Independent processing of increments and decrements in odorant concentration by ON and OFF olfactory receptor neurons

Abstract

A salient feature of the insect olfactory system is its ability to detect and interpret simultaneously the identity and concentration of an odorant signal along with the temporal stimulus cues that are essential for accurate odorant tracking. The olfactory system of the cockroach utilizes two parallel pathways for encoding of odorant identity and the moment-to-moment succession of odorant concentrations as well as the rate at which concentration changes. This separation originates at the peripheral level of the ORNs (olfactory receptor neurons) which are localized in basiconic and trichoid sensilla. The graded activity of ORNs in the basiconic sensilla provides the variable for the combinatorial representation of odorant identity. The antagonistically responding ON and OFF ORNs in the trichoid sensilla transmit information about concentration increments and decrements with excitatory signals. Each ON and OFF ORN adjusts its gain for odorant concentration and its rate of change to the temporal dynamics of the odorant signal: as the rate of change diminishes, both ORNs improve their sensitivity for the rate of change at the expense of the sensitivity for the instantaneous concentration. This suggests that the ON and OFF ORNs are optimized to detect minute fluctuations or even creeping changes in odorant concentration.

ON selectivity in the Drosophila visual system is a multisynaptic process involving both glutamatergic and GABAergic inhibition

“…One prominent example is the split into ON and OFF pathways, where individual neurons become selective to either increases (ON) or decreases (OFF) in a signal. Such an ON/OFF dichotomy enables more efficient coding of stimuli in the visual system (Gjorgjieva et al, 2014) and occurs across many different species and sensory modalities, such as vision, olfaction, audition, thermosensation, and electrolocation (Bennett, 1971; Gallio et al, 2011; Scholl et al, 2010; Tichy and Hellwig, 2018; Werblin and Dowling, 1969). Examples of how the split into ON and OFF pathways is implemented in sensory information processing have already been described.…”

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

“…Neuroanatomical and electrophysiological studies show that these sensilla are located on the distal and proximal margins of each of the 120–180 antennal segments. They make up about 6% of the olfactory sensilla in the male cockroach (Schaller, 1978; Burgstaller and Tichy, 2012; Tichy and Hellwig, 2018). Inserting the tip of a needle electrode into the sensillum base enables recording the action potentials of both ORN types at the same time.…”

“…In this way, concentration increments and decrements are encoded by excitatory signals. During slow and continuous concentration changes, both types of ORNs not only signal the moment-to-moment succession of odorant concentrations but also the rate at which concentration changes (Burgstaller and Tichy, 2011, 2012; Tichy and Hellwig, 2018). Furthermore, the rate of concentration change modulates the gain of responses for fluctuations in the odorant concentration.…”

“…Electrophysiological recordings provide evidence for the existence of “pulse slope detectors” on chemoreceptors of the lateral antennules of the American lobster (Zettler and Atema, 1999). In the cockroach, the ON and OFF ORNs on the antennae meet the requirements of detectors for the upward and downward rate of change of the food odor concentration (Tichy and Hellwig, 2018). If the rate of concentration change is truly a fundamental aspect of insect orientation in an odorant plume, information about the concentration rate should be robust across a range of different flow velocities.…”

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

“…Does an increase in the rate of concentration increase determine the ORNs performance in detecting concentration differences along a gradient? There is no definite answer, but electrophysiological experiments with a specific type of ON and OFF ORNs located in morphologically identifiable single-walled trichoid (swC) sensilla on the cockroach's antenna revealed that the differential sensitivity or the gain of responses for the rate of concentration change decreases rather than increases with rising rate of change (Burgstaller and Tichy, 2012;Tichy et al, 2016;Tichy and Hellwig, 2018). The high gain for slow rates of change improves the cockroach's ability to detect slowly fluctuating or creeping concentration changes which persist in one direction.…”