Jennifer S. Altman

Descending interneurones from the brain and suboesophageal ganglia and their role in the control of locust behaviour

Abstract Lesion and stimulation experiments suggest that the suboesophageal ganglion (SOG) plays a special role in the control of insect behaviour: in bilateral coordination and by maintaining ongoing motor activity. Anatomical observations indicate that there are descending interneurones (DINs) originating in the SOG in addition to those from the brain. An SOG preparation for sampling both types of DIN intracellularly in walking locusts is described. Forty-three units showing activity changes during leg movements and walking were recorded. Using dye injection six were shown to be through-running axons; one was an SOG ascending interneurone; and eight were SOG DINs, 7 contralateral, one ipsilateral. All fired before or during movements and received various sensory inputs. Many gave complex responses to different modalities, several showing directional preferences. Some SOG neurones showed spontaneous changes in activity; activity outlasting movements; or responses to passive as well as active movements. These preliminary results suggest neuronal substrates for the special functions of the SOG in behaviour. They also indicate that DINs, rather than being simple relays, are part of a dynamic network which includes the motor centres. Regulation of complex and subtle aspects of behaviour may be achieved by dynamic and sequential patterns of activity in groups of DINs, some of which may be multifunctional.

Suboesophageal Neurons Involved in Head Movements and Feeding in Locusts

The projections of nerves 6 and 7 of the locust suboesophageal ganglion (SOG) were stained by axonal filling with cobalt chloride. Nerve 6 contains two motoneurons which innervate neck muscles 50 and 51. Sensory neurons innervating hairs on the dorso-occipital region of the head also enter the ganglion through nerve 6 and terminate in a small bilateral plexus. The projections of the head hairs in nerve 6 do not overlap the arborizations of the motoneurons or the neurons of nerve 7, but lie in the same area as descending sensory neurons from wind–sensitive hairs of the front of the head. One branch of nerve 7 (7 B) contains two fibres which innervate the salivary gland. These ‘salivary’ neurons (labelled SN1 and SN2) have their cell bodies in the ganglion. The second branch, 7A, contains sensory neurons from the submentum of the labium, which form four sensory plexuses, two dorsal and two ventral. The sensory plexuses from the submentum have specific regions of overlap with the salivary neurons and with the neck muscle motoneurons. We interpret these as indicating a flow of information from labial receptors signalling head and mouthpart movement to neurons involved in salivation and head movement. We further postulate that the anatomical separation of the various sensory plexuses is indicative of functional localization within the ganglion.

Programmed cell death: the paths to suicide.

fection. In this regard, a congenital deficiency in the [~2 integrin chain, and therefore in LFA-1, results in a condition called leucocyte adhesion deficiency, which is lethal unless treated by bone marrow transplantation in early life 1°. It has been proposed that the use of combinations of pairs of adhesion receptors and activation signals by leucocytes could explain the selective recruitment of certain leucocyte subsets, such as memory lymphocytes, to particular lymph nodes or sites of infiammarion, and the preferential recruitment of neutrophils early in the inflammatory process 15. This may be of particular interest in multiple sclerosis, for example, where relapse and remission are common features of the disease. Finally, with respect to acute CNS trauma, the prospect of antiinflammatory treatment by blocking leucocyte recruitment is particularly attractive as it is likely to require only a short period of treatment and should not lead to side effects, such as an immune response to the therapeutic antibody. In addition, short-term treatment should not leave patients vulnerable to the effects of infection by diminishing their normal immune response.

New Models for Motor Control

What do a prototype robot (Brooks 1989) and a model for the control of behavioral choice in insects (Altman and Kien 1987a) have in common? And what do they share with a scratching cat (Shadmehr 1989)? The answer is distributed control systems that do not depend on a central command center for the execution of behavioral outputs. The first two in particular are examples of a growing trend to replace the long-held concept of linear hierarchical control of motor output with one of decentralized, distributed control, with inputs at many levels and the output a consensus of the activity in several centers. Brooks (1989) describes a six-legged machine that, in its most advanced form, can walk over rough terrain and prowl around following a source of warmth, such as a person. The six legs, chosen as a compromise between stability and ease of coordination, give the robot a superficial resemblance to an insect but the similarity goes deeper. The modular control system, designed strictly on engineering principles for maximum efficiency and economy, bears a striking similarity to the model we have proposed elsewhere (Altman and Kien 1987a) to describe the organization of the motor system in insects such as the locust. In both systems, the same set of components can generate different behaviors, depending on the context, and similar principles govern the generation of different levels of behavior, from movements of a single leg to coordinated responses of the whole beast. Neither requires a single center for integrating all sensory information and conflicts tend to be resolved by consensus at the motor level.

Preparation and execution of movement: Parallels between insect and mammalian motor systems

1. The organization of the motor systems underlying locomotion in insects and mammals is surprisingly similar. There are also parallels between the insect motor system and the system underlying reaching and the occulomotor system in primates. 2. The movements generated by all these systems are planned or prepared before their execution and there is a partial separation of circuits for preparation and execution. 3. These circuits consist of multiple descending pathways interconnected to form overlapping loops which work co-operatively to determine the motor output. Thus, both insect and mammalian motor systems can be treated as parallel distributed (PDP) systems. 4. This enables a comparison of functional levels of processing in the different systems and also provides a basis for modelling motor systems with attractor neural networks.

A Model for Decision Making in the Insect Nervous System

Little is known about the neuronal mechanisms for selecting behavioural outputs appropriate to ongoing conditions. We present a model in which decisions are made by a concensus between the inputs at each stage in the system, not by a few neurones in a single centre. The stages are interconnected by loops of varying lengths, each with specific control functions. Neuromodulators and hormones contribute to the overall output by altering excitability but no single input is necessary and sufficient for producing any output.

Organisation of intersegmental interneurons in the suboesophageal ganglion of Schistocerca gregaria (Forksal) and Locusta migratoria migratorioides (Reiche & Fairmaire) (Acrididae, Orthoptera

Abstract The subeosophageal ganglion (SOG) in insects is both a segmental centre coordinating the mouthparts and neck muscles and a suprasegmental motor control centre. Descending interneurons (DINs) and ascending interneurons (AINs) originating in the SOG project to the segmental motor centres of the ventral nerve cord and to the brain, respectively. Here, we show that there are about 300 DINs with cell bodies in the SOG, and present detailed description of the morphology of the 36 largest DINs and 17 AINs, most of which are members of bilateral pairs. Most have extensive dorsal branching usually extending through more than one of the 3 fused segmental neuromeres. All have some ventral or ventrolateral branching, but 2 DINs and 2 AINs are characterised by particularly extensive ventromedial branching. Some of the other AINs have more extensive ventral branching than the DINs. Functional implications of the overlaps of the interneurons with motor, sensory and other interneurons in the SOG support the role of these neurons in suprasegmental co-ordination with a possible subsidiary role in local motor control.

The role of sensory inputs in insect flight motor pattern generation

Abstract Studies on intact flying locusts are revealing the important part played by phasic sensory inputs in regulating the flight motor output in insects and require a radical revision of the concept of the flight pattern generator.

Decision-making in the insect nervous system: a model for selection and maintenance of motor programmes

Publisher Summary This chapter presents a decision-making model system for the selection and maintenance of motor programs. In this model, the selection of an appropriate output is a function distributed over the whole nervous system. A particular behavior occurs as a result of the balance of activities in different parts of the nervous system at any instant. The decision-making model considers the motor system as several interconnected stations, which approximate to brain, suboesophageal ganglion, and segmental ganglia in the locust. Each station contains the networks that generate the output of the station. The three basic principles that determine the model are across-fiber patterns, consensus, and interconnections in loops. These principles offer tools for analyzing the operations of circular systems, taking the dynamics and flexibility of behavior into account. This model is useful in analyzing the functions of various molluscan networks and is able to simulate learning and memory. It provides a powerful tool for the formal modeling of a motor function that is now essential for a deeper understanding of the operating principles involved in motor control.

Some insect sensory neurones contain 5-hydroxytryptamine

Immunocytochemistry of the locust central nervous system shows that most segmental nerves, in particular those of the legs, contain afferent fibres that react with antibody to 5-hydroxytryptamine (5-HT). Adsorption controls indicate that the antigen is 5-HT or a closely related compound. This is supported by the finding of significant amounts of 5-HT in leg nerves using reverse phase high-performance liquid chromatography (HPLC) and electrochemical detection. On the other hand 5-HT was not detectable in locust antennal and cercal nerves with either immunocytochemistry or with HPLC. These results strongly support that some populations of sensory neurones in the locust contain 5-HT.