Air drinking by partially ageusic rats

Physiology and Behavior. Vol. 7, pp. 759-761. Pergamon Press, 1971. Printed in Great Britain

Air Drinking by Partially Ageusic Rats' C. K. F O S S E T T , JR. A N D F. R. T R E I C H L E R

Department of Psychology, Kent State University, Kent, Ohio, U.S.A. (Received 8 S e p t e m b e r 1971) FOSSETT,C. K. JR. AND F. R. T~ICnLER, Air-drinkingby partially ageusic rats. PHYSIOL.BEHAV. 7 (5) 759-761, 1971.I An evaluation of the effects of partial conduction ageusia on licking an air-stream was undertaken. Rats with bilateral lingual nerve divisions showed significant reductions in pre to post-operative air-drinking rates, while neither rats with severed glossopharyngeal nerves, nor sham operated controls exhibited similar outcomes. Interruption of some sensory input associated with the physical characteristics of an air-stream appeared to exert partial control over responding for air. Non-nutritive reinforcers

Thirst

Rats

HENDRY AND RASCHE [3] have demonstrated that thirsty rats will lick at a stream of air emanating from a standard metal drinking tube. This behavior, which has been described as air-drinking, appears to reduce subsequent water consumption, perhaps by serving as a substitute for some consummatory behavior associated with the alleviation of thirst. However, satiation of air-drinking appears transitory. Williams, Treichler and Thomas [10] have shown that the satiating effect of ad lib air on subsequent air-drinking was almost completely dissipated within 30 min, and it was suggested that air-drinking provides immediate oral stimulation, paralleling the oral stimulation of fluid ingestion. Experiments attempting to influence rates of air-drinking through the manipulation of the physical characteristics of the air stream have been reported by Treichler and Riccio [7]. Their data and a later report of Oatley and Dickinson [4] have indicated that the rate of air-drinking may be affected by varying the pressure of the air which serves as the reinforcing agent. Such findings suggest that sensory input from oropharyngeal receptors might be manipulated to modify the reinforcing consequences of an air stream. Physiological manipulation of input from the oral cavity might be achieved in at least two ways: (1) through interruption of the oral sensory nervous system either centrally or peripherally, or (2) by changing the physiological conditions of the oral cavity. Chillag and Mendelson [1] have reported that the rate of air-drinking in desalivate rats was initially lower than in normal rats, and that air-licking quickly extinguished almost completely for desalivates. Other airdrinking research utilizing peripheral physiological manipulation appears to be absent in the literature; however, such techniques have been used successfully in experiments dealing with taste preferences and food or water intakes [5, 8, 9]. The present experiment employed the research tactic of peripheral denervation in an attempt to define some pathways which provide the sensory characteristics of a stream of air. Specifically, the effect of bilateral divisions of the

lingual or glossopharyngeal nerves, upon rate of air-drinking was assessed. METHOD

Twenty-four experimentally naive, adult male hooded rats of the Long-Evans strain were used. The apparatus for the measurement of air-drinking consisted of a 26.5 x 26.5 x 30.0 cm. clear plexigias box with a mesh floor. A stainless steel drinking tube with a 122 mm 2 orifice protruded 1 em into the box, and was centered on one wall 5 cm above the floor. Compressed air was passed through a filtered moisture trap and then led into a solenoid valve which could be activated, via a Grason-Stadler Drinkometer, by discrete contacts with the drinking tube. The velocity of air delivered was 20.67 meters/see at the orifice. Each contact allowed delivery of a puff of air for 0.5 see, and the number of contact responses (licks) was counted electrically. A separate apparatus for the measurement of water-drinking was comprised of a 26 x 26 z 30 cm black wooden box with a stainless steel drinking tube protruding 1 cm into the box, 5 cm above the floor. Each lick at the drinking tube activated a solenoid valve which opened for 0.02 see allowing approximately 0.017ml of gravity fed distilled water to be delivered to the tube. The number of contact responses (licks) was counted electrically. Since the air- and water-drinking boxes were apparently dissimilar (clear plastic vs. black wood), it was assumed that they would be discriminably different to hooded rats, and that generalized reinforcing effects would be minimized. The ad lib weights for all rats were recorded for 3 days, and the mean weight for each was calculated; subsequently, each rat was reduced to and maintained at 85 per cent of its mean ad lib weight via water deprivation. Then, on alternate days, rats were given 2 ½-hr adaptation training sessions in the air-drinking apparatus. This consisted of an initial provision of a constant air stream followed by intermittent air deliveries which were manipulated such that animals

IThis work was partially supported by National Science Foundation grant GZ-213 to the first author, and National Institutes of Health grant MH-12934 to the second author. We are indebted to Dr. William B. Vance of Indiana University for instruction in necessary surgical procedures and for the suggestion of the lesion sites. 759

760

FOSSETT AND TREICHI [!R

learned to make discrete tube contacting responses I~r each puff of air. Analogous procedures were employed on opposite days for water-drinking adaptation, and all rats readily licked at the tubes in both the air- and water-drinking apparatuses. The animals were then randomly divided into 3 groups of 8 rats, and half of each of the groups was assigned to begin testing with air, and the other half with water. Testing consisted of assessing each rat's air-drinking for 15 rain or water-drinking for 5 rain, using one test session per day. Air- and water-drinking were assessed on alternate days, and each rat was tested for a total of 4 sessions. Throughout this period, animals were maintained via water rationing at 85 per cent of their pre-deprivation weights. After the last test, each rat was allowed free access to both food and water tmtil the following day, when the surgical manipulation was undertaken. Post-operatively, all rats received a 10-day recovery period with free access to food and water. Following recovery, all rats were deprived of water until they reached 85 per cent of their post-operative ad lib weights. Readaptation and retesting were then undertaken, using procedures like those in original adaptation and testing. Surgical procedures were performed under a general anesthetic (sodium secobarbital, 50 mg/Kg). Animals received either bilateral divisions of the lingual nerve (Group V), bilateral lesions of the gtossopharyngeal nerve (Group IX), or had both the lingual and glossopharyngeal nerves revealed bilaterally without neuronal section (Group CTL). The use of the designation "Group V" is not meant to indicate that this nerve section included only components of the fifth cranial nerve. Indeed, since the site of the lesion was distal to the junction of the fifth and seventh cranial nerves (see Fig. 1) the latter's chorda tympani component was certainly severed. This site was chosen in order to

eliminate those taste afferents which have been speculated to travel via the greater superficial petrosal nerve [6]. The locations of the divisions of the lingual and glossopharyngcal nerves are presented in Fig. l and 2. Since all post-operative testing was completed within 20 days after surgery, it was considered that only minimal regenerative recovery of the sensory capacities associated with the lesions had taken place [5].

~OTID CANAL

(SITE OF LESION) ~TERIOR LACERATED F O ~ PERNAL CAROTID PERNAL CAROTID

PBRIOR ~ R ~ C A T . G~tEL~

FIG. 2. Schematic representation of the bifurcation of the carotid artery and underlying cranial nerves with the site of glossopharyngeal nerve divisions revealed, (adapted from Green, [2]).

+ 1000 ~

~AIR

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+ 500

ZO.

0 "fOR

MAJOR CTS

- 500

-1000, ND

.Group CTL

GroupV

Group IX

IOR

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FIG. I. Schematic representation of the musculature in the ventral lower jaw of the rat with parotid, submaxillary, and major sublingual ducts exposed; the masseter and anterior belly of the digastricus have been dissected to reveal the lingual nerve and the site of its division, (adapted from Greene, [2D.

FIG. 3. Mean difference score per session for rats with divisions of the lingual nerve (Group V), the glossopharyngeal nerve (Group IX), and without nerve damage (Group CTL); a negative score indicates decreased responding from pre-to post-operative measures. RESULTS

Differences between pre- and post-operative lick rates for air and water were calculated; these differences are presented in Fig. 31 where a decline in responding is r e d e d by a

AGEUSIC AIR-DRINKING

761

negative score. The variances of the difference scores for water were found to be non-homogenous, and thus not appropriate for analysis by parametric techniques. Therefore, both the air- and water-drinking measures were analysed via Wilcoxon matched-pairs signed-ranks tests. The results of the analyses indicated that Group V declined significantly in its responding for air (T = 3, p < 0.05), while all other difference measures (V-water, IX-air and water, CTL-air and water) were not significant. Since the variances of the air-drinking measures were homogenous, the number of licks for air was additionally analyzed using analysis of variance and subsequent Newman-Keuls a posteriori tests. The analysis revealed that neither the control Group (CTL) nor the glossopharyngeal Group (IX) differed significantly in pre- and post-operative rates while the lingual nerve Group (V) was reduced significantly from pre- to postoperative measures (p < 0.01). It is suggested that the results of this second analysis support the differential outcome observed in the Wilcoxon tests.

DISCUSSION

The results indicated that lingual nerve divisions reduced the rate of air-drinking, but not water-drinking. Because water-drinking was not attenuated, it was suggested that no general debilitation of licking behavior occurred as a consequence of lingual nerve sections. Further, glossopharyngeal divisions did not reduce air- or water-drinking rates. The lingual nerve appears to transmit both taste and physical (temperature--pressure) stimulation from the anterior portion of the rat's tongue and the glossopharyngeal nerve transmits taste sensation from the posterior portion of the tongue [6]. Although physical and taste sensations were certainly affected by the nerve sections of the present study,

the differential results from the two lesion sites suggest that air-drinking may be partially dependent upon either the area of stimulation or the type of stimulation. The former interpretation would suggest that air-drinking is associated with the anterior but not the posterior portion of the tongue, while the latter view would consider the reinforcing properties of air-drinking to be more dependent on physical sensation (a substantial part of lingual nerve information) and less dependent on taste stimulation (the sensory component of glossopharyngeal information). The second of these two possibilities seems more likely; indeed actual manipulation of the pressure of the air stream has yielded changes in airdrinking rates [4]. Further evidence for airdrinking's afferent dependence on temperature and/or pressure, rather than taste might be gained by interruption of other cranial nerve branches which transmit physical sensation from the posterior oropharyngeal cavity in addition to those which innervate the anterior portion of the tongue. It might be expected that this tactical approach would reduce air-drinking to a level below that found with lingual denervation alone; but, animals prepared in this manner in our laboratory have shown a very low probability of survival and the procedure seems impractical. Because of the variety of sensory information conveyed by the cranial nerve tlunks associated with the oral cavity, and because some motor components also travel via these trunks to influence salivary function (which, in turn, may influence air-drinking), it seems unlikely that nerve divisions offer a very promising method for defining the sensory basis of air-dxinking. However, the present investigation does indicate that while air-drinking may be reduced, it is not eliminated by partial deafferentation. Consequently, air-drinking appears to be related to physical stimulation delivered to a rather wide area of sensory array in the thirsty rat's mouth.

REFERENCES 1. Chillag, D. and J. Mendeison. Air-licking in desalivate rats, Am. Zool. 9: 1, 1969. 2. Greene, E. C. Anatomy of the Pat. New York: Hafner Publishing Company, 1955. 3. Hendry, D. P. and R. H. Rasche. Analysis of a new nonnutritive reinforcer based on thirst. J. comp. physiol. Psychol. 54: 477-483, 1961. 4. Oatley, K. and A. Dickinson, Air-drinking and the measurement of thirst, Anim. Behav. 18: 259-265, 1970. 5. Pfaffman, C. Taste preference and aversion following lingual denervation. J. comp. physiol. Psychol. 45: 393--400, 1952. 6. Pfaffman, C. The Sense of Taste. In Handbook of Physiology, Section 1 : Neurophysiology, edited by J. Field, H.W. Magoun and V. E. Hall. American Physiological Society, Washington, D.C., 1959, pp. 507-533.

7. Treichler, F. R. and D. C. Riccio. Some characteristics of air-puffs as rewarding stimuli for thirsty rats; paper presented at the Psychonomic Society meetings, November, 1968. 8. Vance, W. B. Observations on the role of salivary secretions in the regulation of food and fluid intake in the white rat. Psychol. Monogr. 79: 1-22, 1965. 9. Vance, W. B. Water intake of partially ageusic rats. L(lb Sci. 5: 2017-2021, 1966. 10. Williams, J. L., F. R. Treichler and D. R. Thomas. Satiation and recovery of the air-drinking response in rats. Psychomon. Sci. 1 : 49-50, 1964.