Representation of Thermal Information in the Antennal Lobe of Leaf-Cutting Ants

Abstract

Insects are equipped with various types of antennal sensilla, which house thermosensitive neurons adapted to receive different parameters of the thermal environment for a variety of temperature-guided behaviors. In the leaf-cutting ant Atta vollenweideri, the physiology and the morphology of the thermosensitive sensillum coeloconicum (Sc) has been thoroughly investigated. However, the central projections of its receptor neurons are unknown. Here we selectively stained the three neurons found in single Sc and tracked their axons into the brain of Atta vollenweideri workers. Each of the three axons terminates in a single glomerulus of the antennal lobe (Sc-glomeruli). Two of the innervated glomeruli are adjacent to each other and are located laterally, while the third one is clearly separated and located medially in the antennal lobe. Using two-photon Ca2+ imaging of antennal lobe projection neurons, we studied where in the antennal lobe thermal information is represented. In the 11 investigated antennal lobes, we found up to 10 different glomeruli in a single specimen responding to temperature stimulation. Both, warm- and cold-sensitive glomeruli could be identified. The thermosensitive glomeruli were mainly located in the medial part of the antennal lobe. Based on the general representation of thermal information in the antennal lobe and functional data on the Sc-glomeruli we conclude that temperature stimuli received by Sc are processed in the medial of the three target glomeruli. The present study reveals an important role of the antennal lobe in temperature processing and links a specific thermosensitive neuron to its central target glomerulus.

Clearing pigmented insect cuticle to investigate small insects' organs in situ using confocal laser-scanning microscopy (CLSM)

“…for anterograde labeling of receptor neurons as well as 5HT ir neurons. Anterograde labeling of receptor neurons using a fluorescent tracer allows visualization of, e.g., axonal arbors and varicosities at a resolution comparable with results obtained from dissected brains (Kelber et al, 2006;Ruchty et al, 2010). In our immunocytochemical approach, we compared 5HT ir neurons of our specimens (F. cunicularia) with 5HT ir neurons described in other ant species, and we found similar numbers of neurons at corresponding locations in the protocerebrum (Hoyer et al, 2005;Tsuji et al, 2007).…”

Two cold-sensitive neurons within one sensillum code for different parameters of the thermal environment in the ant Camponotus rufipes

“…Cold-sensitive neurons that respond to temperature changes with a phasic-tonic response dynamic were found in various insect species (Lacher, 1964 ; Loftus, 1968 ; Waldow, 1970 ; Tichy, 1979 ; Nishikawa et al, 1992 ; Merivee et al, 2003 ; Must et al, 2006a , b ; Ruchty et al, 2009 , 2010a , b ). The phasic response of cold-sensitive neurons relates to a change in temperature (temperature changing rate), however, the resolving power of the different systems was rarely quantified (Loftus and Corbière-Tichané, 1981 ; Ameismeier and Loftus, 1988 ; Zopf et al, 2014 ).…”

“…A variety of thermo-sensitive neurons are described for the S. coeloconicum and S. ampullaceum in insects, either combined with chemo-sensitive neurons (Lacher, 1964 ; Altner, 1977 ; Davis, 1977 ; Altner et al, 1981 ; Kleineidam and Tautz, 1996 ) or forming a sensory triad with two hygro-sensitive neurons (Waldow, 1970 ; Tichy, 1979 ; Altner et al, 1981 ; Yokohari et al, 1982 ; Altner and Loftus, 1985 ; Piersanti et al, 2011 ). In ants, thermo-sensitive neurons are known to be associated with the S. coeloconicum and S. ampullaceum (Kleineidam and Tautz, 1996 ), and one phasic-tonic cold-sensitive neuron associated with the S. coeloconicum was described in great detail (Ruchty et al, 2009 , 2010a , b ). This cold-sensitive neuron is highly sensitive for transient temperatures and adapts to steady state temperature.…”

Higher brain centers for social tasks in worker ants, Camponotus japonicus

“…Central projections of sensory neurons from particular antennal sensilla suggest putative functions for these glomeruli. The T1-T5 glomeruli receive sensory inputs from olfactory sensilla, probably including sensory neurons for general odors, sex pheromones, alarm pheromones, and trail pheromones (Galizia et al, 1999;Dupuy et al, 2010;Kelber et al, 2010;Kuebler et al, 2010), whereas the T7 glomeruli receive inputs from ampullaceal, coelocapitular, and coeloconic sensilla, probably including sensory neurons for CO 2 , humidity, and temperature (Kleineidam et al, 2000;Nakanishi et al, 2009Nakanishi et al, , 2010Ruchty et al, 2009Ruchty et al, , 2010a. The T1-T5 and T7 glomeruli are common to both sexes and all castes, about 350 glomeruli in females and about 250 glomeruli in males of the carpenter ant (Nishikawa et al, 2008;Nakanishi et al, 2009Nakanishi et al, , 2010.…”

“…In ants, electrophysiological recordings of sensilla, central projections of sensory neurons, or optical recordings of the antennal lobe suggest putative functions of sensilla on the antennae and glomeruli in the antennal lobe (Dumpert, 1972;Galizia et al, 1999;Yokohari, 1999;Kleineidam et al, 2000;Ozaki et al, 2005;Nakanishi et al, 2009Nakanishi et al, , 2010Ruchty et al, 2009Ruchty et al, , 2010aDupuy et al, 2010;Kelber et al, 2010). Among them, special attention has been paid to the neural bases for nonsexual pheromones in ants.…”