Divergent and convergent projections to the two parallel olfactory centers from two neighboring, pheromone‐receptive glomeruli in the male American cockroach

Abstract

Many animals utilize sex pheromone for detecting conspecific mates. Sex pheromone is usually a blend of two or more components with similar chemical compositions. The pheromone receivers are equipped with localized olfactory glomeruli in the first-order olfactory center for specifically processing these pheromone components. In the American cockroach, Periplaneta americana, either periplanone A or periplanone B emitted by virgin females evokes identical sexual behaviors in males. The antennal lobes of adult male cockroaches have enlarged, neighboring A- and B-glomeruli, which preferentially process periplanones A and B, respectively. By using intracellular recording and staining of neurons in the same preparations, we provide the first detailed projection maps of output neurons (projection neurons; PNs) from the A-glomerulus and the B-glomerulus. Although both PNs project to the mushroom body calyces and the lateral horn, their proximities in the two centers largely differ: in the calyces, the axon terminals of the A-PN were located more predominantly in the periphery compared with those of the B-PN, whereas axon terminals of both PNs were highly congruent in the anteromedial region of the lateral horn. These results suggest that pheromone component signals are dispersed in the mushroom body for specific odor discrimination but are integrated in the lateral horn for generating behaviors common to the pheromone components. Stimulation of the ipsilateral antenna with various odors showed that the odor specificity of A-PN is higher than that of B-PN. The different developmental lineages of A- and B-PNs suggested by these results are discussed.

Interactive parallel sex pheromone circuits that promote and suppress courtship behaviors in the cockroach

“…S5 ). A-PNs selectively respond to PA but not PB ( 23 , 24 , 38 ), which is consistent with the responsivity of PA-SNs. These findings, combined with the results of previous studies, clarify the inhibitory interaction from the PA-processing pathway to the PB-processing pathway in the AL (Fig.…”

Interactive parallel sex pheromone circuits that promote and suppress courtship behaviors in the cockroach

“…S5 ). A-PNs selectively respond to PA but not PB ( 23 , 24 , 38 ), which is consistent with the responsivity of PA-SNs. These findings, combined with the results of previous studies, clarify the inhibitory interaction from the PA-processing pathway to the PB-processing pathway in the AL (Fig.…”

Spatial Receptive Fields for Odor Localization

“…This is also reasonable, given that navigation toward an odor source requires multimodal sensory integration, including proprioceptive information on antennal position and olfactory information acquired in different spatial and temporal points through serial odor sampling. On the contrary, we report that axons terminals of different S-PNs were largely intermingled in the anteromedial region of the LH, i.e., the sexual-pheromone-specific area, where PNs that process both major (periplanone-B) and minor (periplanone-A) components of the female sex pheromone converge [18]. Interestingly, although spatial information appears to be lost, we observed that the volume of S-PNs' axon terminals in the LH was proportional to the volume of the dendritic arborization in the MG and that proximal receptive field S-PNs may provide more synaptic input onto this region than distal receptive field neurons.…”

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

“…Type2 and type1 PNs had dendrites in the antero-dorsal and postero-ventral group glomeruli, respectively ( Figures 1E,F ). Among the 106 glomeruli analyzed, only 10 postero-ventral group glomeruli were connected with the ALT-2 or ALT-3 PNs previously identified (Malun et al, 1993), and two macroglomeruli were connected with sex pheromone-sensitive PNs that terminated in specific regions of higher brain centers (Nishino et al, 2011, 2012a). Here, we focused on the two major streams formed by type1 and type2 PNs.…”

“…In the cockroach, axons of uniglomerular PNs run through the m-ALT and nearby tracts (ALT-2 and ALT-3), and terminate in the medial and lateral calyces (CA) of the MB first and then in the LH (Malun et al, 1993; Strausfeld and Li, 1999a; Nishino et al, 2012a). Retrograde staining of PNs revealed all glomeruli were innervated by PNs running m-ALT and nearby tracts in the cockroach ( Figures 1A,B ).…”

Interactive parallel sex pheromone circuits that promote and suppress courtship behaviors in the cockroach

“…S5 ). A-PNs selectively respond to PA but not PB ( 23 , 24 , 38 ), which is consistent with the responsivity of PA-SNs. These findings, combined with the results of previous studies, clarify the inhibitory interaction from the PA-processing pathway to the PB-processing pathway in the AL (Fig.…”

Spatial Receptive Fields for Odor Localization

“…This is also reasonable, given that navigation toward an odor source requires multimodal sensory integration, including proprioceptive information on antennal position and olfactory information acquired in different spatial and temporal points through serial odor sampling. On the contrary, we report that axons terminals of different S-PNs were largely intermingled in the anteromedial region of the LH, i.e., the sexual-pheromone-specific area, where PNs that process both major (periplanone-B) and minor (periplanone-A) components of the female sex pheromone converge [18]. Interestingly, although spatial information appears to be lost, we observed that the volume of S-PNs' axon terminals in the LH was proportional to the volume of the dendritic arborization in the MG and that proximal receptive field S-PNs may provide more synaptic input onto this region than distal receptive field neurons.…”

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

“…Type2 and type1 PNs had dendrites in the antero-dorsal and postero-ventral group glomeruli, respectively ( Figures 1E,F ). Among the 106 glomeruli analyzed, only 10 postero-ventral group glomeruli were connected with the ALT-2 or ALT-3 PNs previously identified (Malun et al, 1993), and two macroglomeruli were connected with sex pheromone-sensitive PNs that terminated in specific regions of higher brain centers (Nishino et al, 2011, 2012a). Here, we focused on the two major streams formed by type1 and type2 PNs.…”

“…In the cockroach, axons of uniglomerular PNs run through the m-ALT and nearby tracts (ALT-2 and ALT-3), and terminate in the medial and lateral calyces (CA) of the MB first and then in the LH (Malun et al, 1993; Strausfeld and Li, 1999a; Nishino et al, 2012a). Retrograde staining of PNs revealed all glomeruli were innervated by PNs running m-ALT and nearby tracts in the cockroach ( Figures 1A,B ).…”

Interactive parallel sex pheromone circuits that promote and suppress courtship behaviors in the cockroach

“…S5 ). A-PNs selectively respond to PA but not PB ( 23 , 24 , 38 ), which is consistent with the responsivity of PA-SNs. These findings, combined with the results of previous studies, clarify the inhibitory interaction from the PA-processing pathway to the PB-processing pathway in the AL (Fig.…”

Spatial Receptive Fields for Odor Localization

“…This is also reasonable, given that navigation toward an odor source requires multimodal sensory integration, including proprioceptive information on antennal position and olfactory information acquired in different spatial and temporal points through serial odor sampling. On the contrary, we report that axons terminals of different S-PNs were largely intermingled in the anteromedial region of the LH, i.e., the sexual-pheromone-specific area, where PNs that process both major (periplanone-B) and minor (periplanone-A) components of the female sex pheromone converge [18]. Interestingly, although spatial information appears to be lost, we observed that the volume of S-PNs' axon terminals in the LH was proportional to the volume of the dendritic arborization in the MG and that proximal receptive field S-PNs may provide more synaptic input onto this region than distal receptive field neurons.…”

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

“…Type2 and type1 PNs had dendrites in the antero-dorsal and postero-ventral group glomeruli, respectively ( Figures 1E,F ). Among the 106 glomeruli analyzed, only 10 postero-ventral group glomeruli were connected with the ALT-2 or ALT-3 PNs previously identified (Malun et al, 1993), and two macroglomeruli were connected with sex pheromone-sensitive PNs that terminated in specific regions of higher brain centers (Nishino et al, 2011, 2012a). Here, we focused on the two major streams formed by type1 and type2 PNs.…”

“…In the cockroach, axons of uniglomerular PNs run through the m-ALT and nearby tracts (ALT-2 and ALT-3), and terminate in the medial and lateral calyces (CA) of the MB first and then in the LH (Malun et al, 1993; Strausfeld and Li, 1999a; Nishino et al, 2012a). Retrograde staining of PNs revealed all glomeruli were innervated by PNs running m-ALT and nearby tracts in the cockroach ( Figures 1A,B ).…”