Time-varying phase relationship between spiking neuronal responses and local field potentials in olfactory processing in manduca sexta

The Transient Oscillatory Model (TOM) seeks to explain neural coding in the first processing center of the invertebrate olfactory system - the antennal lobe - by proposing that activated primary output neurons participate in the encoding ensemble only transiently, based on the coincidence of their spiking relative to local field potential (LFP) oscillation phase. Using the sphinx moth, Manduca sexta, as a model system, we tested the predictions of the TOM with regard to the trial-to-trial consistency of odor driven oscillations, the phase-locking of action potentials to LFP oscillations, and the role of GABAA receptors in the generation of these oscillations. We quantified the changes in LFP oscillation frequency over time via time-frequency representation (TFR) analysis, and calculated the timing of action potentials relative to the phase of the LFP oscillations (vector-strength analysis). In accordance to the TOM\u27s predictions for the role of LFP oscillations, TFRs revealed that odor-driven oscillations modulate in a stimulus specific manner. However, contrasting with these same predictions, vector-strength analyses illustrated that phase locking was higher during spontaneous activity than during odor response. Finally, in disagreement with TOM predictions, disruption of GABA A receptors by BMI application reduced odor-driven LFP oscillations across time-periods and regions of the AL. Further BMI application reduced phase-locking of action potentials to the LFP, while leaving phase-locking highest during spontaneous activity. Consequently, we find the overall architecture of the TOM to be incompatible with these findings

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