Adaptation and the neural code for taste

428

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Adaptation and the neural code for' taste Some of the problems of quality and intensity coding in gustation that have met with difficulties in analysis in terms of the activity of individual neurons have been successfully approached by our 'across-fiber pattern' analysis of populations of individual neurons 2 ~,6, and this approach has been extended to sensory systems in generaP. As a further extension of the applicability of this approach, we have here investigated its usefulness in aiding our understanding of the complex neural and psychophysical effects of adaptation in gustation. The subjects were pentobarbital anesthetized hamsters. Responses from 25 chorda tympani taste neurons were analyzed in terms of the across-fiber patterns of activity produced. Up3n isolation of a taste neuron, conditioning stimuli were applied for 40 sec prior to the application of the test stimuli. Five test stimuli were used: NaC1, HCI, quinine hydrochloride (QHC1), sucrose, and water. These same stimuli were uszd as conditioning stimuli thus yielding a 5 × 5 experimental matrix. The responses of a relatively 'specific' taste neuron are illustrated in Fig. 1 (all of the data for this neuron appear in Fig. 3, neuron no. 8). In the upper 4 records are shown the responses of this neuron to QHCI, NaCI, HCI and sucrose following water. At these concentrations this neuron responds well only to NaCt. Following adaptation to stimuli other than water, this neuron is seen to be less specific. In the 4th and 5th records, sucrose is seen to arrest the activity produced by previous stimulation with water or NaCI. However, as seen in the 6th record, sucrose elicits a response following prior stimulation with HC1. In the last record it is seen that after adaptation to NaCI this neuron will respond to water. It also responded to water following sucrose and, slightly, after QHC1, but not after HC1. Neurons considered to be 'specific' were found to be 'non-specific' considering all states of adaptation.

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Brain Research, 23 (1970) 428-432

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Fig. 2. Responses of a 'non-specific' taste neuron. The symbols are as in Fig. 1. Several records are continued for two lines. The responses of a broadly tuned or 'non-specific' neuron are shown in Fig. 2 (this neuron appears as neuron no. 9 in Fig. 3). In the first 4 records the responses of this neuron to NaCI, HC1, QHC1 and sucrose are shown. It responded well to NaC1 and sucrose, and slightly to HC1 and QHCI. As with the 'specific' neuron, the responses of this neuron were also dependent on the state of adaptation. As examples, the lower 4 traces show responses to sucrose following the other 4 stimuli: water, NaCI, HC1, and QHC1. This neuron responds following each adapting stimulus with variations in the bursting activity typical of the responses of taste neurons to sucrose a. The results for 12 of the 25 neurons are summarized in Fig. 3 as across-fiber patterns. The responses of these neurons to the various stimuli following water are shown in the bottom row. In comparison to this level of response following water, both enhancement and depression of response with the neurons adapted to other stimuli may be seen in the upper rows. For example, the response of neuron no. 1 to sucrose (3rd column) is depressed following adaptation to HC1 (top row) in comparison to its response to sucrose following water (bottom row); however, following adaptation to NaC1 (4th row), its response to sucrose is enhanced. The main thrust o f handling adaptation data in terms of across-fiber patterns may be discussed in reference to Fig. 3. It is clear in this figure that the shapes of the across-fiber patterns, coding the quality of the taste stimuli 2-0, are in some cases strongly influenced by the preadapting stimuli, and it is well known that the taste of a stimulus depends greatly on the preadapting stimulus 7. In this group o f neurons, the across-fiber patterns for HCI and QHC1 are not greatly influenced by the preadapting stimulus; however, the neural messages for sucrose, NaC1 and water modified by Brain Research, 23 (1970) 428-432

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Fig. 3. Data from 12 of the 25 neurons arranged as across-fiber patterns to show the effects of adaptation to the various stimuli. The number of impulses occurring in the first second of evoked activity is given on the ordinates; the neurons are arranged along the baselines in an arbitrary order consistent throughout the figure. Responses to each test stimulus are arranged in columns, with the different adaptation conditions appearing in the rows. For example, the responses of all stimuli following water appear in the bottom row. Not shown is the fact that these neurons did not respond to water following water (empty lower right cell). Note that the responses to any stimulus are influenced by the adapting stimulus, and that considering all stimulus conditions there are no 'specific' neurons.

the a d a p t i n g stimulus. It is interesting t h a t water elicits a taste message, especially following NaC1; this a c c o r d s well with p s y c h o p h y s i c a l d a t a which show t h a t water m a y p r o d u c e a variety o f tastes d e p e n d i n g on the species a n d c o n c e n t r a t i o n o f the prea d a p t i n g stimulus 1. A recent p a p e r o f W a n g a n d B e r n a r d 9 has p r e s e n t e d an analysis o f a d a p t a t i o n effects in g u s t a t i o n contesting the 'across-fiber p a t t e r n ' p o i n t o f view. T h e y argue in s u p p o r t o f the c o n c e p t o f a p r i m a r y receptor-taste i s o m o r p h i s m a n d a g a i n s t a p o p u l a t i o n a p p r o a c h to g u s t a t o r y coding. Their a r g u m e n t for the t r a d i t i o n a l view is t h a t g u s t a t o r y c o d i n g is m e d i a t e d by a 'few distinct r e c e p t o r types', these r e c e p t o r types being specific to one p r i m a r y taste. These a u t h o r s s u p p o r t e d this p o s i t i o n with a single n e u r o n a d a p t a t i o n study in cats. T h e i r basic d a t a were t h a t a d a p t a t i o n with a given g u s t a t o r y stimulus m a y either enhance o r d i m i n i s h the responsiveness o f an i n d i v i d u a l taste n e u r o n to a following test stimulus. In criticism o f o u r p o p u l a t i o n a p p r o a c h to g u s t a t o r y coding, which was designed to a c c o m m o d a t e b r o a d l y sensitive neurons, W a n g a n d B e r n a r d state t h a t b r o a d l y Brain Research, 23 (1970) 428-432

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431

sensitive neurons should show adaptation effects in one direction only. Since their conditioning procedures produced bidirectional adaptation effects, they concluded that taste receptors cannot be broadly sensitive, and hence coding must proceed via a few quality specific receptor types. However, there is no inherent relation between direction of adaptation effects and breadth of neural sensitivity. For example, adaptation may produce both enhancement and diminution of response in visual neurons broadly tuned across wavelengths. This being the case, Wang and Bernard's data do not provide support for narrowly tuned and thus quality specific taste neurons. Wang and Bernard also point out that taste neurons are maximally sensitive to certain stimuli and that this 'specificity' runs counter to an across-fiber pattern approach. However, no matter how broadly sensitive a neuron is, it will always have a region of maximum sensitivity. They also conclude that these points of maximum sensitivity indicate the presence of fiber types, finding 3 types with the 3 stimuli used; further, that this also is contrary to the across-fiber pattern approach. Even if their data do show the presence of fiber types, we have noted previously 5 that one of the clearest cases of across-fiber pattern encoding applies to the problems of color vision where the presence of receptor types has been amply verified. Adaptation processes introduce a multiplicity of processes which modify the responses of sensory neurons. The origins of the response modifications cannot be interpreted unambiguously in terms of the activity of single neurons considered in isolation. This is due to the fact that any given response change may have a variety of causes. In contrast, the across-fiber pattern population approach provides the mechanisms for unambiguously signaling the stimuli causing various response modifications; that is, there is a unique message for each complex stimulus situation 2-6. The across-fiber pattern approach offers a useful means for studying the diverse neural effects of adaptation, and offers suggestions for the neural bases of the psychophysics of taste adaptation. This work was supported by National Institutes of Health Grant NB-04793 and National Science Foundation Grant 020767. The illustrations were drawn by Maureen Deise. Critical comments by T. Z. Cassel are acknowledged. Department of Ophthalmology, and Department o f Psychology, Duke University, Durham, N.C. 27706 (U.S.A.)

URI YINON ROBERT P. ERICKSON

1 BARTOSHUK,L. M., MCBURNEY,D. H., ANDPFAFFMANN,C., Taste of sodium chloride solutions after adaptation to sodium chloride: Implications for 'water taste', Science, 142 (1964) 967-968. 2 DOETSCH,G. S., AND ERICKSON, R. P., Synaptic processing of taste-quality information in the nucleus tractus solitarius of the rat, J. Neurophysiol., 33 (1970) 490-507. 3 ERICKSON,R.P.,Sensory neural patterns and gustation. InY. ZOTTERMAN(Ed.), Olfaction and Taste, Pergamon, Oxford, 1963, pp. 205-213. 4 ERICKSON,R. P., Neural coding of taste quality. In M. R. KAREAND O. MALLER(Eds.), The Chemical Senses and Nutrition, Johns Hopkins Press, Baltimore, Md., 1967, pp. 313-327. Brain Research, 23 (1970)428-432

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5 ERICKSON, R. P., Stimulus coding in topographic and non-topographic afferent modalities; on the significance of the activity of individual sensory neurons, Psychol. Rev., 75 (1968) 447-465. 6 EmCKSON, R. P., DOETSCH, G. S., AND MARSHALL, D. A., The gustatory neural response function, J. gen. Physiol., 49 (1965) 247-263. 7 MCBURNEY, D. H., Effects of adaptation on human taste function. In C. PFAFt~MANN(Ed.), Ol]action and Taste, Vol. 3, Rockefeller Univ. Press, New York, 1969, pp. 407-419. 8 SATO, M., YAMASHITA, S., AND OGAWA, H., Afferent specificity in taste. In C. PFAVFMANN(Ed.), OIfaction and Taste, Vol. 3, Rockefeller Univ. Press, New York, 1969, pp. 470-487. 9 WANG, M. B., AND BERNARD, R. A., Characterization and interaction of taste responses in chorda tympani fibers of the cat, Brain Research, 15 (1969) 567-570. (Accepted August 13th, 1970)

Brain Research, 23 (1970) 428-432