Central Projection of Antennal Sensory Neurons in the Central Nervous System of the Mirid Bug Apolygus lucorum (Meyer-Dür)

Abstract

The mirid bug Apolygus lucorum (Meyer-Dür), a polyphagous pest, is dependent on olfactory cues to locate various host plant species and mates. In this study, we traced the projection pathway of the antennal sensory neurons and visualized their projection patterns in the central nervous system of A. lucorum through confocal microscopy and digital reconstructions. We also examined the glomerular organization of the primary olfactory center of the brain, the antennal lobe, and created a three-dimensional model of the glomeruli. We found that the axons of the sensory neurons project into the brain via the ipsilateral antennal nerve, and descend further into the gnathal ganglion, prothoracic ganglion, mesothoracic ganglion, and metathoracic ganglion, and reach as far as to the abdominal ganglion. Such a projection pattern indicates that antennal sensory neurons of A. lucorum may be potentially directly connected to motor neurons. The antennal lobe, however, is the major target area of antennal sensory neurons. The antennal lobe is composed of a large number of glomeruli, i.e. 70–80 glomeruli in one AL of A. lucorum. The results of this study which provide information about the basic anatomical arrangement of the brain olfactory center of A. lucorum, are important for further investigations of chemosensory encoding mechanisms of the mirid bug.

Central Projections of Antennal and Labial Palp Sensory Neurons in the Migratory Armyworm Mythimna separata

“…The general staining pattern of all antennal afferents covered innervations in several ipsilateral regions of the central nervous system including the AL, protocerebrum, AMMC, gnathal ganglion, proTG, and mesoTG. Such a widespread projection pattern of the antennal axons was also observed in the locust, Locusta migratoria , blowfly, Calliphora erythrocephala , blood-sucking bug, Rhodnius prolixus , and mirid bug, Apolygus lucorum ( Bräunig et al, 1983 ; Nässel et al, 1984 ; Barrozo et al, 2009 ; Xie et al, 2016 ). The multiple targeting areas may correspond to the different sensory modalities being detected by the antennal sensory neurons.…”

“…In addition, specific staining of selected s. trichoidea showed labeling in AL glomeruli only, indicating that sensory neurons housed inside this numerous population of antennal sensilla terminate in the AL glomeruli exclusively. Such a projection pattern of olfactory sensory neurons has been found in many other insect species within a wide range of orders, for instance, dragonfly Libellula depressa ( Rebora et al, 2013 ), cricket Gryllus bimaculatus ( Yoritsune and Aonuma, 2012 ), cockroach Periplaneta americana ( Nishino et al, 2005 ), louse Columbicola columbae ( Crespo and Vickers, 2012 ), bugs Euschistus heros , R. prolixus , and Apolygus lucorum ( Kristoffersen et al, 2008 ; Barrozo et al, 2009 ; Xie et al, 2016 ), aphid Sitobion avenae , Metopolophium dirhodum , and Acyrthosiphon pisum ( Kristoffersen et al, 2008 ; Kollmann et al, 2011 ), psyllid Trioza apicalis ( Kristoffersen et al, 2008 ), beetle Tribolium castaneum ( Dippel et al, 2016 ), A. mellifera ( Nishino et al, 2009 ), moth Helicoverpa armigera ( Zhao et al, 2016 ), D. melanogaster ( Stocker et al, 1983 ), Aedes aegypti , and Anopheles gambiae ( Distler and Boeckh, 1997 ; Anton et al, 2003 ; Ignell et al, 2005 ).…”

“…As its name suggests, the AMMC is the center for input from antennal mechanosensory neurons and for controlling movement of the antenna. Similarly to the general arrangement in the AL, the projection pattern of antennal sensory neurons in the AMMC is to a large extent conserved across a wide range of insects ( Ignell et al, 2005 ; Nishino et al, 2005 ; Kamikouchi et al, 2006 ; Kristoffersen et al, 2008 ; Barrozo et al, 2009 ; Nishino et al, 2009 ; Kollmann et al, 2011 ; Crespo and Vickers, 2012 ; Yoritsune and Aonuma, 2012 ; Rebora et al, 2013 ; Xie et al, 2016 ; Zhao et al, 2016 ).…”

“…aegypti , and An. gambiae ( Nässel et al, 1984 ; Ignell et al, 2005 ; Kamikouchi et al, 2006 ; Ai et al, 2007 ; Nishino et al, 2009 ; Rebora et al, 2013 ; Xie et al, 2016 ). However, these are mechanosensory neurons originating from the pedicel: in C. erythrocephala from the campaniform sensilla and in D. menlanogaster and A. mellifera from the Johnston’s organ ( Nässel et al, 1984 ; Kamikouchi et al, 2006 ; Ai et al, 2007 ).…”

“…Axons of LPO sensory neurons project via the labial nerve to three main regions of the central nervous system: (1) to the LPO glomerulus (LPOG) in each antennal lobe, the primary olfactory center in the insect brain, (2) to the gnathal ganglion, and (3) to the ventral nerve cord ( Bogner et al, 1986 ; Kent et al, 1986 ; Zhao et al, 2013 ). The antennal axons, on the other hand, target (1) all glomeruli of the ipsilateral antennal lobe except for the LPOG, (2) the antennal mechanosensory and motor center (AMMC), (3) the gnathal ganglion, and (4) the ventral nerve cord ( Xie et al, 2016 ). Whereas the LPO houses sensory neurons tuned to one odor cue only, i.e., CO 2 , the antennal neurons are tuned not only to a large amount of odor stimuli but to several sensory modalities including taste, mechano-sensation, humidity, and temperature as well ( Schneider, 1964 ; Altner and Loftus, 1985 ; Nishikawa et al, 1995 ; Jørgensen et al, 2006 ; Guerenstein and Hildebrand, 2008 ; Popescu et al, 2013 ; Enjin et al, 2016 ; Frank et al, 2017 ).…”