AT S A FR BURSTS

Vol (cc)*

Mean

SD

10

14.42

10.92

30

23.66

5.05

40

30.85

7.62

*No pressure recordings taken at 20 cc (see text) was the S 'x and stimulus OFF, the SD. Thus, the overshoot, recorded as the total number of responses emitted in S,a prior to the first pause of at least 2 sec, occurred during fluid infusion into the bladder. The overshoot values dropped as training progressed, falling below 24 presses, thus suggesting that response cessation was due to the presence of the stimulus rather than a missed reinforcement. This distinction previously [9, 16, 17] had been ambiguous, since the number of overshoot responses exceeded that necessary for delivery of a reinforcer. Latency, the time between the initiation of SD and the first lever-press, was recorded during the withdrawal of fluid from the bladder. It remained constant across volumes at approximately 12 to 15 sec. In our earlier research [9, 16, 17] on the large and small intestines, rhythmic inflation and deflation of a balloon at 1 Hz was the SD and its absence was the S A. Discrimination reversal results [16] were identical to the overshoot and latency data obtained in the present study. Thus, as a general characteristic of visceral stimulation, the onset is more quickly discriminated than the offset. With respect to the urinary bladder, a possible explanation is provided by the activity of the sympathetic feedback loop. It is evident that the removal of the stimulus when the bladder is already in a somewhat relaxed state is not as

OPERANT DISCRIMINATION OF URINARY BLADDER STIMULATION readily perceived as the introduction of the stimulus into a bladder which is empty. Also, it is possible that skeletal muscles provide a source of extraneous stimulation which interferes with visceral learning [4, 5, 10]. It is important to note that, with the passage of time in S a , reflexive relaxation of the bladder resulted in leverpressing bursts. Correspondingly high and low pressure recordings were evident, thus producing non-reinforced responses in what physiologically would be SD conditions. Comparing the mean threshold values (Table 3 ) t o PC D (Table 1) for each volume reveals that the controlling stimulus intensity may be a pressure well below that produced by 40 cc of fluid volume. Rather than specifying the volume of fluid, it would have been more appropriate to manipulate pressure as the independent variable, since that was the significant stimulus dimension for discrimination. In addition to methodological considerations, this fact has implications for applied human behavior, for example, in the area of toilet training. It is in this line of reasoning that Adam states, "interoceptive impulses inform the higher centres about conditions which necessitate active operant r e s p o n s e s . . . The transmission of stimuli concerning micturition and defecation is an important task of the interoceptive system" ([1] pp. 1 3 6 - 3 7 ) . Most parents assume that a linear relation exists between bladder pressure, the adequate stimulus for the behavior of urination, and time. This assumption, of course, is unwarranted because of the relaxation reflex in the bladder. Rather, there is an approximately linear relation between urine volume and time, but a more complex function for bladder pressure and time. Thus, reminding a yet-to-be trained child that it is time to

587

urinate may produce a negative response from the child, even though there may be a considerable volume of urine in the (relaxed) bladder. It may be argued that the manner in which these stimuli are discerned is precisely according to the discrimination paradigm suggested in the present study. What is needed is that the internal " . . . environment needs to be coordinated with the external environment by whatever means can be contrived in order that a scientific account of the stimulus control of the organism may be completed" ([8] p. 134). Many external SD's, such as appropriate toilet facilities, verbal instructions, and absence of clothing, combined with various reinforcers, have been incorporated as necessary SD's in the genesis and maintenance of this very complex chain of events which result in the behavioral pattern of toilet training. Because parents are unable to observe directly the state of the bladder pressure at any given moment, training of young children is difficult and inefficient. Enuresis, especially the nocturnal type, may be viewed as a failure in bladder discrimination training. Such an approach suggests an explanation for the behavioral intervention which has been shown [18] to be effective therapeutically. Miller [11] agrees that visceral afferent impulses may play an important role in the control of overt behavior and in behavioral rehabilitation, by training a patient to discern small changes in visceral functions. Skinner asserts, "The new evidence simply points to the fact that what is experienced introspectively is a physical condition of the body, as a behavioristic theory of knowledge has always contended" ([15] p. 262).

REFERENCES

1. ,~d~m, G. Interoception and Behavior. Budapest: Akademiai Kiado, 1967. 2. Bykov, K. M. The Cerebral Cortex and the Internal Organs. (Translated by R. Hodes). Moscow: Foreign Languages Publishing House, 1959. 3. Cook, L., A. Davidson, D. J. Davis and R. T. Kelleher. Epinephrine, norepinephrine, and acetylcholine as conditioned stimuli for avoidance behavior. Science 131: 990-991, 1960. 4. DiCara, L. V. and N. E. Miller. Heart rate learning in the noncurarized state, transfer to the curarized state, and subsequent retraining in the noncurarized state. Physiol. Behav. 4: 621-624, 1969. 5. DiCara, L. V. and J. M. Weiss. Effect of heart-rate learning under curare on subsequent noncurafized avoidance learning. J. comp. physiol. Psychol. 69: 368-374, 1969. 6. Edvardsen, P. Nervous control of urinary bladder in cats I. The collecting phase. Acta physiol, scand. 72: 157-171, 1968. 7. Hays, W. L. Statistics for Psychologists. New York: Holt, Rinehart, and Winston, 1963. 8. Hefferline, R. F. Learning theory and clinical psychology - an eventual symbiosis. In: Experimental Foundations of Clinical Psychology, edited by A. J. Bachrach. New York: Basic Books, 1962, pp. 97-138. 9. McCoy, F. B. Operant discrimination of a mechanical stimulus in the colon. Masters Thesis, University of Southern California, 1968.

10. Miller, N. E. Learning of visceral and glandular responses. Science 163: 434-445, 1969. 11. Miller, N. E. Learning of glandular and visceral responses. In: Current Status o f Physiological Psychology, edited by D. Singh and C. T. Morgan. Monterey, California: Brooks/Cole, 1972, pp. 228-250. 12. Razran, G. The observable unconscious and the inferable conscious in current Soviet psychophysiology: Interoceptive conditioning, semantic conditioning, and the orienting reflex. Psychol. Rev. 68: 81-147, 1961. 13. Schuster, C. R. and J. V. Brady. The discriminative control of a food reinforced operant by interoceptive stimulation. I. P. Pavlov Z higher nerv. Activ. 14: 448-458, 1964. 14. Siegel, S. Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill, 1956. 15. Skinner, B. F. Contingencies of Reinforcement: A Theoretical Analysis. New York: Appleton-Century-Crofts, 1969. 16. Slucki, H., G. Adam and R. W. Porter. Operant discrimination of an interoceptive stimulus in rhesus monkeys. J. expl anal. Behav. 8: 405-414, 1965. 17. Slucki, H., F. B. McCoy and R. W. Porter. Interoceptive sD of the large intestine established by mechanical stimulation. Psychol. Rep. 24: 35-42, 1969. 18. S°ld°ff' S" Operant discriminati°n °f an inter°ceptive stimulus in the urinary bladder of intact and dorsal root transected female rhesus monkeys. Unpublished doctoral dissertation, University of Southern California, 1971. 19. Yates, A. J. Behavior Therapy. New York: Wiley, 1970.