Antennal lobe representations are optimized when olfactory stimuli are periodically structured to simulate natural wing beat effects

Abstract

Animals use behaviors to actively sample the environment across a broad spectrum of sensory domains. These behaviors discretize the sensory experience into unique spatiotemporal moments, minimize sensory adaptation, and enhance perception. In olfaction, behaviors such as sniffing, antennal flicking, and wing beating all act to periodically expose olfactory epithelium. In mammals, it is thought that sniffing enhances neural representations; however, the effects of insect wing beating on representations remain unknown. To determine how well the antennal lobe (AL) produces odor dependent representations when wing beating effects are simulated, we used extracellular methods to record neural units and local field potentials (LFPs) from moth AL. We recorded responses to odors presented as prolonged continuous stimuli or periodically as 20 and 25 Hz pulse trains designed to simulate the oscillating effects of wing beating around the antennae during odor guided flight. Using spectral analyses, we show that ~25% of all recorded units were able to entrain to “pulsed stimuli”; this includes pulsed blanks, which elicited the strongest overall entrainment. The strength of entrainment to pulse train stimuli was dependent on molecular features of the odorants, odor concentration, and pulse train duration. Moreover, units showing pulse tracking responses were highly phase locked to LFPs during odor stimulation, indicating that unit-LFP phase relationships are stimulus-driven. Finally, a Euclidean distance-based population vector analysis established that AL odor representations are more robust, peak more quickly, and do not show adaptation when odors were presented at the natural wing beat frequency as opposed to prolonged continuous stimulation. These results suggest a general strategy for optimizing olfactory representations, which exploits the natural rhythmicity of wing beating by integrating mechanosensory and olfactory cues at the level of the AL.

Co-option of a motor-to-sensory histaminergic circuit correlates with insect flight biomechanics

“…Local field potentials within the AL have also been shown to respond to fluctuations at least up to approximately 70 Hz [22], well within the range of Lepidopteran wing-beat frequencies. In addition, neural population responses from the AL of M. sexta track and represent olfactory stimuli optimally when odours are presented at the wing-beat frequency [23]. This finding also corresponds to enhanced olfactory acuity as measured behaviourally [55], supporting the conclusion that their olfactory system has adapted to encode information that is embedded within a temporal structure induced by their own active sampling behaviour.…”

“…This suggests that while the MDHns may be present in many insect taxa, they do not necessarily innervate the olfactory system, which may reflect differences in the impact of species-specific flight mechanics on odour plumes [20,21]. The olfactory system of M. sexta is able to track odours pulsed at the wing-beat frequency [22,23], so we, therefore, hypothesized that MDHn innervation of the AL arose because of selective pressures associated with a need to process odours carried by flight-induced air flow oscillations during plume tracking. We used a comparative approach to determine when over evolutionary time the MDHns began to innervate the AL and if this trait was lost with the evolution of different flight biomechanics within the Lepidoptera.…”

Olfactory coding in the turbulent realm

“…The dynamic of odorant reaching the insect antenna depends not only on the turbulence but also on active olfactory sampling behaviors including wing beating, antennal flicking and body displacement [74,81,82]. In realistic olfactory searches strong correlations in detection dynamics (time and concentration) are due to the strategy implemented by moths.…”

Direct inhibition of histamine receptors in the antennal lobe of Manduca sexta: Putative evidence for an olfactory corollary discharge circuit

“…Thus, as the moth crosses into a plume, packets of odor within the plume are experienced as discontinuous pulses that entrain to the wing beat. Accordingly, physiological studies of olfactory processing as well as behavioral studies of olfactory acuity demonstrate that simulating wing beat effects on airflow enhances olfactory function (Daly et al, 2013;Houot et al, 2014;Tripathy et al, 2010;). For example, electroantennogram measures, AL local field potentials and spiking in both LNs and PNs all entrain to olfactory stimuli that match the natural wing beat frequency.…”

“…Furthermore, in flight, the insect is constantly being exposed to the forces of oscillating airflow caused by wing flapping. Interestingly, as with sniffing in mammals (Mainland and Sobel, 2006), the olfactory pathway respond to these "clean-air" mechano-sensory stimuli at wing beat frequencies that are preferentially tracked and processed by the (AL; Houot et al, 2014;Tripathy et al, 2010). Although the mechanism for mechanosensory driven activation of AL neurons has not been identified in insects, in mammals it is the olfactory receptors themselves that transduce the mechanosensory signals (Connelly et al, 2015;Grosmaitre et al, 2007).…”