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Interactions between stimuli with different taste qualities
physiology and Behavior, Vol. 10, pp. 1101-l
106. Brain Research
Publications
Inc., 1973. Printed
m the U.S.A.
Interactions Between Stimuli with Different Taste Qualities’ DONALD
H .MC BURNEY
Department of Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania 15260 AND LINDA M. BARTOSHUK’ Pioneering Research Laboratov,
U. S. Army Natick Laboratories, Natick, Massachusetts 01760
(Received 13 September
1972)
MCBURNEY, D. H. AND L. M. BARTOSHUK. Interactions between stimuli with different taste qualities. PHYSIOL. BEHAV. lO(6) 1101-1106, 1973.-Adaptation effects were exammed between all possible palrs of the following substances: water, NaCl, urea, citric acid, caffeine, and sucrose. Each substance was used both as an adapting solution and as a test stimulus. Adaptation to a stimulus of one quality affects the taste of other stimuli through the addition of a water taste to the usual taste of the second stimulus, rather than by enhancement of the response to the second stimulus, per se, as had previously been thought. That IS, water becomes a taste stimulus when it is presented followmg various adaptation conditions. The taste of the water solvent in the second stimulus adds to the normal taste of the solute in that stimulus No
evidence was found for true interactions among different taste qualities. Adaptation effects
Taste qualities
STUDIES of gustatory adaptation can be divided into two general categories: those in which the adapting and test stimuli have the same taste quahty and those in which the qualities are different. Interest in the latter arose initially from a turn-of-thecentury controversy over whether different taste qualities were sufficiently distinct to constitute different sensory modalities. bhrwall [23] argued that the
basic tastes were as different from each other as they were from, say, colors or sounds. Kiesow, however, performed epperiments showing interactions among the taste qualities that included the enhancement of one quality by prior exposure of the tongue to a stimulus having a different quality. Kiesow reported finding this cross enhancement (he called it successive contrast) among all pairs of the four basic taste qualities [ 12,131. Subsequent studies [ 10, 15, 2 1 I have supported the existence of cross-enhancement, with one exception; Hahn and Ulbrich 1111 found no changes in thresholds after adapting to substances with qualities different from that of the test solution. Their procedure deserves special attention because it differs considerably from conventional procedures. In order to prevent recovery from adaptation during the measurement
of threshold, they mixed the substance to be tested in the adapting solution instead of water. This procedure inadvertently prevented the occurrence of the water taste, a phenomenon that was not understood at that time. We now know that water becomes a taste stimulus when it is presented following adaptation to many sapid substances. Bartoshuk, McBurney and Pfaffmann [5] found that adapting to weak NaCl caused water to have a sour-bitter taste. The concentration of sodium m that experiment was in the range of normal mixed saliva, implying that the tastes often attributed to distilled water are due to sodium chloride adaptation. Since then it has been shown that all four basic tastes can be produced in water by suitable adaptation [ 2, 16, 191. It has also been shown that the water taste of a compound will add to the taste of a weak solution that follows it [9,161. The water taste phenomenon suggests a reinterpretation of those studies that found cross-enhancement. The enhancement may have been produced by the water in which the second stimulus was dissolved rather than by the solute itself. Of the earlier studies, only Hahn and Ulbrich controlled for the water taste and only they failed to find cross-enhancement. The
‘Based on research conducted in part when L. M. Bartoshuk was on the staff of the U. S. Army Natick Laboratories and D. H. McBumey visited under support of the Army Research Office at Durham, North Carolina. Supported in part by PHS Grant NS 07873-04 to D. H. McBumey. We thank T. R. Shick for technical assistance. “Now at John B. Pierce Foundation and Yale Umversity, 290 Congress Avenue, New Haven, Connecticut 06519. 1101
MCBURNEY AND BAR.1 OSHU h
1102
expenment was designed to test for crossenhancement with an experimental design that allowed for the independent measurement of the water taste of the adapting solution and the enhancement of the normal taste of the second solution. present
30
[-
HOH .
NOCI ,
1
UREA
CITRIC
CAFFEINE /
1~,’
SUCROSE
METHOD Subjects
The two authors, two colleagues familiar with taste research and six naive volunteers served as subjects Solutions All solutrons were made of reagent grade chemicals in distilled water except for commercial sucrose. The followmg stimuli had been matched in overall subjective intensity to 0.1 M NaCl pnor to the study: 0.1 M caffeine, 0.004 M citric acid, 0.18 M sucrose, 0.82 M urea, and 0.1 M NaCl. In addition, there were two other concentrations of each compound l/2 log step and 1 log step weaker than the matched concentrations. Apparatus
The adapting solutions and stimuli were presented to the extended anterior dorsal tongue by a gravity flow system [see 18 I . All solutions were maintained at 34” C. Procedure
A concentration series of each substance was scaled with SIX adaptmg solutions: water and the highest concentratton of each of the five substances listed above. Stimuli and adapting solutions were randomized. The tongue was adapted to the appropriate solution for 30 set before exposure to the test stimulus.
CONCENTRATIONS
OF
SUCROSE
FIG. 1. Effects of adaptatton to water and to five compounds on the taste of water and sucrose. The top row shows the effects on the total taste intensity. The other rows show the effect on bitterness, sweetness, sourness and saltiness, respectively. Each column shows the effects of one adapting condition. Within each cell, the four points show the effects of a particular adapting solution on the total mtensity or the intensity of one quality of water and sucrose. The left-most point in each cell represents water, followed by the three concentrations of sucrose, m order. The vertical lines indicate +l standard error of the mean Nacl
UREA
CITRIC
CAFFEINE
50 -
Psychophyszcal Method
SubJects gave a magnitude estimate of the overall mtensity of taste and then divrded their estimates among the four taste qualities according to the relative strength of each quality present [29] In this manner, an estimate of the overall intensity and the intensities of each of the four taste qualities of a stimulus were obtained on a single trial. RESULTS Each S’s data were multiplied by a constant to equate the average numbers assigned to the total taste intensity of each stimulus. The arithmetic means of the adjusted data are plotted in Figs. 1 through 5. Within each cell, the four points making up the curve consist of water and the three concentrations of the test stimulus. Figure 1 shows the effect of the various adapting conditions on the taste of the sucrose solutions. Each column shows the effect of one adapting condition. The rows show the effect of the various adapting conditions on the total intensity and on bitterness, sweetness, sourness and saltiness from the top down. For example, in Fig. 1 the effect of adpatation to urea on the taste of sucrose may be seen by comparing the first column, which shows the taste of sucrose solutions after water adaptation, with the third column which shows the taste of sucrose solutions after urea adaptation. The total taste functions seem to show that adaptation to urea enhanced
CONCENTRATIONS
OF
NaCi
FIG. 2. Same as for Fig. 1 for NaCl.
SUCROSE
INTERACTIONS
HOH
1103
BETWEEN TASTE QUALITIES
NaCl
UREA
CITRIC
CAFFEINE
SUCROSE
HOH
NaCi
UREA
CITRIC
CAFFEINE
SUCROSE
t-4-4 ?!!!!J --
-b&l
CONCENTRATIONS
FIG. 3.
OF
CAFFEINE
CONCENTRATIONS
FIG. 5.
Same as for Fig. 1 for caffeine. CITRIC
HOH
CAFFEINE
SUCROSE
401---_
CONCENTRATIONS
FIG. 4.
OF
CITRIC
ACID
Same as for Fig. 1 for citric acid.
weak sucrose. However, the functions for the individual qualities show that adaptation to urea actually added the salty taste of water-after-urea to the sweetness of sucrose. Adaptation to NaCl produced similar apparent enhancement that was actually the addition of the usual bittersour taste of water-after-NaCl. The only case in which the sweetness of sucrose appeared to be enhanced occurred for
OF
UREA
Same as for Fig. 1 for urea.
adaptation to caffeine which makes water taste sweet. As may be expected, sucrose adaptation decreased the sweetness of sucrose. Figures 2 through 5 show the effect of these adapting conditions on NaCl, caffeine, citric acid and urea, respectively. Just as with sucrose stimuli, when total intensity appears to be enhanced, an examination of the breakdown into component qualities shows that the enhancement is actually the addition of the appropriate water taste quality. There are a few effects as shown in Figs. l--S, such as the enhancement of the bitterness of urea by caffeine and the reduction of the saltiness of NaCl by caffeine, that are not predictable from cross adaptation or water taste effects, but speculation concerning these would be premature at this point. Since the adapting condition determines the apparent enhancement, we collapsed the data across all test compounds for each adpating condition (Fig. 6). The top row shows the magnitude of the vanous taste qualities of water after adaptation to the various adapting solutions compared to water adaptation. NaCl produces a sour-bitter water taste, urea produces a salty water taste, citric acid and caffeine produce a sweet water taste and sucrose produces a very weak bitter water taste These are the typical water tastes for these compounds. The other rows show the tastes of the test solutions after adaptation to the various compounds compared to their taste after water adaptation at each of the three concentrations, i.e., the water tastes after the solute tastes have been subtracted. Adaptation has the same qualitative effect on the different compounds as on water but the effect decreases with increasing intensity of the test solutions. Bars that extend below the baseline represent typical cross adaptation. It 1s important to note that when cross-adaptation occurs, the stimuli are usually found to have qualities in common. For example, in Fig. 2 citric acid cross adapts NaCl. Figure 4 shows that citric acid, in fact, tastes somewhat salty.
1104
MCBURNEY AND BAR’I‘OSHUK
UREA
NCICi '
n q
SALTY SWEET
CITRIC
CAFFEINE __./-
SUCROSE ----~.--._,
@j SOUR &$j BITTER
FIG. 6 The effect of adaptation to each of the five compounds on water and the three concentrations of the test compounds, collapsed over all test compounds. Each column represents the effect of adaptation to one compound. The rows show the effect of adaptation to the compound listed above the column on the taste of water (top row) and the three concentrations of the test compounds (from the second row down) Within each cell the bars show the change in each taste quahty of the test compounds compared to a basehne of water adaptation. Bars that extend upward indicate that adaptation to the compound hsted at the top of the column mcreased that quality across all compounds tested, compared to water adaptation. Bars that project downward Indicate that adaptation to the particular compound reduced that quality across all compounds. The vertical lines indicate +l standard error of the mean. An asterisk lndlcates that the difference IF
slgmficant at the 0 05 Ievel The data indicate that when two stimuh are tasted successively, two phenomena operate to determine the taste of the second stimulus. The water solvent of the second
solution may take on a taste because of adaptation to the first solution, and the taste of the solute in the second solution may be reduced In intensity If the first and second solutes have taste qualities in common. The water taste and the solute taste do not sum linearly but appear to suppress one another just as two solute tastes do. DISCUSSION The results of this study are consistent with the results of both Kiesow and Meiselman, even though these studies
appear to support the existence of cross-enhancement. Although Klesow reported that taste qualities mutually enhance each other, exammation of his data shows that the enhancement was not always m the proper quality. For example, NaCl after HCi was often described as sweeter rather than saltier which agrees with the present study. bhrwall 1231 mentioned this point in a cnticism of Klesow’s work but the review articles of the day failed to recognize the significance of Ghrwall’s article. Meiselman obtained enhancement with QSO, and sucrose but not with NaCl adaptation. The QSO, and sucrose concentrations he used typically produce good water responses. However, the NaCl concentration used was higher than those producing optimal water responses [2] Since Meiselman’s subjects
INTERACTIONS
BETWEEN TASTE QUALITIES
1105
reported only the predominant taste quality of the stimuli (personal communication, H. L. Meiselman), it is possible that the enhancement found was not in the usual taste quality, but was the result of a water taste. The studies of Mayer and of Dallenbach and Dallenbach [lO,lS] do not specify the method used to obtain thresholds in enough detail to allow assessment of the possible effects of water tastes. However, the contradiction between the conclusions from their studies and that of Hahn is clear. Hahn inadvertently prevented water responses by mixing his test stimulus in the adapting stimulus and found no enhancement. Mayer and Dallenbach and Dallenbach did not prevent water responses and did observe apparent enhancement. Neural studies on hamster, rat, and cat show both cross-adaptation and cross-enhancement (7, 28,30,3 1I. In these cases, the apparent enhancement observed could have been contributed by water tastes. Unfortunately, the experiments do not all contain the appropriate controls to allow this to be demonstrated directly. For example, Wang and Bernard [30] tested the effects of three adapting conditions (NaCl, HCl, and quinme) on taste response to these same stimuli in single chorda tympani fibers in the cat. They found cross-adaptation in some cases and cross-enhancement in others. The following example is particularly interesting: “.... in one fiber the response to HCl was potentiated after prior adaptation to NaCl while the NaCl response was depressed when it followed adaptation to HCl.” They describe such effects as “....interactions between taste stimuli which may mvolve inhibitory and excitatory connections.” However, the occurrence of water tastes can explain such observations without assuming interaction. Water responses in the cat, as well as in man and other mammals, have been shown to be contingent on the nature of the preceding adapting solution [ 1, 3, 41. If the fiber cited in the example of Wang and Bernard responded to water-after-NaCl, the HCl-after-NaCl could have been enhanced because two responses actually occurred: one response to water-after-NaCl plus another to HCl. NaCl after HCl need not be enhanced if the fiber did not respond to water-after-HCl. The suppression of NaCl after HCl may be the result of simple cross-adaptation. We have already seen a similar result in the human data in this paper. Citric acid tastes somewhat salty as well as sour and can cross-adapt some of the saltiness of NaCl. Two of the other studies, those of Yinon and Erickson [3 11 and Smith and Frank [ 281, did include the proper controls for water tastes. In recordmgs from single chorda tympani fibers in the hamster, the adapting solutions that produced the greatest apparent enhancement also produced the most responses to water [ 3 11 Whole nerve recordings from the rat showed similar results. The adapting solution that produced the apparent enhancement (sucrose) also produced responses to water [28] . The demonstration of interactions between taste substances of different qualities would have important implications for sensory coding. Wang and Bernard [30] have already suggested that the interactions in their study might
be related to the connections between frog papillae demonstrated by Rapuzzi and Casella [27]. A mechanism of this type has considerable appeal since lateral connections are important in other senses, especially vision. However, all of the cross-enhancement effects demonstrated up to now can be explained without proposing such a mechanism. This does not prove that crossenhancement due to interactions among solutes never occurs. However, any efforts to prove that such effects do exist must include controls to assess the contribution of water responses. Kiesow’s studies on interactions among taste qualities appear to have been designed to search for analogies with color vision. Kiesow reported contrast between different tongue areas [ 131, which is analogous to simultaneous color contrast, compensation or loss of quality resulting from mixing two primary tastes [ 141 and crossenhancement which is analogous to color after-images. We must now be skeptical of these results. Loss of quality in taste mixtures is a rare phenomenon if it occurs at all. Contrast between different tongue areas has failed a more recent replication test [ 261, and the present study suggests that cross-enhancement is due to the addition of water tastes rather than true interactions among qualities. With these revisions of older conclusions about taste qualities, a new much simpler view emerges: the four taste qualities appear to be relatively independent of one another. This conclusion is supported by other taste psychophysical studies in which one quality can be altered without altering others [6, 17,20,29]. The four basic tastes are used with some embarrassment by current taste investigators. Some of this resistance seems to be due to a broadening of the term taste to include sensations mediated other than by the taste buds. The four taste qualities were arrived at m the classical literature by mtrospective analysis that involved taking care to eliminate these other inputs. Another source of resistance to the concept of basic tastes is the animal work, where by the nature of the case, it is not possible to talk about quality, only similarity or dissimilarity of two responses. Electrophysiological studies on lower animals do not suggest specific mechanisms for the four qualities but instead support nonspecificity, that is, many single taste fibers are responsive to several taste stimuli [8,22,24, 251. It is true that the basic tastes cannot be exactly analogous to color primaries because of the failure of taste mixtures to produce new qualities or to neutralize qualities in the components of the mixture. It is possible that we should think in terms of the skin senses where we ordinarily speak of different senses with interactions among them. The fact remains that substances are perceived as having taste qualities that can be described in terms of a relatively small number of names. The qualities we identify may be arbitrary and they may not be exhaustive, but we cannot do justice to taste expenence without recognizing that substances do not just taste similar or dissimilar. Whether or not we call these qualities primaries is less important than determining the relationships among them.
REFERENCES 1. Bartoshuk, L. M. Effects of adaptation on responses to water m cat and rat. Doctoral disseratlon, Brown University. Ann Arbor, Mich.: University Microfilms, 1965, No. 65-13,630.
2. Bartoshuk, L. M. Water taste in man. Percept Psychophys 3: 69-12,1968.
1106
MCBURNEY
3. Bartoshuk, L. M. and C. Pfaffmann. Effects of pre-treatment on the water taste response m cat and rat. Fedn Proc. 24: 207, 1965 (abstract no 441) 4 Bartoshuk, L. M., M A. Harned and L. H. Parks Taste of water m cat effects of sucrose preference Sczence 171: 699-701, 1971 5 Bartoshuk, L. M., D H McBurney and C. Pfaffmann. Taste of sodmm chlorrde solutrons after adaptation to sodium chlorrde rmplications for the “Water taste.” Sczence 143: 967-968. 1964 6 Bartoshuk, L. M., G P. Dateo, D J Vandenbelt, R. D Buttrick and L. Long. Effects of Gymnema sylvestre and Synsepalum dulqficum on taste m man In Taste and Olfactron III, edited by C Pfaffmann New York. Rockefeller University Press, 1969, pp 436-444 I. Betdler, L. M. The physiological basrs of taste In Symposzum on Physzologtcal Psychology, ACR-1 Pensacola, Fla: Office of Naval Research, 1955, pp. l-34. 8 Beidler, L. M , I. Y. Frshman and C. Hardrman. Species dtfferences m taste responses. Am. J Physzol 181: 235-239, 1955
9. Bogart, L M A salty taste following urea adaptatron tmphcatrons for a mechanism encoding saltiness. Doctoral dissertation, Umverstty of Pittsburgh. Ann Arbor, Mrch Umversrty Mtcrofilms, 1969, No. 70-75371. 10. Dallenbach, J W and K M Dallenbach The effects of bitter-adaptation on sensrtivtty to other taste qualities Am J Psycho/
56: 21-31,1943
11
Hahn, H and L. Ulbrrch Eme systematrsche Untersuchung der Geschmackschwellen Pflicgers Archges Physzol. 250:
12
Henmng. H Psychologische
357-385,1948. Handbuch
Studren am Geschmackssmn. In Arbertsmethoden, edited by E. Urban and Schwarzenberg. 1927, pp
der Blologischen
Aberhalden Berlm 6277740 13. Kresow, F Bertrage zur Physrologischen Psychologre des Geschmackssinnes Phzl Stud 10: 5233561,1894 14 Kresow, F. Bertrage zur Physrologschen Psychologre des Geschmackssmnes Phd Stud 12: 255-278.1896. 1s Mayer, B Messende Untersuchungen uber die Umstimmung des Geschmackswerkzeugs Zert Sznnesphyszol 58: 133-152, 1927
AND BARTOSHUk
16
McBurney, D H. Effects of adaptation on human tdqtt‘ functton In. Olfactron and Taste III, edited by C Pfatfmann New York Rockefeller University Press, 1969, pp 407 419 17 McBurney, D H. Gustatory cross-adaptation between sweet tastmg compounds Percept Pbychophys 11: 225 --227, 1972. 18 McBurney. D. H Magnitude estimations of the taste of aodmm chlortde after adaptation to sodium chlorrde. .I pxp Ps~chol 72: 869-873. 1966 19. McBurney, D H and T R Shrck. Taste ,md water taste of twenty-six compounds for man Percept Psychophys 10: 249-252.1971
McBurney, D. H , D. V Smith and T R. Shrck Gustatorv cross adaptation sourness and bitterness Percept Pqychophbs 11: 228-232.1972 21. Merselman H L Adaptation and cross-adaptatron of the four gustatory quahties. Percept Psychophys 4: 368--372, 1968 22 Oakley, B and R M. BenJamm Neural mechamsms of taste.
20.
Physzol Rev 46: 173-211.1966
23
Ohrwall, H Dte Modahtats-und Quahtatsbegrtffe m der Smnesphystologie und deren Bedeutung. Skand Arch Phvszol. 11: 245-272,190l 24. Pfaffmann, C Gustatory afferent impulses J cell camp Physzol 17: 243-258, 1941. 25. Pfaffmann, C Gustatory nerve Impulses m rat, cat and rabbit J Neurophyslol
18: 429-440,19%5
26.
Pfaffmann. C.. L. M Bartoshuk and D. H. McBurnev Taste psychophysics In Handbook of Sensory Physzology, -Vol IV, Chemical Senses, 2, Taste, edited by L M Beidler. Berlin Springer-Verlag, 1971, pp 75--101 27 Rapuzzr, G and C Casella Innervation of fungrform papillae m the frog tongue J. Neurophyaol 28: 154.-165, 1965 28. Smith D V and M Frank Cross adaptation between salts m the chorda tympam nerve of the rat. Phyaol Behav 8: 213-220,
1972
Smith, D. V and D H. McBurney Gustatory cross-adaptation does a single mechanism code the salty taste? J exp Psychol. 80: 101-105, 1969 30. Wang, M B and R. A Bernard. Characterrzatron and mteraction of taste response m chorda tympam fibers of the cat. Bram Res 15: S67-570,1969 31 Ymon, U. and Erickson, R. P Adaptation and the neural code for taste. Brazn Res 23: 428-432, 1970 29
106. Brain Research
Publications
Inc., 1973. Printed
m the U.S.A.
Interactions Between Stimuli with Different Taste Qualities’ DONALD
H .MC BURNEY
Department of Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania 15260 AND LINDA M. BARTOSHUK’ Pioneering Research Laboratov,
U. S. Army Natick Laboratories, Natick, Massachusetts 01760
(Received 13 September
1972)
MCBURNEY, D. H. AND L. M. BARTOSHUK. Interactions between stimuli with different taste qualities. PHYSIOL. BEHAV. lO(6) 1101-1106, 1973.-Adaptation effects were exammed between all possible palrs of the following substances: water, NaCl, urea, citric acid, caffeine, and sucrose. Each substance was used both as an adapting solution and as a test stimulus. Adaptation to a stimulus of one quality affects the taste of other stimuli through the addition of a water taste to the usual taste of the second stimulus, rather than by enhancement of the response to the second stimulus, per se, as had previously been thought. That IS, water becomes a taste stimulus when it is presented followmg various adaptation conditions. The taste of the water solvent in the second stimulus adds to the normal taste of the solute in that stimulus No
evidence was found for true interactions among different taste qualities. Adaptation effects
Taste qualities
STUDIES of gustatory adaptation can be divided into two general categories: those in which the adapting and test stimuli have the same taste quahty and those in which the qualities are different. Interest in the latter arose initially from a turn-of-thecentury controversy over whether different taste qualities were sufficiently distinct to constitute different sensory modalities. bhrwall [23] argued that the
basic tastes were as different from each other as they were from, say, colors or sounds. Kiesow, however, performed epperiments showing interactions among the taste qualities that included the enhancement of one quality by prior exposure of the tongue to a stimulus having a different quality. Kiesow reported finding this cross enhancement (he called it successive contrast) among all pairs of the four basic taste qualities [ 12,131. Subsequent studies [ 10, 15, 2 1 I have supported the existence of cross-enhancement, with one exception; Hahn and Ulbrich 1111 found no changes in thresholds after adapting to substances with qualities different from that of the test solution. Their procedure deserves special attention because it differs considerably from conventional procedures. In order to prevent recovery from adaptation during the measurement
of threshold, they mixed the substance to be tested in the adapting solution instead of water. This procedure inadvertently prevented the occurrence of the water taste, a phenomenon that was not understood at that time. We now know that water becomes a taste stimulus when it is presented following adaptation to many sapid substances. Bartoshuk, McBurney and Pfaffmann [5] found that adapting to weak NaCl caused water to have a sour-bitter taste. The concentration of sodium m that experiment was in the range of normal mixed saliva, implying that the tastes often attributed to distilled water are due to sodium chloride adaptation. Since then it has been shown that all four basic tastes can be produced in water by suitable adaptation [ 2, 16, 191. It has also been shown that the water taste of a compound will add to the taste of a weak solution that follows it [9,161. The water taste phenomenon suggests a reinterpretation of those studies that found cross-enhancement. The enhancement may have been produced by the water in which the second stimulus was dissolved rather than by the solute itself. Of the earlier studies, only Hahn and Ulbrich controlled for the water taste and only they failed to find cross-enhancement. The
‘Based on research conducted in part when L. M. Bartoshuk was on the staff of the U. S. Army Natick Laboratories and D. H. McBumey visited under support of the Army Research Office at Durham, North Carolina. Supported in part by PHS Grant NS 07873-04 to D. H. McBumey. We thank T. R. Shick for technical assistance. “Now at John B. Pierce Foundation and Yale Umversity, 290 Congress Avenue, New Haven, Connecticut 06519. 1101
MCBURNEY AND BAR.1 OSHU h
1102
expenment was designed to test for crossenhancement with an experimental design that allowed for the independent measurement of the water taste of the adapting solution and the enhancement of the normal taste of the second solution. present
30
[-
HOH .
NOCI ,
1
UREA
CITRIC
CAFFEINE /
1~,’
SUCROSE
METHOD Subjects
The two authors, two colleagues familiar with taste research and six naive volunteers served as subjects Solutions All solutrons were made of reagent grade chemicals in distilled water except for commercial sucrose. The followmg stimuli had been matched in overall subjective intensity to 0.1 M NaCl pnor to the study: 0.1 M caffeine, 0.004 M citric acid, 0.18 M sucrose, 0.82 M urea, and 0.1 M NaCl. In addition, there were two other concentrations of each compound l/2 log step and 1 log step weaker than the matched concentrations. Apparatus
The adapting solutions and stimuli were presented to the extended anterior dorsal tongue by a gravity flow system [see 18 I . All solutions were maintained at 34” C. Procedure
A concentration series of each substance was scaled with SIX adaptmg solutions: water and the highest concentratton of each of the five substances listed above. Stimuli and adapting solutions were randomized. The tongue was adapted to the appropriate solution for 30 set before exposure to the test stimulus.
CONCENTRATIONS
OF
SUCROSE
FIG. 1. Effects of adaptatton to water and to five compounds on the taste of water and sucrose. The top row shows the effects on the total taste intensity. The other rows show the effect on bitterness, sweetness, sourness and saltiness, respectively. Each column shows the effects of one adapting condition. Within each cell, the four points show the effects of a particular adapting solution on the total mtensity or the intensity of one quality of water and sucrose. The left-most point in each cell represents water, followed by the three concentrations of sucrose, m order. The vertical lines indicate +l standard error of the mean Nacl
UREA
CITRIC
CAFFEINE
50 -
Psychophyszcal Method
SubJects gave a magnitude estimate of the overall mtensity of taste and then divrded their estimates among the four taste qualities according to the relative strength of each quality present [29] In this manner, an estimate of the overall intensity and the intensities of each of the four taste qualities of a stimulus were obtained on a single trial. RESULTS Each S’s data were multiplied by a constant to equate the average numbers assigned to the total taste intensity of each stimulus. The arithmetic means of the adjusted data are plotted in Figs. 1 through 5. Within each cell, the four points making up the curve consist of water and the three concentrations of the test stimulus. Figure 1 shows the effect of the various adapting conditions on the taste of the sucrose solutions. Each column shows the effect of one adapting condition. The rows show the effect of the various adapting conditions on the total intensity and on bitterness, sweetness, sourness and saltiness from the top down. For example, in Fig. 1 the effect of adpatation to urea on the taste of sucrose may be seen by comparing the first column, which shows the taste of sucrose solutions after water adaptation, with the third column which shows the taste of sucrose solutions after urea adaptation. The total taste functions seem to show that adaptation to urea enhanced
CONCENTRATIONS
OF
NaCi
FIG. 2. Same as for Fig. 1 for NaCl.
SUCROSE
INTERACTIONS
HOH
1103
BETWEEN TASTE QUALITIES
NaCl
UREA
CITRIC
CAFFEINE
SUCROSE
HOH
NaCi
UREA
CITRIC
CAFFEINE
SUCROSE
t-4-4 ?!!!!J --
-b&l
CONCENTRATIONS
FIG. 3.
OF
CAFFEINE
CONCENTRATIONS
FIG. 5.
Same as for Fig. 1 for caffeine. CITRIC
HOH
CAFFEINE
SUCROSE
401---_
CONCENTRATIONS
FIG. 4.
OF
CITRIC
ACID
Same as for Fig. 1 for citric acid.
weak sucrose. However, the functions for the individual qualities show that adaptation to urea actually added the salty taste of water-after-urea to the sweetness of sucrose. Adaptation to NaCl produced similar apparent enhancement that was actually the addition of the usual bittersour taste of water-after-NaCl. The only case in which the sweetness of sucrose appeared to be enhanced occurred for
OF
UREA
Same as for Fig. 1 for urea.
adaptation to caffeine which makes water taste sweet. As may be expected, sucrose adaptation decreased the sweetness of sucrose. Figures 2 through 5 show the effect of these adapting conditions on NaCl, caffeine, citric acid and urea, respectively. Just as with sucrose stimuli, when total intensity appears to be enhanced, an examination of the breakdown into component qualities shows that the enhancement is actually the addition of the appropriate water taste quality. There are a few effects as shown in Figs. l--S, such as the enhancement of the bitterness of urea by caffeine and the reduction of the saltiness of NaCl by caffeine, that are not predictable from cross adaptation or water taste effects, but speculation concerning these would be premature at this point. Since the adapting condition determines the apparent enhancement, we collapsed the data across all test compounds for each adpating condition (Fig. 6). The top row shows the magnitude of the vanous taste qualities of water after adaptation to the various adapting solutions compared to water adaptation. NaCl produces a sour-bitter water taste, urea produces a salty water taste, citric acid and caffeine produce a sweet water taste and sucrose produces a very weak bitter water taste These are the typical water tastes for these compounds. The other rows show the tastes of the test solutions after adaptation to the various compounds compared to their taste after water adaptation at each of the three concentrations, i.e., the water tastes after the solute tastes have been subtracted. Adaptation has the same qualitative effect on the different compounds as on water but the effect decreases with increasing intensity of the test solutions. Bars that extend below the baseline represent typical cross adaptation. It 1s important to note that when cross-adaptation occurs, the stimuli are usually found to have qualities in common. For example, in Fig. 2 citric acid cross adapts NaCl. Figure 4 shows that citric acid, in fact, tastes somewhat salty.
1104
MCBURNEY AND BAR’I‘OSHUK
UREA
NCICi '
n q
SALTY SWEET
CITRIC
CAFFEINE __./-
SUCROSE ----~.--._,
@j SOUR &$j BITTER
FIG. 6 The effect of adaptation to each of the five compounds on water and the three concentrations of the test compounds, collapsed over all test compounds. Each column represents the effect of adaptation to one compound. The rows show the effect of adaptation to the compound listed above the column on the taste of water (top row) and the three concentrations of the test compounds (from the second row down) Within each cell the bars show the change in each taste quahty of the test compounds compared to a basehne of water adaptation. Bars that extend upward indicate that adaptation to the compound hsted at the top of the column mcreased that quality across all compounds tested, compared to water adaptation. Bars that project downward Indicate that adaptation to the particular compound reduced that quality across all compounds. The vertical lines indicate +l standard error of the mean. An asterisk lndlcates that the difference IF
slgmficant at the 0 05 Ievel The data indicate that when two stimuh are tasted successively, two phenomena operate to determine the taste of the second stimulus. The water solvent of the second
solution may take on a taste because of adaptation to the first solution, and the taste of the solute in the second solution may be reduced In intensity If the first and second solutes have taste qualities in common. The water taste and the solute taste do not sum linearly but appear to suppress one another just as two solute tastes do. DISCUSSION The results of this study are consistent with the results of both Kiesow and Meiselman, even though these studies
appear to support the existence of cross-enhancement. Although Klesow reported that taste qualities mutually enhance each other, exammation of his data shows that the enhancement was not always m the proper quality. For example, NaCl after HCi was often described as sweeter rather than saltier which agrees with the present study. bhrwall 1231 mentioned this point in a cnticism of Klesow’s work but the review articles of the day failed to recognize the significance of Ghrwall’s article. Meiselman obtained enhancement with QSO, and sucrose but not with NaCl adaptation. The QSO, and sucrose concentrations he used typically produce good water responses. However, the NaCl concentration used was higher than those producing optimal water responses [2] Since Meiselman’s subjects
INTERACTIONS
BETWEEN TASTE QUALITIES
1105
reported only the predominant taste quality of the stimuli (personal communication, H. L. Meiselman), it is possible that the enhancement found was not in the usual taste quality, but was the result of a water taste. The studies of Mayer and of Dallenbach and Dallenbach [lO,lS] do not specify the method used to obtain thresholds in enough detail to allow assessment of the possible effects of water tastes. However, the contradiction between the conclusions from their studies and that of Hahn is clear. Hahn inadvertently prevented water responses by mixing his test stimulus in the adapting stimulus and found no enhancement. Mayer and Dallenbach and Dallenbach did not prevent water responses and did observe apparent enhancement. Neural studies on hamster, rat, and cat show both cross-adaptation and cross-enhancement (7, 28,30,3 1I. In these cases, the apparent enhancement observed could have been contributed by water tastes. Unfortunately, the experiments do not all contain the appropriate controls to allow this to be demonstrated directly. For example, Wang and Bernard [30] tested the effects of three adapting conditions (NaCl, HCl, and quinme) on taste response to these same stimuli in single chorda tympani fibers in the cat. They found cross-adaptation in some cases and cross-enhancement in others. The following example is particularly interesting: “.... in one fiber the response to HCl was potentiated after prior adaptation to NaCl while the NaCl response was depressed when it followed adaptation to HCl.” They describe such effects as “....interactions between taste stimuli which may mvolve inhibitory and excitatory connections.” However, the occurrence of water tastes can explain such observations without assuming interaction. Water responses in the cat, as well as in man and other mammals, have been shown to be contingent on the nature of the preceding adapting solution [ 1, 3, 41. If the fiber cited in the example of Wang and Bernard responded to water-after-NaCl, the HCl-after-NaCl could have been enhanced because two responses actually occurred: one response to water-after-NaCl plus another to HCl. NaCl after HCl need not be enhanced if the fiber did not respond to water-after-HCl. The suppression of NaCl after HCl may be the result of simple cross-adaptation. We have already seen a similar result in the human data in this paper. Citric acid tastes somewhat salty as well as sour and can cross-adapt some of the saltiness of NaCl. Two of the other studies, those of Yinon and Erickson [3 11 and Smith and Frank [ 281, did include the proper controls for water tastes. In recordmgs from single chorda tympani fibers in the hamster, the adapting solutions that produced the greatest apparent enhancement also produced the most responses to water [ 3 11 Whole nerve recordings from the rat showed similar results. The adapting solution that produced the apparent enhancement (sucrose) also produced responses to water [28] . The demonstration of interactions between taste substances of different qualities would have important implications for sensory coding. Wang and Bernard [30] have already suggested that the interactions in their study might
be related to the connections between frog papillae demonstrated by Rapuzzi and Casella [27]. A mechanism of this type has considerable appeal since lateral connections are important in other senses, especially vision. However, all of the cross-enhancement effects demonstrated up to now can be explained without proposing such a mechanism. This does not prove that crossenhancement due to interactions among solutes never occurs. However, any efforts to prove that such effects do exist must include controls to assess the contribution of water responses. Kiesow’s studies on interactions among taste qualities appear to have been designed to search for analogies with color vision. Kiesow reported contrast between different tongue areas [ 131, which is analogous to simultaneous color contrast, compensation or loss of quality resulting from mixing two primary tastes [ 141 and crossenhancement which is analogous to color after-images. We must now be skeptical of these results. Loss of quality in taste mixtures is a rare phenomenon if it occurs at all. Contrast between different tongue areas has failed a more recent replication test [ 261, and the present study suggests that cross-enhancement is due to the addition of water tastes rather than true interactions among qualities. With these revisions of older conclusions about taste qualities, a new much simpler view emerges: the four taste qualities appear to be relatively independent of one another. This conclusion is supported by other taste psychophysical studies in which one quality can be altered without altering others [6, 17,20,29]. The four basic tastes are used with some embarrassment by current taste investigators. Some of this resistance seems to be due to a broadening of the term taste to include sensations mediated other than by the taste buds. The four taste qualities were arrived at m the classical literature by mtrospective analysis that involved taking care to eliminate these other inputs. Another source of resistance to the concept of basic tastes is the animal work, where by the nature of the case, it is not possible to talk about quality, only similarity or dissimilarity of two responses. Electrophysiological studies on lower animals do not suggest specific mechanisms for the four qualities but instead support nonspecificity, that is, many single taste fibers are responsive to several taste stimuli [8,22,24, 251. It is true that the basic tastes cannot be exactly analogous to color primaries because of the failure of taste mixtures to produce new qualities or to neutralize qualities in the components of the mixture. It is possible that we should think in terms of the skin senses where we ordinarily speak of different senses with interactions among them. The fact remains that substances are perceived as having taste qualities that can be described in terms of a relatively small number of names. The qualities we identify may be arbitrary and they may not be exhaustive, but we cannot do justice to taste expenence without recognizing that substances do not just taste similar or dissimilar. Whether or not we call these qualities primaries is less important than determining the relationships among them.
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