1.8 Taste
1.8.1 Why do vertebrates possess separate gustatory and olfactory systems?
If the difference between taste and olfaction in vertebrates were, as in C. elegans, that the former detects soluble molecules and the latter detects airborne ones (Pierce-Shimomura et al., 2001), then how does one explain the fact that fish have both? For this reason, vertebrate olfaction is defined as chemical information transmitted to the central nervous system (CNS) by neurons through cranial nerve I, while chemical information detected by specialized epithelial cells and trans- mitted to the CNS by cranial nerve VII (facial), IX (glosopharyngeal), or X (vagal) is termed gustation
5. The Cramer-Rao lower bound on the mean squared error of estimation used by Zhang and Sejnowski bounds the error rate given the amount of information present in the encoding variable chosen. But nothing guarantees that Zhang and Sejnowski’s choice, neuronal firing rates during a time window Tau, are the opti- mal encoding variable or the one used by the brain. With 1 or few spikes per perceptual event per neuron, mean firing rate may constitute a comparatively poor source of information. Perhaps spike timing, an analog quantity, is a better way to go to optimize estimation.
Zhang and Sejnowski’s theoretical results suggest that the accuracy of a 2-D code should be unaffected by the width of the tuning curves. Nevertheless, multiple parallel maps, exhibiting neuronal tuning with differ- ent widths, are universal in sensory systems, even when they do not exist at the sensory periphery (Konishi, 1986; Lewis and Maler, 2001). Maps with greater tuning widths have been found to result in equal accuracies of estimation for some parameters, greater accuracies for others and smaller accuracies for others still (Lewis and Maler, 2001).
Finally, it must also be noted that although Zhang and Sejnowski suggested the Fisher information per neuron increases with increasing tuning width for stimulus dimensionalities greater than 2, they showed that Fisher information per spike always decreases with increasing tuning width. If energetic considerations pre- vail, the latter could be more relevant.
Taste
or taste (Hara, 1994). While this makes the definition unambiguous, it leaves unanswered the ques- tion of why two separate and apparently nonhomologous systems evolved. If fish were the descen- dants of land vertebrates, it could be hypothesized that olfaction originally evolved for the detection of volatiles in land animals, and taste evolved for the detection of soluble molecules, and that olfac- tion was later adapted to detect soluble molecules in fish. But our current understanding of verte- brate evolution maintains that the original vertebrate precursors were aquatic (Encyclopaedia Brittannica Online, 2001).
A second possibility is that gustation evolved to sense ingested molecules, while olfaction evolved to sense the surroundings. There are two problems with this hypothesis. The first is that external taste buds are common in fish: the yellow bullhead (Ictalurus natalis), for example, has taste buds
Figure 1.1. Specialist and generalist coding in taste neurons. Each neuron was tested for its sensitivity to 4 chemicals: 0.5 M sucrose, 0.1 M NaCl, 0.01 M HCl, and 0.02 M QHCl. The solid black bar below each spike record represents the duration of stimulus application (15 s) (reproduced from Lundy and Contreras, 1999).
Taste
on its entire body surface (Hara, 1994). This problem could be dismissed if this was a secondary adaptation not present in the original vertebrates. The second problem, though, is that even if their locations in the body are different, it is not clear why the same original system could not be co-opted to a different location.
Interestingly, in Drosophila, the 33 aminoacid signature motif characteristic of the GR gustatory gene family is present but somewhat diverged in33 of the 60 members of thefamily of Drosophila odorant receptor (DOR) genes. The DORgenes, however, possess additional conserved motifs not present inthe GR genes and define a distinctfamily (Clyne et al., 1999; Gao and Chess, 1999;
Vosshall et al., 1999, 2000). Indeed, the gustatory receptors are anextraordinarily divergent family, of which the odorant receptorsare in fact just a single branchamong many (Robertson, 2001). This great divergence hints atgreat antiquity, and indeed five geneshave been found that form three lin- eages within the gustatory familyin the nematode Caenorhabditis elegans genome, indicating that the superfamily predates the nematode—arthropod divergence (Robertson, 2001). These observa- tions suggest that the putativegustatory and olfactory receptor gene families mayhave evolved from a common ancestral gene (Scott et al., 2001). Consistent with a common origin, in insects, both types of receptors may be found side-by-side, not localized to different organs as in vertebrates (Schneider, 1963).
In agreement with the large size of the family of taste receptor genes, in fish, taste appears to respond to a wide spectrum of compounds (Kotrschal, 2000). So the size of the stimulus space is unlikely to be the critical distinction between olfaction and taste. In contrast, the difference between them appears to lie in their behavioral outputs. Whereas stimulation of the taste systems alone trig- gers reflexes, complex, conditional or conditioned behaviors occur only when the olfactory system is intact (Kotrschal, 2000). Thus, our responses to different tastes are to a large degree hardwired — thus the ease with which terms adapted from taste, such as sour and sweet, are co-opted for other
Taste
meanings, meaning which are constant across cultural barriers. Descriptions of odors, on the other hand, have a much greater cultural or experience-dependent component, and are therefore imprac- tical as descriptors outside their specific realm.
Finally, olfaction appears to work at low thresholds, designed for remote sensing, while taste appears to operate with higher thresholds and designed mainly for close-distance discrimination (Kotrschal, 2000).