ABSTRACT
In many sensory systems adaptation acts as a gain control mechanism that optimizes sensory performance by trading increased sensitivity to low stimulus intensity for decreased sensitivity to high stimulus intensity. Adaptation of insect antennal olfactory receptor neurons (ORNs) has been studied for strong odour concentrations, either pulsed or constant. Here, we report that during slowly oscillating changes in the concentration of the odour of lemon oil, the ON and OFF ORNs on the antenna of the cockroach Periplaneta americana adapt to the actual odour concentration and the rate at which concentration changes. When odour concentration oscillates rapidly with brief periods, adaptation improves gain for instantaneous odour concentration and reduces gain for the rate of concentration change. Conversely, when odour concentration oscillates slowly with long periods, adaptation increases gain for the rate of change at the expense of instantaneous concentration. Without this gain control the ON and OFF ORNs would, at brief oscillation periods, soon reach their saturation level and become insensitive to further concentration increments and decrements. At long oscillation periods, on the other hand, the cue would simply be that the discharge begins to change. Because of the high gain for the rate of change, the cockroach will receive creeping changes in odour concentration, even if they persist in one direction. Gain control permits a high degree of precision at small rates when it counts most, without sacrificing the range of detection and without extending the measuring scale.
Subject(s)
Action Potentials/physiology , Adaptation, Physiological/physiology , Olfactory Receptor Neurons/physiology , Sense Organs/cytology , Smell/physiology , Action Potentials/drug effects , Animals , Cockroaches/physiology , Dose-Response Relationship, Drug , Male , Odorants , Periodicity , Plant Oils/pharmacology , Regression Analysis , Time FactorsABSTRACT
The ON and OFF olfactory receptor neurons (ORNs) on the antenna of the American cockroach respond to the same changes in the concentration of the odor of lemon oil, but in the opposite direction. The same jump in concentration raises impulse frequency in the ON and lowers it in the OFF ORN and, conversely, the same concentration drop raises impulse frequency in the OFF and lowers it in the ON ORN. When the new concentration level is maintained, it becomes a background concentration and affects the responses of the ON and OFF ORNs to superimposed changes. Raising the background concentration decreases both the ON-ORN's response to concentration jumps and the OFF-ORN's response to concentration drops. In addition, the slopes of the functions approximating the relationship of impulse frequency to concentration changes become flatter for both types of ORNs as the background concentration rises. The progressively compressed scaling optimizes the detection of concentration changes in the low concentration range. The loss of information caused by the lower differential sensitivity in the high concentration range is partially compensated by the higher discharge rates of the OFF ORNs. The functional asymmetry of the ON and OFF ORNs, which reflects nonlinearity in the detection of changes in the concentration of the lemon oil odor, improves information transfer for decrements in the high concentration range.
