Odor coding by antagonistic ON and OFF responses

Olfactory stimuli exhibit multiple features that are detected by olfactory receptor neurons against a noisy background and differentiated by the central nervous system. The use of parallel channels may overcome some limitations provided by features for which the signal-to-noise ratio is low at the input. The greater capacity, sensi- tivity and flexibility in coding by the use of parallel pathways must be investigated empirically, in anatomical, phys- iological or evolutionary terms. The cockroach is an interesting model for such research. The peripheral food-odor mediating system can be subdivided into a dual parallel pathway which originates at the periphery in two structur- ally different types of sensilla. The olfactory receptor neurons of the first sensillum type are generalist, responding to a spectrum of different food odors, those of the second type contain a pair of ON and OFF olfactory receptor neurons that responds antagonistically to changes in the concentration of a particular food odor. The ON and OFF units provide excitatory responses for both increments and decrements in odor concentration. Furthermore, they are highly sensitive to physical properties of the olfactory signal like the instantaneous odor concentration and the rate of change in odor concentration. The data suggests that different features of the olfactory signal are extracted along the dual parallel pathway, which preferentially mediate either the chemical identity of the odorant or the detection of physical properties required for odor-guided actions. These results, however, must be qualified by the different experimental procedures used in the studies on the two pathways: pulse-like changes in odor concentration in studies of the generalists and slowly oscillating concentration changes in studies of the ON and OFF units. The different response dynamics and levels of excitability could result from different stimulation tech- niques rather than from different intrinsic properties of olfactory receptor neurons. In order to exclude that physi- cal factors external to sensillum define the responses we will reinvestigate the two processing pathways with identical stimulation techniques. In the majority of physiological experiments, a reductionistic approach does not consider the time course of odor concentration stimulus by using brief on-off concentration pulses. To control the rate of concentration change, we invented a dilution flow olfactometer which delivered not only odor pulses but also slow and continu- ous changes in odor concentration at various rate (between 0.5%/s and 50%/s). Slowly oscillating concentration changes were critical for the discovery of the antagonistically responding ON and OFF olfactory receptor neurons. They are also useful for studying the ability of peripheral and higher order neurons to encode the rate of change in odor concentration and establish the existence of a dual parallel pathway at the periphery and the first level of signal processing, the AL. Two separate pathways of olfactory processing may have evolved because identifica- tion of the odorant and its use for action require quite different transformations of the olfactory signals. To be able to orientate successfully within an odor plume, it is essential that the nervous system computes not only the in- stantaneous odor concentration but also the direction and rate of its change.

The segregation of sensory information into parallel ON and OFF responses is a key process in promoting the detection of slight changes in stimulus intensity by providing excitatory signals for both stimulus increments and stimulus decrements. Examples of excitatory ON and OFF dichotomy have been found in nearly every sensory domain that has been studied with regard to this aspect, including vision, audition, touch, electro-, thermo- and hygroreception. We were first to discover the ON and OFF pathways in olfaction. Since concentration increments and decrements do not occur physically at the same time in the same place, the polarity of the responses of the neurons to changes in odor concentration resembles complementary pairs of electronic amplifiers. Using a "push-pull" arrangement, the output contrast between up and down concentration fluctuations is enhanced, leading to a high modulation depth. The ON and OFF ORNs have a remarkable capacity to detect both the instantaneous odor concentration and the rate of its change. A characteristic feature of the ORNs that distinguishes them from an artificial olfactory system, referred to as an electronic nose, is that the magnitude of the output voltage of the sensor or the voltage peak depends on odor concentration, without indicating the rate of concentration change. Of course an electronic nose can be used to determine the rate of concentration change by making readings at different time, but there is no part of its scale which refers to anything but concentration. Regarding the ORNs, there appears to be no impulse frequency which refers simply to concentration. With the simultaneous dependence on concentration and the rate of change, frequency of the ON ORN is higher at the higher concentration of the different combinations of concentration and its rate of change, and frequency of the OFF ORN is higher at the lower concentration of different combinations. We identified two mechanisms of gain control that give different weight to each of the two parameters: Robust gain control provides a stable concentration sensitivity over a range of fluctuations in odor concentrations to facilitate the representation of odor identity, and variable gain control allows an instantaneous analysis of the onset slopes of concentration fluctuations or the rates at which concentration of odor peaks increase. Our studies offer new insight into the intrinsic features of an expanding plume that are represented in the cockroach's peripheral olfactory system, enabling the insect to track odor plumes even in the absence of wind. It is hardly believable that this level of specialization is exclusively developed in the cockroach.