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

Abstract

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 network oscillations and how they control spike timing. To test these predictions, 16 channel electrode arrays were placed within the antennal lobe (AL) 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 to 30 Hz; 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 = 25–55 Hz; odor-driven = 55–85 Hz). 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 receptor 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.

Multichannel brain recordings in behavingDrosophilareveal oscillatory activity and local coherence in response to sensory stimulation and circuit activation

“…In the current study, we extend the scale-free hypothesis for oscillations to even smaller brains and ask whether endogenously generated and behaviorally relevant oscillations are also present in the fruit fly brain, which has only ϳ100,000 neurons (Shimada et al 2006). We demonstrate that oscillations in statistically distinct frequency bands appear to be generated endogenously and not only as a consequence of external stimuli (Christensen et al 2003;Daly et al 2011;Kirschfeld 1992;Laurent and Naraghi 1994;Tang and Juusola 2010;van Swinderen and Greenspan 2003).…”

“…LFP recordings represent summed synaptic activity across networks of neurons and often exhibit voltage oscillations in both mammals and invertebrates Daly et al 2011). To determine whether these oscillations correspond to specific functions, such as sensory processing, we examined how neural oscillations varied across brain structures while flies were exposed to sensory stimuli (visual, olfactory, or mechanosensory) and during transient activation of neural circuits in transgenic animals.…”

“…In the fruit fly, Drosophila melanogaster, visual salience has been linked to increased 20-to 30-Hz activity in the brain (van Swinderen and Greenspan 2003), and these oscillations appear to have behavioral relevance for stimulus selection and suppression (Tang and Juusola 2010;van Swinderen 2007). Several studies have demonstrated that endogenous oscillations in insects are induced during sensory stimulation (Christensen et al 2003;Daly et al 2011), suggesting that oscillations may be a result of transiently induced synchronous network activity in response to stimuli. Given that Drosophila flies display attentionlike behavior (Sareen et al 2011;Tang and Juusola 2010;van Swinderen and Greenspan 2003), endogenous oscillations in the insect brain may perform similar functional roles for neural processing as in vertebrates.…”

“…Although correlations between brain oscillations and behavior have been observed across nervous systems from mammals to invertebrates, the function of oscillatory activity in invertebrate brains has been debated (Christensen et al 2003;Daly et al 2011;Kirschfeld 1992;Laurent and Naraghi 1994;Martin et al 2011). In locusts, endogenous oscillations in olfactory neurons are involved in encoding odor cues (Cassenaer and Laurent 2012;Laurent and Naraghi 1994).…”

Regulation of specialists and generalists by neural variability improves pattern recognition performance

“…The main reasons to chose the olfactory system of insects are: the simplicity of the structural organization [3,4,5,6,7,8,9,10], the nature of the neural coding [11,12,13,14,15,16,17,2,18,19], the advent of the genetic manipulation techniques that isolate brain areas during the formation of memories [20,21,22,23], and the extensive odor conditioning experiments that shed light into the dynamics of learning during discrimination tasks [24,25,26,27,28,29]. Olfactory systems implement simple mechanisms to realize a quick and stable odorant discrimination [30], a goal we want to achieve through computer modeling.…”