Modular timer networks: abdominal interneurons controlling the chirp and pulse pattern in a cricket calling song

Abstract

Chirping male crickets combine a 30 Hz pulse pattern with a 3 Hz chirp pattern to drive the rhythmic opening-closing movements of the front wings for sound production. Lesion experiments suggest two coupled modular timer-networks located along the chain of abdominal ganglia, a network in A3 and A4 generating the pulse pattern, and a network organized along with ganglia A4–A6 controlling the generation of the chirp rhythm. We analyzed neurons of the timer-networks and their synaptic connections by intracellular recordings and staining. We identified neurons spiking in phase with the chirps and pulses, or that are inhibited during the chirps. Neurons share a similar “gestalt”, regarding the position of the cell body, the dendritic arborizations and the contralateral ascending axon. Activating neurons of the pulse-timer network elicits ongoing motor activity driving the generation of pulses; this activity is not structured in the chirp pattern. Activating neurons of the chirp-timer network excites pulse-timer neurons; it drives the generation of chirps and during the chirps the pulse pattern is produced. Our results support the hypothesis that two modular networks along the abdominal ganglion chain control the cricket calling song, a pattern generating network in the mesothoracic ganglion may not be required.

Lesions of abdominal connectives reveal a conserved organization of the calling song central pattern generator (CPG) network in different cricket species

“…In G. bimaculatus , lesions to the abdominal nerve cord implicated a different role of each abdominal ganglion for the generation of pulses and chirps, which define the calling song structure (Jacob and Hedwig 2016 ). These findings showcase the importance of the abdominal ganglia in cricket song pattern generation and have been supported by intracellular studies of singing interneurons recorded and identified in the abdominal ganglia (Schöneich and Hedwig 2011 , 2012 ; Jacob and Hedwig 2019 , 2020 ).…”

“…This is in line with the results in G. bimaculatus (Jacob and Hedwig 2016 ), suggesting that the A3 ganglion is part of a pulse-timer network. This is also supported by the discovery of an ascending opener interneuron in A3 (Schöneich and Hedwig 2011 , 2012 ), which has been identified in five cricket species (Jacob and Hedwig 2019 , 2020 ) and is an element of the singing-CPG. It shows bursts of spikes preceding wing opener motoneuron activity and elicits singing motor activity upon current injection.…”

Acoustic signalling in Orthoptera

“…In Gryllus bimaculatus, lesions to the abdominal nerve cord showed that the abdominal ganglia each have a different role in defining the song structure (Jacob and Hedwig, 2016). Data derived from intracellular recordings of activity in singing interneurons provide support for the results obtained by lesioning (Jacob and Hedwig, 2019;Jacob and Hedwig, 2020;Schöneich and Hedwig, 2011;.…”

A small, computationally flexible network produces the phenotypic diversity of song recognition in crickets

“…In this scenario, a female network that has the capacity to produce many different preference types supports the ability of the communication system to diverge. However, this co-evolution of song preference and song structure requires male song production networks to be as flexible as the female song recognition networks (Jacob and Hedwig, 2020;Schöneich, 2020). There is also accumulating evidence for genetic coupling between the networks that produce and recognize the song pattern, which may ensure that sender and receiver stay tuned during evolution of song pattern (Xu and Shaw, 2019;Schöneich, 2020;Xu and Shaw, 2021).…”