Combinatorial odor discrimination in the brain: Attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli

Abstract

The rules governing the central discrimination of odors are complex and poorly understood, but a growing body of evidence supports the hypothesis that olfactory glomeruli may represent functionally distinct coding modules in the brain. Testing this hypothesis requires that both the functional characteristics and the spatial position of the glomerulus under study be uniquely identifiable. To address these questions, we examined a specialized array of glomeruli (the macroglomerular complex; MGC) in the antennal lobe of male moths that receives input from olfactory receptor cells tuned specifically to female-released odorants that either promote upwind flight (conspecific sex pheromones) or inhibit it (interspecific antagonists). By using a three-dimensional reconstruction method based on high-resolution laser-scanning confocal microscopy, we generated precise spatial maps of the MGC glomeruli in two related noctuid species with similar pheromone chemistry, Heliothis virescens and Helicoverpa zea. To determine the breadth of tuning of individual MGC glomeruli in processing information about these social signals, we used intracellular recording and staining methods to examine the responses of projection (output) neurons that innervate MGC glomeruli and that each project an axon to higher integrative centers. In both species, a close correspondence was found between the odor specificity of the projection neurons and the glomerulus (or glomeruli) supplied by them. The binary blend of pheromone components for each species was represented by neural activity in only two distinct glomeruli in both H. virescens and H. zea. Odorants that antagonize upwind flight when they are added to the respective pheromonal blends evoked excitatory activity in output neurons restricted to a third glomerulus in the MGCs of both species. In summary, these results suggest that the selective activation of different combinations of functionally distinct MGC glomeruli is a general means for discriminating these specific attractant and antagonist chemical signals in the brain.

Representation of pheromones, interspecific signals, and plant odors in higher olfactory centers; mapping physiologically identified antennal-lobe projection neurons in the male heliothine moth

“…The fact that the information about the two principal pheromone components are kept mainly separated along the mALT via two physiologically distinct neuron categories, as shown here and in several previous studies on heliothine moths (Vickers et al, 1998; Vickers and Christensen, 2003; Zhao and Berg, 2010), justifies a short comment. The purpose of keeping the general pheromone information segregated from the inter-specific signal information at this level seems obvious, based on the opposite behavioral responses induced by the different signals.…”

“…In addition, competitive blocking on the receptors has been ruled out by adding the “inhibiting” compounds to the pheromones. Furthermore, a separation of the pheromone and the interspecific signal information has been well documented in several species, including the two heliothine species investigated here, both as concerns input to and output from the MGC (Christensen et al, 1995; Hansson et al, 1995; Berg et al, 1998, 2005; Vickers et al, 1998; Zhao and Berg, 2010). Thus, the next relevant question was whether the separation is kept in the lateral horn.…”

“…Heliothine moths are suitable for studying central neuronal mechanisms underlying not only information about multicomponent pheromone blends but also of interspecific signals inhibiting the pheromone attraction (Christensen et al, 1991, 1995; Mustaparta, 1996; Berg et al, 1998, 2005; Vickers et al, 1998; Vickers and Christensen, 2003; Zhao and Berg, 2010). In general, the specificity of pheromone sensory neurons as distinct neuron types conveying information about one component to specific MGC-units of the AL applies to all species studied.…”

“…In general, the specificity of pheromone sensory neurons as distinct neuron types conveying information about one component to specific MGC-units of the AL applies to all species studied. Regarding the out-put information from the male-specific glomeruli, most projections neurons identified are reported to maintain, to a certain extent, the specificity of the sensory neurons by responding best to the “key” compound whereas a smaller proportion integrates information about both components (Vickers et al, 1998; Vickers and Christensen, 2003; Zhao and Berg, 2010). As the present study includes MGC-neurons of the first mentioned category only, it was relevant to ask how particular pheromone components are mapped in the lateral horn.…”

“…By tracing functionally characterized receptor neurons and antennal-lobe projection neurons, a general chemotopic organization of the male-specific MGC has been demonstrated in a number of geographically isolated and sympatric heliothine species including the American tobacco budworm moth, Heliothis virescens (Christensen et al, 1995; Hansson et al, 1995; Berg et al, 1998; Vickers et al, 1998; Vickers and Christensen, 2003), Heliothis subflexa (Baker et al, 2004), Helicoverpa zea (Christensen et al, 1991; Cossé et al, 1998; Vickers et al, 1998; Lee et al, 2006), and Helicoverpa assulta (Berg et al, 2005; Zhao and Berg, 2010). Especially intriguing, is the use of chemical signals in communication both within and across the species in this group.…”