Odors Pulsed at Wing Beat Frequencies are Tracked by Primary Olfactory Networks and Enhance Odor Detection

Each down stroke of an insect's wings accelerates axial airflow over the antennae. Modeling studies suggest that this can greatly enhance penetration of air and air-born odorants through the antennal sensilla thereby periodically increasing odorant-receptor interactions. Do these periodic changes result in entrainment of neural responses in the antenna and antennal lobe (AL)? Does this entrainment affect olfactory acuity? To address these questions, we monitored antennal and AL responses in the moth Manduca sexta while odorants were pulsed at frequencies from 10–72 Hz, encompassing the natural wingbeat frequency. Power spectral density (PSD) analysis was used to identify entrainment of neural activity. Statistical analysis of PSDs indicates that the antennal nerve tracked pulsed odor up to 30 Hz. Furthermore, at least 50% of AL local field potentials (LFPs) and between 7–25% of unitary spiking responses also tracked pulsed odor up to 30 Hz in a frequency-locked manner. Application of bicuculline (200 μM) abolished pulse tracking in both LFP and unitary responses suggesting that GABAA receptor activation is necessary for pulse tracking within the AL. Finally, psychophysical measures of odor detection establish that detection thresholds are lowered when odor is pulsed at 20 Hz. These results suggest that AL networks can respond to the oscillatory dynamics of stimuli such as those imposed by the wing beat in a manner analogous to mammalian sniffing

Space Takes Time: Concentration Dependent Output Codes from Primary Olfactory Networks Rapidly Provide Additional Information at Defined Discrimination Thresholds

As odor concentration increases, primary olfactory network representations expand in spatial distribution, temporal complexity and duration. However, the direct relationship between concentration dependent odor representations and the psychophysical thresholds of detection and discrimination is poorly understood. This relationship is absolutely critical as thresholds signify transition points whereby representations become meaningful to the organism. Here, we matched stimulus protocols for psychophysical assays and intracellular recordings of antennal lobe (AL) projection neurons (PNs) in the moth Manduca sexta to directly compare psychophysical thresholds and the output representations they elicit. We first behaviorally identified odor detection and discrimination thresholds across an odor dilution series for a panel of structurally similar odors. We then characterized spatiotemporal spiking patterns across a population of individually filled and identified AL PNs in response to those odors at concentrations below, at, and above identified thresholds. Using spatial and spatiotemporal based analyses we observed that each stimulus produced unique representations, even at sub-threshold concentrations. Mean response latency did not decrease and the percent glomerular activation did not increase with concentration until undiluted odor. Furthermore, correlations between spatial patterns for odor decreased, but only significantly with undiluted odor. Using time-integrated Euclidean distance (ED) measures, we determined that added spatiotemporal information was present at the discrimination but not detection threshold. This added information was evidenced by an increase in integrated distance between the sub-detection and discrimination threshold concentrations (of the same odor) that was not present in comparison of the sub-detection and detection threshold. After consideration of delays for information to reach the AL we find that it takes ∼120–140 ms for the AL to output identity information. Overall, these results demonstrate that as odor concentration increases, added information about odor identity is embedded in the spatiotemporal representation at the discrimination threshold

Sensory responses of descending brain neurons in the walking cricket Gryllus bimaculatus

Sensory responses of various descending brain neurons, their modulation during standing or walking, and the correlation of such modulations with stimulus category were investigated. Stimuli involving (1) static or moving grating, artificial calling songs with (2) the conspecific and (3) an ultrasound frequency, or (4) air puffs to the cerci were presented to crickets walking in an open loop paradigm. The morphology of different descending interneurons in the brain and thoracic ganglia is described, together with their respective response properties. Some cells were excited, others inhibited by, and only some were directionally sensitive to the optomotor stimulus. Responses to artificial calling songs with conspecific and ultrasound frequency differed in the way the syllables of the sounds were coded and in the representation of ipsi- and contralateral stimuli. The majority of cells tested responded to air puffs. Stimulus representation differed among individuals of morphological types, but was very similar among individual interneurons of the morphologically homogenous i5 group. Stimuli approximating predators (air puffs, ultrasound) were usually represented during walking and standing; however, most neurons only responded to the other stimuli only during walking. These results indicate that the same neurons show different responses, and may have different functions, under different behavioral conditions.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/42181/1/359-187-1-1_s003590000171.pd

Detailed characterization of local field potential oscillations and their relationship to spike timing in the antennal lobe of the moth Manduca sexta.

The transient oscillatory model of odor identity encoding seeks to explain how odorants with spatially overlapped patterns of input into primary olfactory networks can be discriminated. This model provides several testable predictions about the distributed nature of subthreshold oscillations and how they control spike timing. To test these predictions, 16 channel electrode arrays were placed within the antennal lobe of the moth Manduca sexta. Unitary spiking and multi site local field potential (LFP) recordings were made during spontaneous activity and in response to repeated presentations of an odor panel. We quantified oscillatory frequency, cross correlations between LFP recording sites, and spike-LFP phase relationships. We show that odor-driven AL oscillations in Manduca are frequency modulating (FM) from ~100–30Hz; this was odorant and stimulus duration dependent. FM oscillatory responses were localized to one or two recording sites suggesting a localized (perhaps glomerular) not distributed source. LFP cross correlations further demonstrated that only a small (r<0.05) distributed and oscillatory component was present. Cross spectral density analysis demonstrated the frequency of these weakly distributed oscillations was state dependent (spontaneous activity= 25-55Hz; odor-driven= 55-85Hz). Surprisingly, vector strength analysis indicated that unitary phase locking of spikes to the LFP was strongest during spontaneous activity and dropped significantly during responses. Application of bicuculline, a GABAA antagonist, significantly lowered the frequency content of odor-driven distributed oscillatory activity. Bicuculline significantly reduced spike phase locking generally, but the ubiquitous pattern of increased phase locking during spontaneous activity persisted. Collectively, these results indicate that oscillations perform poorly as a stimulus-mediated spike synchronizing mechanism for Manduca and hence are incongruent with the transient oscillatory model