On the Role of the Head Ganglia in Posture and Walking in Insects

Abstract

In insects, locomotion is the result of rhythm generating thoracic circuits and their modulation by sensory reflexes and by inputs from the two head ganglia, the cerebral and the gnathal ganglia (GNG), which act as higher order neuronal centers playing different functions in the initiation, goal-direction, and maintenance of movement. Current knowledge on the various roles of major neuropiles of the cerebral ganglia (CRG), such as mushroom bodies (MB) and the central complex (CX), in particular, are discussed as well as the role of the GNG. Thoracic and head ganglia circuitries are connected by ascending and descending neurons. While less is known about the ascending neurons, recent studies in large insects and Drosophila have begun to unravel the identity of descending neurons and their appropriate roles in posture and locomotion. Descending inputs from the head ganglia are most important in initiating and modulating thoracic central pattern generating circuitries to achieve goal directed locomotion. In addition, the review will also deal with some known monoaminergic descending neurons which affect the motor circuits involved in posture and locomotion. In conclusion, we will present a few issues that have, until today, been little explored. For example, how and which descending neurons are selected to engage a specific motor behavior and how feedback from thoracic circuitry modulate the head ganglia circuitries. The review will discuss results from large insects, mainly locusts, crickets, and stick insects but will mostly focus on cockroaches and the fruit fly, Drosophila.

Keywords: central complex; cerebral ganglia; gnathal ganglia; insect; motor control; neuroethology; posture; walking.

FIGURE 1

(A) The tripod gait predominantly used by cockroaches. Blue bars represent swing phases of the left (L) and right (R) front (1), middle (2), and hind legs (3) (modified with permission from Ayali et al., 2015). (B) To evaluate synchronization and coordination, activity (EMG) is recorded from the same muscle in two different legs. Period and time delay are measured cycle by cycle. (C) Relative occurrence of phases of R2 in the cycle of R3 is represented as a histogram. In the present case, the median phase is 0.5 showing that this pair of legs are active in anti-phase.

FIGURE 2

Coordination in cockroaches with head ganglia lesions. Left panels: EMG traces from the coxal depressor muscles, demonstrating the coordination between the right mesothoracic leg (R2) and the right and left metathoracic legs (R3 and L3) in control, CRG-less, and GNG-less cockroaches. Spontaneously initiated locomotion of control and brainless cockroaches is characterized by the tripod-gait coordination. GNG-less cockroaches fail to show spontaneous tripod-gait coordinated locomotion. Right panels: Relative occurrence of phases of R2 and R3 in the cycle of L3. The median phases are also indicated. Note the lack of tripod-gait coordination in GNG-less cockroaches (adapted with permission from Gal and Libersat, 2006). A cockroach is also shown ventral side up with red dots indicating the location of the insertion of the EMG electrodes.

FIGURE 3

Similarity of the anatomy of the central complex across species. (A) Overview of the central complex and support structures: The protocerebral bridge (PB), fan-shaped body (FB) or central body upper (CBU), ellipsoid body (EB) or central body lower (CBL), noduli (NO), and lateral accessory lobe (LAL) in the locust and cockroach. (B) Same like in A for locust and fly (reprinted with permission from Turner-Evans and Jayaraman, 2016; with permission of Copyright Clearance center, license number 4597641450839 and courtesy of Vivek Jayaraman).

FIGURE 4

(A) An adult wasp stings a cockroach into the head to manipulate the cockroach behavior. (B) Drawing of a frontal view of the cockroach head ganglia (CRG: cerebral ganglia, CX: central complex, AL: antennal lobes, MB: mushroom bodies; GNG: gnathal ganglia). (C) Diagram of the cockroach CRG. Central complex is within red rectangle. PB: protocerebral bridge, FB: fan-shaped body, EB: ellipsoid body, LAL: lateral accessory lobes, MB: mushroom bodies (reproduced with permission from Ritzmann et al., 2012; courtesy of Josh Martin and Roy Ritzmann; License: CC BY 4) (D) Autoradiographs of the cerebral ganglia and the gnathal ganglia of a cockroach stung by a radio-labeled wasp. Black staining indicates the presence of venom (adapted with permission from Haspel et al., 2003).

FIGURE 5

Activity in coxal slow motoneuron recorded as EMG spikes from the coxal depressor muscle after procaine injection to the central complex (CX). (A) Representative EMG recordings traces of coxal slow motoneuron ongoing activity 5 min after (upper trace; before procaine effect), 30 min after (middle trace; peak procaine effect), and 30 min after (lower trace; recovery from procaine effect) procaine injection to the CX. (B) Comparison of EMG spikes (spikes/sec) following saline (control; n = 6) and procaine (n = 6) injection to the CX. A significant decrease (P < 0.05; t-test) was found 30 min after procaine injection as compared to 30 min after saline injection. Each bar represents the averaged spikes/second ± SEM; significance is indicated with asterisk. (C) A representative image for postmortem verification of injection site. Arrow indicates the injection site in the fan-shaped body of the CX (adapted with permission from Emanuel and Libersat, 2017).