Neural basis of singing in crickets: central pattern generation in abdominal ganglia

Abstract

The neural mechanisms underlying cricket singing behavior have been the focus of several studies, but the central pattern generator (CPG) for singing has not been localized conclusively. To test if the abdominal ganglia contribute to the singing motor pattern and to analyze if parts of the singing CPG are located in these ganglia, we systematically truncated the abdominal nerve cord of fictively singing crickets while recording the singing motor pattern from a front-wing nerve. Severing the connectives anywhere between terminal ganglion and abdominal ganglion A3 did not preclude singing, although the motor pattern became more variable and failure-prone as more ganglia were disconnected. Singing terminated immediately and permanently after transecting the connectives between the metathoracic ganglion complex and the first unfused abdominal ganglion A3. The contribution of abdominal ganglia for singing pattern generation was confirmed by intracellular interneuron recordings and current injections. During fictive singing, an ascending interneuron with its soma and dendrite in A3 depolarized rhythmically. It spiked 10 ms before the wing-opener activity and hyperpolarized in phase with the wing-closer activity. Depolarizing current injection elicited rhythmic membrane potential oscillations and spike bursts that elicited additional syllables and reliably reset the ongoing chirp rhythm. Our results disclose that the abdominal ganglion A3 is directly involved in generating the singing motor pattern, whereas the more posterior ganglia seem to provide only stabilizing feedback to the CPG circuit. Localizing the singing CPG in the anterior abdominal neuromeres now allows analyzing its circuitry at the level of identified interneurons in subsequent studies.

Cellular basis for singing motor pattern generation in the field cricket (Gryllus bimaculatus DeGeer)

“…Recent experiments had revealed that these two ganglia house the singing-pattern generator (Schöneich and Hedwig 2011). To test whether a recorded interneuron was part of the singing CPG, we modulated its spike activity by intracellular current injection and analyzed its impact on the ongoing motor pattern.…”

“…As the mesothoracic ganglion houses the motoneurons, which are driving the sonorous wing movements, for some decades it was surmised that the singing CPG is also located in this ganglion (review: Kutsch and Huber 1989). Recent studies, however, demonstrated that the neural network that generates the singing motor pattern spans from the metathoracic (Hennig and Otto 1995) to the first unfused abdominal ganglion (Schöneich and Hedwig 2011), and preliminary experiments reported an ascending singing interneuron in the first unfused abdominal ganglion, which elicited and reset the singing motor pattern when stimulated with intracellular current injection (Schöneich and Hedwig 2011). …”

Rigidity and Flexibility: The Central Basis of Inter-Leg Coordination in the Locust

“…In the locust, beyond their role in walking, the hind legs are used for jumping and accordingly differ structurally from the two rostral pairs of legs. Furthermore, anatomically, the metathoracic ganglion is fused together with three abdominal ganglia, which could affect the thoracic central patterns, as shown in cricket song production (Schöneich and Hedwig, 2011). Some studies in insects have already indicated that the metathoracic motor activity differs functionally from that of the pro- and mesothoracic ganglia: Bässler et al (1985) showed that the inherent direction of stepping of the stick insect hind legs is backward, whereas the front legs naturally walk forward, and a recent study on fruit flies identified metathoracic ganglion neurons that induce backward-walking (Bidaye et al, 2014).…”

Towards an Understanding of the Neural Basis of Acoustic Communication in Crickets

“…However, singing always immediately stops when connectives between T3 and A3 are sectioned (Fig. 8.2b, c;Schöneich and Hedwig 2011). Thus, a crucial part of the singing network must be housed in A3 and current results point towards T3-A3 as the ganglia housing the network of the singing pattern generator.…”

“…MB mushroom body, α-L alpha lobe, β-L beta lobe, Pe pedunculus, CB central body complex, PB protocerebral bridge. a From Wenzel and Hedwig (1999), b from Schöneich and Hedwig (2011), c modified from (Huber 1955; Fig. 1) with permission of John Wiley and Sons stimulation with Eserine is an efficient way to release singing activity, even after all thoracic sensory and motor nerves are cut a fictive singing motor pattern is generated (Poulet and Hedwig 2006).…”