Multielectrode recordings of cockroach antennal lobe neurons in response to temporal dynamics of odor concentrations.

The initial representation of the instantaneous temporal information about food odor concentration in the primary olfactory center, the antennal lobe, was examined by simultaneously recording the activity of antagonistic ON and OFF neurons with 4-channel tetrodes. During presentation of pulse-like concentration changes, ON neurons encode the rapid concentration increase at pulse onset and the pulse duration, and OFF neurons the rapid concentration decrease at pulse offset and the duration of the pulse interval. A group of ON neurons establish a concentration-invariant representation of odor pulses. The responses of ON and OFF neurons to oscillating changes in odor concentration are determined by the rate of change in dependence on the duration of the oscillation period. By adjusting sensitivity for fluctuating concentrations, these neurons improve the representation of the rate of the changing concentration. In other ON and OFF neurons, the response to changing concentrations is invariant to large variations in the rate of change due to variations in the oscillation period, facilitating odor identification in the antennal-lobe. The independent processing of odor identity and the temporal dynamics of odor concentration may speed up processing time and improve behavioral performance associated with plume tracking, especially when the air is not moving.

The Performance of Olfactory Receptor Neurons: The Rate of Concentration Change Indicates Functional Specializations in the Cockroach Peripheral Olfactory System.

Slow and continuous changes in odor concentration were used as a possible easy method for measuring the effect of the instantaneous concentration and the rate of concentration change on the activity of the olfactory receptor neurons (ORNs) of basiconic sensilla on the cockroach antennae. During oscillating concentration changes, impulse frequency increased with rising instantaneous concentration and this increase was stronger the faster concentration rose through the higher concentration values. The effect of the concentration rate on the ORNs responses to the instantaneous concentration was invariant to the duration of the oscillation period: shallow concentration waves provided by long periods elicited the same response to the instantaneous concentration as steep concentration waves at brief periods. Thus, the double dependence remained unchanged when the range of concentration rates varied. This distinguishes the ORNs of basiconic sensilla from those of trichoid sensilla (Tichy and Hellwig, 2018) which adjust their gain of response according to the duration of the oscillating period. The precision of the ORNs to discriminate increments of slowly rising odor concentration was studied by applying gradual ramp-like concentration changes at different rates. While the ORNs of the trichoid sensilla perform better the slower the concentration rate, those of the basiconic sensilla show no preference for a specific rate of concentration increase. This suggests that the two types of sensilla have different functions. The ORNs of the trichoid sensilla may predominately analyze temporal features of the odor signal and the ORNs of the basiconic sensilla may be involved in extracting information on the identity of the odor source instead of mediating the spatial-temporal concentration pattern in an odor plume.

Developing and testing of an air dilution flow olfactometer with known rates of concentration change.

BACKGROUND: Concentration is a variable aspect of an odor signal and determines the operation range of olfactory receptor neurons (ORNs). A concentration increase is perceived as an odor stimulus. The role that the rate of concentration increase plays thereby has been studied with electrophysiological techniques in ORNs of the cockroach. A key prerequisite for these studies was the development of an air dilution flow olfactometer that allowed testing the same change in concentration at various rates. NEW METHOD: The rate of concentration change was controlled and varied by changing the mixing ratio of odor-saturated and clean air by means of proportional valves. Their input voltages were phase shifted by 180° to hold the mixed air at a particular constant volume flow rate. RESULTS: Using this stimulation technique, we identified, in a morphologically distinct sensillum on the cockroach's antenna, antagonistically responding ON and OFF ORNs which display a high sensitivity for slow changes in odor concentration. COMPARISON WITH EXISTING METHODS: The olfactometer is unique because it enables delivering slowly oscillating concentration changes. By varying the oscillation period, the individual effects of the instantaneous odor concentration and its rate of change on the ORNs' responses can be determined. CONCLUSIONS: The olfactometer provides a new experimental approach in the study of odor coding and opens the door for improved comparative studies on olfactory systems. It would be important to gain insight into the ORNs' ability to detect the rate of concentration change in other insects that use odors for orientation in different contexts.

Encoding of Slowly Fluctuating Concentration Changes by Cockroach Olfactory Receptor Neurons Is Invariant to Air Flow Velocity.

The ON and OFF olfactory receptor neurons (ORNs) on the cockroach antenna display a high sensitivity for the rate at which odorant concentration changes. That rate of change acts as a gain control signal that improves the sensitivity of both ORNs for fluctuating concentration changes. By means of extracellular recording techniques, we find in both types of ORNs an increased gain for the rate of concentration change when the duration of the oscillation period increases. During long-period oscillations with slow concentration changes, the high gain for the rate of concentration change improves the ORNs ability to detect low rates of concentration changes when the fluctuations are weak. To be useful in plume tracking, gain control must be invariant to the air flow velocity. We describe that raising the level of the flow rate has no effect on the ON-ORN responses to concentration changes down to rates of 2%/s, but exerts a slight increase on the OFF-ORN response during these extremely low rates. At 4%/s, however, the OFF-ORN response is also unaffected by the flow rate level. The asymmetry corresponds with a generally higher sensitivity of the OFF-ORN to concentration changes. Nevertheless, the gain of both ORNs for the concentration rate change is robust against the air flow velocity. This makes possible an instantaneous analysis of the rate of concentration change for both directions of change by one or the other ORN. Therefore, the ON and OFF ORNs are optimized to encode concentration increments and decrements in a turbulent odorant plume.