Odors pulsed at wing beat frequencies are tracked by primary olfactory networks and enhance odor detection

Tripathy, Shreejoy J.; Peters, Oakland J.; Staudacher, Erich M.; Kalwar, Faizan; Hatfield, Mandy; Daly, Kevin C.

doi:10.3389/neuro.03.001.2010

Cited by 62 publications

(127 citation statements)

References 81 publications

(125 reference statements)

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“…Previous studies reported maximum odor-tracking frequencies between 5 and 50 Hz in EAG and single ORN recordings (12-14, 16, 18, 38, 39) and between 10 and 30 Hz in olfactory interneurons in the antennal lobe (17,40,41). These lower maximum pulse tracking frequencies might reflect the low-pass filter properties of the odor delivery devices.…”

Section: Discussionmentioning

confidence: 90%

“…Olfactory transduction speed has never been measured directly, and estimates range from 10 to 30 ms (8)(9)(10)(11). Previous studies suggest that the maximum pulse tracking frequency of ORNs is species specific and ranges from 5 to 50 Hz (12)(13)(14)(15)(16)(17)(18)(19). However, these numbers do not match the high temporal resolution observed in behavioral studies (2)(3)(4)(5)(6)(7).…”

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confidence: 98%

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High-speed odor transduction and pulse tracking by insect olfactory receptor neurons

Szyszka

Gerkin

Galizia

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

115

101

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Sensory systems encode both the static quality of a stimulus (e.g., color or shape) and its kinetics (e.g., speed and direction). The limits with which stimulus kinetics can be resolved are well understood in vision, audition, and somatosensation. However, the maximum temporal resolution of olfactory systems has not been accurately determined. Here, we probe the limits of temporal resolution in insect olfaction by delivering high frequency odor pulses and measuring sensory responses in the antennae. We show that transduction times and pulse tracking capabilities of olfactory receptor neurons are faster than previously reported. Once an odorant arrives at the boundary layer of the antenna, odor transduction can occur within less than 2 ms and fluctuating odor stimuli can be resolved at frequencies more than 100 Hz. Thus, insect olfactory receptor neurons can track stimuli of very short duration, as occur when their antennae encounter narrow filaments in an odor plume. These results provide a new upper bound to the kinetics of odor tracking in insect olfactory receptor neurons and to the latency of initial transduction events in olfaction.olfaction | olfactory receptor neurons | odor transduction | temporal resolution | insect O dors carried in air plumes quickly break up into thin filaments that spread out across short distances from an odor source (1). The ability to track the temporal structure of filaments in an odor plume is essential for insects to segregate concurrent odors that arise from different sources (2-6). However, it is not clear whether signal transduction times and tracking rates of olfactory receptor neurons (ORNs) are fast enough to allow animals to use the higher frequency components of information present in odor plumes. Insect odor-guided behavior is remarkably robust against the spatial and temporal variability inherent in olfactory stimuli. For example, moths and beetles use temporal stimulus cues to segregate concurrent odors from closely spaced sources (2-5), and honey bees can detect 6-ms asynchrony in the onset of concurrent odor stimuli and use this onset asynchrony to segregate concurrent odors (6, 7). These observations of fast temporal resolution challenge the frequent notion that olfaction has slow integration times relative to other senses. Olfactory transduction speed has never been measured directly, and estimates range from 10 to 30 ms (8-11). Previous studies suggest that the maximum pulse tracking frequency of ORNs is species specific and ranges from 5 to 50 Hz (12-19). However, these numbers do not match the high temporal resolution observed in behavioral studies (2-7).We tested the limits of olfactory transduction speed and pulse tracking in five different insect species by measuring ORN population responses using electroantennogram (EAG) recordings. The amplitude and dynamics of EAG signals are proportional to the number of sensilla stimulated (20). They are also affected by receptor current amplitude, positions of the neurons relative to the recording electrode, and elec...

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Section: Discussionmentioning

confidence: 90%

mentioning

confidence: 98%

High-speed odor transduction and pulse tracking by insect olfactory receptor neurons

Szyszka

Gerkin

Galizia

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

115

101

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“…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.…”

Section: Resultsmentioning

confidence: 99%

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

Chapman¹,

Bradley²,

Haught³

et al. 2017

Proc. R. Soc. B.

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Nervous systems must adapt to shifts in behavioural ecology. One form of adaptation is neural exaptation, in which neural circuits are co-opted to perform additional novel functions. Here, we describe the co-option of a motor-to-somatosensory circuit into an olfactory network. Many moths beat their wings during odour-tracking, whether walking or flying, causing strong oscillations of airflow around the antennae, altering odour plume structure. This self-induced sensory stimulation could impose selective pressures that influence neural circuit evolution, specifically fostering the emergence of corollary discharge circuits. In Manduca sexta, a pair of mesothoracic to deutocerebral histaminergic neurons (MDHns), project from the mesothoracic neuromere to both antennal lobes (ALs), the first olfactory neuropil. Consistent with a hypothetical role in providing the olfactory system with a corollary discharge, we demonstrate that the MDHns innervate the ALs of advanced and basal moths, but not butterflies, which differ in wing beat and flight pattern. The MDHns probably arose in crustaceans and in many arthropods innervate mechanosensory areas, but not the olfactory system. The MDHns, therefore, represent an example of architectural exaptation, in which neurons that provide motor output information to mechanosensory regions have been co-opted to provide information to the olfactory system in moths.

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“…In Lepidoptera and other insects, the periodicity of the inflow of air due to flapping means that insects receive odor in pulses rather than in a continuous fashion (Sane and Jacobson, 2006;Horsmann et al, 1983). Recent work on olfactory sensitivity (Tripathy et al, 2010) showed that the hawk moth, M. sexta, can track odor pulses up to 30Hz with peak sensitivity at wing beat frequencies. During flapping, proper positioning of the antenna may help ensure that the antenna receives these pulses over the maximal length of its receptive surface.…”

Section: Role Of Antennal Positioning In Flightmentioning

confidence: 99%

The neural mechanisms of antennal positioning in flying moths

Krishnan

Prabhakar

Sudarsan

et al. 2012

Journal of Experimental Biology

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SUMMARYIn diverse insects, the forward positioning of the antenna is often among the first behavioral indicators of the onset of flight. This behavior may be important for the proper acquisition of the mechanosensory and olfactory inputs by the antennae during flight. Here, we describe the neural mechanisms of antennal positioning in hawk moths from behavioral, neuroanatomical and neurophysiological perspectives. The behavioral experiments indicated that a set of sensory bristles called Böhmʼs bristles (or hair plates) mediate antennal positioning during flight. When these sensory structures were ablated from the basal segments of their antennae, moths were unable to bring their antennae into flight position, causing frequent collisions with the flapping wing. Fluorescent dye-fills of the underlying sensory and motor neurons revealed that the axonal arbors of the mechanosensory bristle neurons spatially overlapped with the dendritic arbors of the antennal motor neurons. Moreover, the latency between the activation of antennal muscles following stimulation of sensory bristles was also very short (<10ms), indicating that the sensorimotor connections may be direct. Together, these data show that Böhmʼs bristles control antennal positioning in moths via a reflex mechanism. Because the sensory structures and motor organization are conserved across most Neoptera, the mechanisms underlying antennal positioning, as described here, are likely to be conserved in these diverse insects.Supplementary material available online at

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Odors pulsed at wing beat frequencies are tracked by primary olfactory networks and enhance odor detection

Cited by 62 publications

References 81 publications

High-speed odor transduction and pulse tracking by insect olfactory receptor neurons

High-speed odor transduction and pulse tracking by insect olfactory receptor neurons

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

The neural mechanisms of antennal positioning in flying moths

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