Coding of taste stimuli by hamster brain stem neurons

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Abstract
Mammalian taste neurons are typically broadly responsive to stimuli of different taste quality. It has been proposed that taste quality is coded by the relative amounts of activity across these broadly tuned afferents (i.e., by an across-fiber pattern). Another view holds that there are identifiable classes of taste neurons and that quality is coded by activity in these particular sets of afferents (i.e., by activity in labeled lines). The relationship between the taste neuron types in the hamster brain stem and these proposed neural codes for taste quality are examined. Multidimensional scaling of the stimulus relationships within and across the neuron groups is employed in an attempt to understand the role of these various classes of neurons in the coding of taste quality. The neural response patterns in the parabrachial nuclei (PbN) to stimuli of a particular quality are dominated by a particular class of neurons. The most active neurons in the patterns evoked by sweet-tasting stimuli are those in the S-neuron class (as defined in a previous paper). The responses of the H-neuron group dominate the patterns evoked by the acids, particularly the organic acids. Similarly, the N-neuron class dominates the patterns elicited across these neurons by the sodium salts. The exclusion of any one class of neurons from the population results in a dispersal of its most effective stimuli within a multidimensional stimulus space. Across all 31 PbN neurons, the sweet-tasting compounds elicit highly similar patterns of activity, resulting in a tight grouping of these stimuli in the stimulus space. Without the S-neurons, these stimuli no longer evoke correlated patterns of activity and are, as a result, no longer in close proximity in the stimulus space. Thus, the S-neuron group provides input that is necessary to establish similar across-neuron patterns for the sweet-tasting stimuli. Similar results obtained with the H-neurons for the patterns evoked by the nonsodium salts and acids but not for the N-neurons and the 2 sodium salts. Although a given neuron group is responsible for the similarities in the patterns elicited by a particular group of stimuli, no one class of neurons is sufficient to establish different patterns between dissimilar-tasting compounds. Multidimensional scaling of the stimulus relationships within each of the neuron classes shows that the patterns evoked by very dissimilar stimuli are often highly correlated within a neuron class. The neural distinction between many behaviorally discriminable stimuli depends on the simultaneous activity in different classes of neurons. These analyses indicate that those cells that would be termed a labeled line by one point of view determine the similarities and differences in the across-neuron patterns of activity that, according to the other view, code the tastes of the various stimuli. Particular sets of neurons are critical for coding the tastes of particular classes of stimuli, but activity in more than one group of neurons is necessary for the unambiguous coding of taste quality.

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