Neurochemical Architecture of the Central Complex Related to Its Function in the Control of Grasshopper Acoustic Communication

Abstract

The central complex selects and coordinates the species- and situation-specific song production in acoustically communicating grasshoppers. Control of sound production is mediated by several neurotransmitters and modulators, their receptors and intracellular signaling pathways. It has previously been shown that muscarinic cholinergic excitation in the central complex promotes sound production whereas both GABA and nitric oxide/cyclic GMP signaling suppress its performance. The present immunocytochemical and pharmacological study investigates the question whether GABA and nitric oxide mediate inhibition of sound production independently. Muscarinic ACh receptors are expressed by columnar output neurons of the central complex that innervate the lower division of the central body and terminate in the lateral accessory lobes. GABAergic tangential neurons that innervate the lower division of the central body arborize in close proximity of columnar neurons and thus may directly inhibit these central complex output neurons. A subset of these GABAergic tangential neurons accumulates cyclic GMP following the release of nitric oxide from neurites in the upper division of the central body. While sound production stimulated by muscarine injection into the central complex is suppressed by co-application of sodium nitroprusside, picrotoxin-stimulated singing was not affected by co-application of this nitric oxide donor, indicating that nitric oxide mediated inhibition requires functional GABA signaling. Hence, grasshopper sound production is controlled by processing of information in the lower division of the central body which is subject to modulation by nitric oxide released from neurons in the upper division.

Encoding wide-field motion and direction in the central complex of the cockroach, Blaberous discoidalis

“…Interestingly, a recent metaanalysis strongly suggests that the CX is deeply homologous to the mammalian basal ganglia (Strausfeld and Hirth, 2013). Moreover, the CX is heavily invested in GABAergic (inhibitory) receptors as well as receptors for numerous neuromodulators, including dopamine (Homberg et al, 1999;Kahsai and Winther, 2011;Kunst et al, 2011;Kahsai et al, 2012).…”

Widespread Sensitivity to Looming Stimuli and Small Moving Objects in the Central Complex of an Insect Brain

“…Evidence for polarization-independent visual functions largely originates from behavioral experiments on mutant and transgenic flies (Drosophila melanogaster) with defects in parts of the CC. These studies suggest that CC neurons detect the orientation and elevation of edges (Liu et al, 2006), play a role in visually mediated spatial orientation memory (Neuser at al., 2008) and place memory (Ofstad et al, 2011), and are involved in the visual control of gap-crossing behavior . Data from neuronal recordings substantiating these results are missing, however, except for a single study reporting responses to moving bars in the CC of flesh flies (Phillips-Portillo, 2012).…”

“…5). Kunst et al (2011) showed that activation of PoU1 neurons in grasshoppers inhibits the generation of calling songs. This further supports the shut-off hypothesis.…”

“…Instead, CBU neurons were speculated to modify the response properties of polarization-sensitive neurons depending on the behavioral state of the insect (Homberg, 1994;Heinze and Homberg, 2009). Additionally, CBU neurons in flies (Liu et al, 2006;Phillips-Portillo, 2012) and locusts (Homberg, 1994) process unpolarized visual information.…”

GABA immunostaining in the central complex of dicondylian insects

“…GABA is a major inhibitory transmitter in the insect brain (Buckingham, Biggin, Sattelle, Brown, & Sattelle, ; Lummis, ). In all species studied, including grasshoppers (Homberg, Vitzthum, Müller, & Binkle, ; Kunst, Pförtner, Aschenbrenner, & Heinrich, ), the house cricket (Strambi et al, ), the tobacco hawk moth (Homberg, Kingan, & Hildebrand, ), the American cockroach (Blechschmidt, Eckert, & Penzlin, ), the honeybee (Mota et al, ; Schäfer & Bicker, ), and two species of flies (Hanesch et al, ; Meyer, Matute, Streit, & Nässel, ), the CBL showed dense GABA immunostaining. Detailed analysis in the locust Schistocerca gregaria , the fly Drosophila melanogaster , and the moth Manduca sexta identified tangential neurons of the CBL (termed TL neurons in locusts, R neurons in flies) to be immunostained.…”