Food odor coding by parallel ON and OFF responses

Previous studies from our laboratory have demonstrated the existence of ON and OFF olfactory receptor cells on the antennae of the cockroach which respond antagonistically to fluctuating changes in the concentration of food odor. This segregation of the olfactory input provides excitatory signals for both increments and decrements in food odor concentration. Since both types of cells are responding simultaneously to the same change in odor concentration, they are able to enhance the temporal profile of an odor signal in order to maximize the steady flow of food odor information to the brain. When presented with slow and continuous changes in odor concentration, the ON and OFF olfactory receptor cells display a dependence on both the concentration and the rate with which concentration changes. The impulse frequency of the ON cell is higher at the higher odor concentration values and is lower at the lower values; conversely, the impulse frequency of the OFF cell is higher at the lower concentrations and is lower at the higher values. In general, however, the faster the rate of increase becomes, the higher the frequency of the ON cell, and conversely, the faster the rate of decrease, the higher the frequency of the OFF cell. Thus, the effect of odor concentration on both cells is reinforced by the rate of change. That nature has gone to such complexities suggests that great benefits must be reaped from parallel ON and OFF responses for the analysis of food odor information. In this project, we address the role of the ON and OFF responses in optimizing the transfer of temporal information about changing food odor concentration. As walking insects face very different problems from flying insect when searching for an odor source, we will make a comparative study of the nocturnal cockroach Periplaneta americana and the noctuid moth Agrotis ipsilon. We will determine how much information about the food odor stimuli can be extracted from the impulse discharges of ON and OFF olfactory receptor cells and how much information is available from processing the momentary state of activity in ON and OFF antennal lobe neurons. The question is whether the olfactory systems in both insect species employ common principles of signal processing, based on the ON and OFF olfactory receptor cells and the ON and OFF antennal lobe neurons. All the studies of odor information transfer from olfactory receptor cells to antennal lobe neurons used brief pulse- like changes in odor concentration, nothing is known about the transfer of long-lasting odor pulses or slow and continuous changes in odor concentration. We invented a dilution flow olfactometer that delivered not only abrupt, pulse-like changes in odor concentration but also slow and continuous ramp-like and even sinusoidal changes in odor concentration, i.e., odor pulses that are shaped like a rectangle, a trapezoid or a sine wave. It is critical to understand how stimulus dynamics influence the olfactory responses in antennal receptor cells and antennal lobe neurons before we can fully interpret olfactory information coding

In the cockroach peripheral olfactory system, the segregation of fruit odor information into parallel ON and OFF responses is a key process in promoting the detection of slight changes in odor concentration by providing excitatory signals for both increments and decrements. Since both types of olfactory receptor neurons are responding oppositely to the same change in odor concentration, they are able to enhance the temporal profile of an odor signal in order to maximize the steady flow of food odor information to the brain. To understand the functional role of parallel olfactory processing by means of the ON and OFF olfactory receptor neurons, a detailed knowledge of their response characteristics is required. In the first paper we demonstrate that odor concentration held at a constant level has a twofold effect on the discharge rates of the ON and OFF olfactory receptor neurons (Burgstaller M, Tichy H (2011) J Neurophysiol 105: 834-845). (1) While odor concentration is constant, both types of olfactory receptor neurons maintain a continuous discharge with a constant frequency that depends on the concentration level. (2) When both cell types are presented with changes in odor concentration, the discharge rate is affected simultaneously by the magnitude of the change and by the level from which the change was initiated. The ON olfactory receptor neurons discharge rate is high when the concentration jump is large, but for a given jump, frequency tends to be higher still when the initial concentration is also low. The frequency of the OFF olfactory receptor neurons is high at large concentration drops, but higher still when the initial concentration is also low. Thus, the effect of changing odor concentrations on the responses of both the ON and OFF olfactory receptor neurons is reinforced by falling initial odor concentrations. In the second paper we report that during slowly oscillating changes in the concentration of the odor of lemon oil the ON and OFF olfactory receptor neurons adapt to changes in the actual concentration and the rate at which concentration changes (Burgstaller M, Tichy H (2012) Eur J Neuroscience 35: 519-526). When odor concentration oscillates rapidly with brief periods, adaptation improves the gain for instantaneous concentration and reduces the gain for the rate of concentration change. Conversely, when odor concentration oscillates slowly with long periods, adaptation increases the gain for the rate of change at the expense of instantaneous concentration. The signals controlling gain must be derived directly from the stimulus input or from a signal of the olfactory receptor neurons itself. This may limit the accuracy with which gain can be controlled, but it permits the olfactory receptor neurons to operate over a wide range of stimulus conditions and to maintain sensitivity as the olfactory input changes.