Coordination of central odor representations through transient, non-oscillatory synchronization of glomerular output neurons

Abstract

At the first stage of processing in the olfactory pathway, the patterns of glomerular activity evoked by different scents are both temporally and spatially dynamic. In the antennal lobe (AL) of some insects, coherent firing of AL projection neurons (PNs) can be phase-locked to network oscillations, and it has been proposed that oscillatory synchronization of PN activity may encode the chemical identity of the olfactory stimulus. It remains unclear, however, how the brain uses this time-constrained mechanism to encode chemical identity when the stimulus itself is unpredictably dynamic. In the olfactory pathway of the moth Manduca sexta, we find that different odorants evoke gamma-band oscillations in the AL and the mushroom body (a higher-order network that receives input from the AL), but oscillations within or between these two processing stages are not temporally coherent. Moreover, the timing of action potential firing in PNs is not phase-locked to oscillations in either the AL or mushroom body, and the correlation between PN synchrony and field oscillations remains low before, during, and after olfactory stimulation. These results demonstrate that olfactory circuits in the moth are specialized to preserve time-varying signals in the insect's olfactory space, and that stimulus dynamics rather than intrinsic oscillations modulate the uniquely coordinated pattern of PN synchronization evoked by each olfactory stimulus. We propose that non-oscillatory synchronization provides an adaptive mechanism by which PN ensembles can encode stimulus identity while concurrently monitoring the unpredictable dynamics in the olfactory signal that typically occur under natural stimulus conditions. I n the olfactory systems of widely divergent species, the patterns of odor-evoked neural activity that spread across the olfactory glomeruli at the first stage of processing are both spatially and temporally complex (1-7). The distributed and dynamic nature of these central responses has also complicated efforts to decipher the rules underlying olfactory stimulus identification and discrimination in the brain. In the antennal lobe (AL) of insects, the equivalent of the olfactory bulb in vertebrates, increasing evidence suggests that specific patterns of synchronous firing across a distributed array of AL projection neurons (PNs) may encode different features of an olfactory stimulus (8-12). For example, some studies suggest that global network oscillations can be used as a periodic time reference to help coordinate and update (with each oscillation cycle) the specific PN ensemble that encodes the chemical identity of the olfactory stimulus (3,8). It remains unresolved, however, whether a temporally structured mechanism like oscillatory synchronization can reliably encode information about the chemical identity of a stimulus that is itself temporally unpredictable. We used the sphinx moth Manduca sexta, an animal that possesses anatomically discrete and identifiable glomeruli and shows robust behavioral responses to different olfactor...

Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe

“…Likewise, none of the pairs with low response similarity displayed significant coactivity. This result agrees with an increasing number of studies showing that specific temporal relationships among functionally defined neurons may be used by the brain to recognize and discriminate different features of an olfactory stimulus, although the mechanisms underlying these temporal relationships may vary in different olfactory systems (Christensen et al, , 2003Laurent et al, 2001;Lei et al, 2002;Sachse and Galizia, 2002). Manduca PNs, unlike those in locusts (Laurent et al, 2001), exhibit transient synchronization in response to olfactory stimulation, not involving fast oscillations (Christensen et al, 2003;Daly et al, 2004a,b).…”

“…In an extension of previous models (Gelperin and Tank, 1990;Freeman, 1992), a proposed temporal coding mechanism could explain how molecularly similar odorants are discriminated in the insect AL (Stopfer et al, 1997;Laurent et al, 2001), but the well defined spatial aspects of the olfactory code are minimally represented in this model (Wehr and Laurent, 1996;Theunissen, 2003). Other studies in both vertebrates and invertebrates support an alternative model in which both the spatial and temporal aspects of the olfactory signals are inseparable components of the code (Spors and Grinvald, 2002;Christensen et al, 2003). To evaluate these hypotheses in greater detail, it is necessary to use a method that allows high-resolution monitoring of odor-evoked activity in both space and time.…”

“…Some studies have shown that mitral/tufted (M/T) cells or projection neurons (PNs) innervating the same glomerulus are more likely to show correlated firing in response to a stimulus (Buonviso and Chaput, 1990;Carlson et al, 2000;Lei et al, 2002;Christensen et al, 2003;Schoppa and Urban, 2003). Other studies have found, however, that the M/T cells innervating different glomeruli in the same region of the OB can also show strong correlations (Kashiwadani et al, 1999).…”

ϒ Spike-Field Coherence in a Population of Olfactory Bulb Neurons Differentiates between Odors Irrespective of Associated Outcome

“…However, in contrast with studies in zebrafish (Blumhagen et al, 2011) and invertebrates (Stopfer et al, 1997;Laurent, 2002;Christensen et al, 2003), experiments in awake mammals indicate that overall changes in M/T cell firing do not necessarily carry information on odor identity. Indeed, the odor-induced changes in firing rate are, in some awake rodent studies, sparse or absent (Rinberg et al, 2006;Davison and Katz, 2007;Gschwend et al, 2012;Blauvelt et al, 2013;Wachowiak et al, 2013), but in other studies there are odor-induced increases or decreases in the overall firing rate of 10 -80% of the M/T cells (Doucette and Restrepo, 2008;Fuentes et al, 2008;Doucette et al, 2011; see also Cury and Uchida, 2010; Shusterman et al, 2011).…”

“…Importantly in the insect olfactory system, when an odor is presented, it induces transient ϒ frequency oscillation in the neural population of the antennal lobe (equivalent to the mammalian OB), and silencing ϒ oscillation interferes with discrimination of closely related odorants (Stopfer et al, 1997;Laurent, 2002;Perez-Orive et al, 2002;Christensen et al, 2003). In mammals, ϒ LFP responses in the OB are thought to carry information on odor identity (Nusser et al, 2001;Beshel et al, 2007;Lepousez and Lledo, 2013;Kay, 2014).…”