Abstract
The locust olfactory system interfaces with the external world through antennal receptor neurons (ORNs), which represent odors in a distributed, combinatorial manner. ORN axons bundle together to form the antennal nerve, which relays sensory information centrally to the antennal lobe (AL). Within the AL, an odor generates a dynamically evolving ensemble of active cells, leading to a stimulus-specific temporal progression of neuronal spiking. This experimental observation has led to the hypothesis that an odor is encoded within the AL by a dynamically evolving trajectory of projection neuron (PN) activity that can be decoded piecewise to ascertain odor identity. In order to study information coding within the locust AL, we developed a scaled-down model of the locust AL using Hodgkin–Huxley-type neurons and biologically realistic connectivity parameters and current components. Using our model, we examined correlations in the precise timing of spikes across multiple neurons, and our results suggest an alternative to the dynamic trajectory hypothesis. We propose that the dynamical interplay of fast and slow inhibition within the locust AL induces temporally stable correlations in the spiking activity of an odor-dependent neural subset, giving rise to a temporal binding code that allows rapid stimulus detection by downstream elements.
Highlights
The locust antennal lobe (AL) can be deconstructed within the framework of stimulus encoding, providing an excellent system in which to study early sensory processing
In a previous paper (Patel et al, 2009), we showed that our model exhibits (a) GABA-dependent 20 Hz local field potential (LFP) oscillations that decay over the first second of stimulation, (b) slow temporal patterning of projection neuron (PN) responses generated by the slow inhibitory current from local neurons (LNs) to PNs, and (c) preservation of slow patterning after removal of fast GABA synapses to abolish the network oscillation
We begin by showing that when network activity is examined over a long time window (1 s), correlated PN firing occurs only when two conditions are satisfied: (1) fast GABAergic inhibition is present within the network; (2) slow inhibition is absent from the network
Summary
The locust antennal lobe (AL) can be deconstructed within the framework of stimulus encoding, providing an excellent system in which to study early sensory processing. Application of picrotoxin to the AL to block fast GABAA receptors abolishes the global 20 Hz oscillation but preserves slow patterning (MacLeod and Laurent, 1996; MacLeod et al, 1998), eliminating synchrony while leaving firing rates undisturbed. These features imply that the AL odor response consists of synchronized bursts of PN spikes occurring in 50 ms time steps, with the precise subset of PNs that contribute spikes to each burst evolving gradually from one oscillation cycle to the in an odor-specific manner (Wehr and Laurent, 1996)
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