Pheromone responsiveness threshold depends on temporal integration by antennal lobe projection neurons

Abstract

The olfactory system of male moths has an extreme sensitivity with the capability to detect and recognize conspecific pheromones dispersed and greatly diluted in the air. Just 170 molecules of the silkmoth (Bombyx mori) sex pheromone bombykol are sufficient to induce sexual behavior in the male. However, it is still unclear how the sensitivity of olfactory receptor neurons (ORNs) is relayed through the brain to generate high behavioral responsiveness. Here, we show that ORN activity that is subthreshold in terms of behavior can be amplified to suprathreshold levels by temporal integration in antennal lobe projection neurons (PNs) if occurring within a specific time window. To control ORN inputs with high temporal resolution, channelrhodopsin-2 was genetically introduced into bombykol-responsive ORNs. Temporal integration in PNs was only observed for weak inputs, but not for strong inputs. Pharmacological dissection revealed that GABAergic mechanisms inhibit temporal integration of strong inputs, showing that GABA signaling regulates PN responses in a stimulus-dependent fashion. Our results show that boosting of the PNs' responses by temporal integration of olfactory information occurs specifically near the behavioral threshold, effectively defining the lower bound for behavioral responsiveness.optogenetics | pheromone orientation behavior | transgenic silkmoth | olfaction O lfaction is a key element in many aspects of animal behavior, such as foraging, oviposition, and mate recognition. In many moth species, a special class of odorants called sex pheromones plays a critical role for identification of and orientation to potential mates. Because sex pheromones emitted by females are greatly diluted and dispersed in the air, sophisticated olfactory systems to detect minute amounts of sex pheromones and processing systems to translate subtle peripheral sensory responses into appropriate behavioral responses have evolved in male moths. Theoretical calculations have shown that the detection of 170 molecules of the sex pheromone bombykol [(E,Z)-10,12-hexadecadienol] can trigger sexual behavioral responses in males of the silkmoth Bombyx mori (1). The physical and chemical mechanisms in the antennae, the sensilla, and the olfactory receptor neurons (ORNs) responsible for this remarkably high sensitivity, which can detect even a single molecule, are well understood (2, 3). However, it is unclear how a small number of spikes from a small number of ORNs is processed centrally to allow for high behavioral responsiveness.In moths, pheromone molecules are detected by specialized antennal ORNs that express particular pheromone receptor genes (4-10). The axons of ORNs convey pheromone information to the first olfactory center, the antennal lobe (AL; an analog of the vertebrate olfactory bulb). The AL is composed of a number of glomeruli where ORNs establish connections with two types of neurons: projection neurons (PNs), which relay olfactory information to higher brain regions, and local interneurons (LNs), which are involved ...

Natural search algorithms as a bridge between organisms, evolution, and ecology

“…Dictyostelium cells can detect concentration gradients amounting to differences in the occupancy of only five chemoattractant receptors between the up-gradient and down-gradient sides of the cell (41). Silkmoths detect and respond to as few as 170 molecules of sex pheromone by temporally integrating subthreshold activity of olfactory receptor neurons (8). Sensitivity often comes at the cost of susceptibility to noise, raising the question of what kinds of environmental conditions could have selected for such extreme sensitivity.…”

“…Many organisms studied in the laboratory readily execute search behaviors and research groups are already using techniques like computer vision, virtual reality, microfabricated landscapes, and optogenetics to measure and manipulate search behavior and to link sensory input to behavioral output (8,(65)(66)(67). The high-resolution data such studies generate provide the kind of information needed to build and parameterize mathematical models of search strategies.…”

“…Knowledge of the proximate mechanisms that organisms use to capture and integrate sensory information will help address these and other fundamental ecological and evolutionary questions. The flow of ideas can and has also moved in the opposite direction; understanding the selective pressures imposed by the need to search effectively and the physical properties of search environments can help to reveal the function of neural and biophysical structures (e.g., bursting olfactory receptor neurons) (11,58), and may also help explain the striking sensitivity of many sensory organs (8,45,99). Progress in these and other areas will benefit from a more formal integration of studies of sensory biology and decision-making, the physics and ecology of search environments, and the evolution of search strategies by natural selection.…”

Smelling Time: A Neural Basis for Olfactory Scene Analysis

“…Animals could use a different coding strategy than the bORN ensemble strategy to encode short time scales that match or approach the time scale of typical neuronal dynamics. In moths, for example, PNs temporally integrate weak odor signals to increase the sensitivity of the system over a time scale that corresponds well to the most rapid (<80 msec) temporal dynamics of odor signals in the natural environment [35]. While insects also deal with slower odor signals, how they do so is unclear.…”

Illuminating odors: when optogenetics brings to light unexpected olfactory abilities

“…For example, one can express ChR2 in a particular subset of neurons and stimulate them while investigating the response of other neuron subsets one by one. This was achieved in a recent study that uses insects as a system model (Tabuchi et al 2013). In insects, ORNs project to a structure called the antennal lobe, where they connect to the projection neurons (PNs).…”