Chemosensory Coding At The Periphery

In the real world, animals encounter thousands of chemicals. Most of these are meaningless, in the sense that no behavioral response is required, whereas some are critical. A sensory system thus serves two opposing functions. First, the effective sensory system must act as a filter, allowing the animal to ignore most potential stimuli so that it can concentrate on the important ones. Second, the same system must be sensitive, sometimes exquisitely sensitive, to biologically relevant stimuli and must continuously transmit a "summary" report to the brain or central nervous system. The receptor proteins and associated transduction molecules provide the specificity (only some things are adequate stimuli) and sensitivity (the effectiveness of the amplification step in transduction). The nature of the summary neural message is the problem addressed in studies of peripheral sensory coding. In insect chemosensory coding, the problem can be as simple as a few highly specific receptor proteins recognizing a three- or four-component blend of pheromone molecules all housed on a pair of cells found in each of many thousand antennal sensilla. At the other extreme, a leaf beetle may be faced with a food choice of two closely related plants, each with many chemicals to which its tens of gustatory cells are capable of responding. When one is comparing these two scenarios, it is not the number of sensory cells that constitutes the relative scale of the coding problem, but the number of chemical compounds that can be sensed by these cells, and the combinations of compounds that are possible.

In the pheromone example, there are two cell types (each sensillum has one of each type). They respond differently to, for example, four pheromone molecules and not much else. Also, one or two of the pheromone molecules may be completely nonstimulatory to one of the two cells. In addition, only two of the four compounds in the blend may be sufficient to stimulate a full array of behaviors necessary for the male to find the female. The coding problem, though overly simplified to make the point, could thus be reduced to the following: cell A responds only to compound A, and cell B responds only to compound B. Both cells continuously signal to the antennal lobe the levels of compounds A and B detected in the air. If cell A is firing at twice the rate of cell B and both cells are firing at some rate, then the moth flies upwind. Thus the code is a simple comparison, and the large number of cells involved is a kind of amplifier, reflecting the overwhelming importance of the pheromone system to the animal. The two cells, A and B in this example, can be thought of as labeled lines, each sending unique information about the concentration of compound A or B. The central nervous system uses a simple hardwired rule to compare this paired input, and, accordingly, behavior is or is not released.

The beetle, potentially, has a more difficult coding problem. Many experiments have shown that gustatory cells of plant-feeding insects are affected by numerous single plant compounds. Ubiquitous compounds such as water, salts, amino acids, and sugars are sensed by some cells on the mouthparts of all such insects. Less widely distributed chemicals such as alkaloids, terpenes, glucosinolates, and other so-called secondary plant compounds, are stimuli for cells that are variously scattered throughout the class Insecta. To exemplify this coding problem, consider a Colorado potato beetle facing the choice of a potato leaf (host plant) or a tomato leaf (marginal host) (Fig. 4A). The gustatory cells in the beetle's mouthpart sensilla (on the galea), are all sensitive to different compounds. Both direct stimulation by some molecules and inhibition of one molecule by another are known, as are some injury effects in the presence of when too much glycoalkaloid (compounds in potatoes and tomatoes). Not surprisingly, the summary report such a four-cell system sends to the brain comprises two kinds of message, one for potato and one for tomato (Fig. 4B). The complex array of stimuli represented by potato actually stimulate a single cell—the others may well be inhibited. The tomato leaf juice, on the other hand, causes several cells to fire in an inconsistent pattern. The first is another example of a labeled-line type of code; while the second is an across-fiber pattern. In the latter type of code, the brain is receiving information from several physiologically distinct cells, and it is the pattern that is important. It is thought that the across-fiber code pattern prevails in many situations involving complex chemical mixtures. Progress in this area is impeded by the inherent variability of the types of recording possible in the across-fiber pattern (see, e.g., Fig. 4B).

FIGURE 4 (a) Summary of the behaviors exhibited by newly emerged Colorado potato beetle adults when provided with either potato (host plant) or tomato (nonhost plant); numbers of beetles indicated inside heavy arrows. Beetles first examine the leaf, then they squeeze it between their mandibles (macerate) before taking a small bite, which they taste for only a short time. If the plant is acceptable, they very quickly move to sustained feeding. If the plant is less acceptable, few beetles will feed. The decision to not feed is made after considerable time has been spent in examining, macerating, taking small bites, and sometimes repeating one or more of these steps. [Modified from Harrison, G. D., (1987). Host—plant discrimination and evolution of feeding preferences in the Colorado potato beetle, Leptinotarsa decemlineata. Physiol. Entomol. 12, 407—415.] (b) Taste sensilla are important in making the kinds of decisions shown in (a). If potato leaf juice is the stimulus, four cells in nine sensilla on the mouthparts respond by sending a clear, almost labeled-line (cell 1), message to the central nervous system. When tomato leaf juice is the stimulus, a mixed message is provided from the four cells housed in each of the nine sensilla, and this message varies considerably across the available sensilla. The result is a type of acrossfiber pattern that signals "do not eat." [Modified from Haley Sperling, J. L., and Mitchell, B. K. (1991). A comparative study of host recognition and the sense of taste in Leptinotarsa. J. Exp. Biol. 157, 439-459. © Company of Biologists LTD.]

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