Insect Neurochemistry and Neurophysiology

Alexej B. Borkovec

• Publisher: CRC Press
• Year: 2019
• Print ISBN: 9781315894492
• eBook ISBN: 9781351090490
• Topic: Biological Sciences
• Subtopic: Biology
• Index: Biological Sciences

This book represents proceedings from ICINN 1993, and comprises papers on nerve function, neurotransmitters, ion channels, second messengers and neuropeptides. By using a variety of techniques, combining aspects of nrurophysiology, pharmacology, immunology, peptide separation and sequencing or molecular biology, it has become possible to study systems in greater detail and complexity than before.

Reviews

Neural networks and the control of locomotion in insects

M. Burrows

Zoology Department, University of Cambridge Downing Street, Cambridge CB2 3EJ, England

This paper analyses some of the neural mechanisms by which adaptive locomotory behaviour of an insect is produced, in order to learn about the general properties of the neurones involved, and the circuits that they form. This vast topic is reduced to more manageable proportions by concentrating on a specific question: how are sensory signals from mechanoreceptors on a leg processed in the central nervous system so that an appropriate and fine adjustment of posture or locomotion is produced? What are the networks that are involved and how are they designed for this processing? How are the constituent intemeurones connected to perform these tasks and in particular what are the integrative properties of the essential local intemeurones?

The leg and the nervous system chosen for study belong to a locust (Schistocerca gregaria (Forskal)). This insect is chosen for the design of its nervous system and for the range of behaviour that it shows. Moreover, intracellular recordings can be made from neurones whilst the animal is alert, so that the action of a particular neurone can be related directly to the behaviour of the animal. Individual neurones can be identified according to their physiological actions and properties, their morphology at the level of the light microscope, and the distribution of their synapses as seen in the electron microscope.

Local reflexes

Some 10,000 sensory axons from one hind leg converge onto the segmental, metathoracic ganglion that controls the movements of the hind legs. Many of these afferents are from mechanoreceptors that provide information about touch (exteroceptors) and about movement of the joints (proprioceptors), but many others are from chemoreceptors. By contrast, only some 100 motor neurones are responsible for generating the complex patterns of muscular contractions that are required of this leg in locomotion and in adjusting posture. Considerable convergence and integration is therefore indicated. Moreover, the spatial information provided by the receptors must be preserved because specific local reflexes can be evoked by stimulation of restricted arrays of receptors (Siegler and Burrows, 1986). For example, touching hairs on the ventral surface of the tibia causes the trochanter to levate and move the femur forwards, the tibia to extend and the tarsus to depress, whereas touching hairs a few mm away on the dorsal tibia causes a different sequence of movements of these joints. These are adaptive compensatory reflexes ensuring that the leg moves to avoid an object into which it might bump during the course of locomotion. These reflexes define the nature of the integrative problems that must be solved in the nervous system. Similarly, movements of a joint evoke reflex responses in the motor neurones innervating muscles of that and adjacent joints. In quiescent animals these inputs result in resistance reflexes that oppose the imposed movements, but in more active animals assistance reflexes result which reinforce the movement.

The neural commonents

Each half of the metathoracic ganglion contains all the motor neurones that move a hind leg and perhaps as many as 1,000 interneurones, of which a few hundred are involved with the control of each leg. Many are local interneurones with branches restricted entirely to this ganglion. There are 2 classes of these local interneurones, some which normally generate action potentials (spiking local interneurones) and some which normally do not (non spiking local interneurones). Others are intersegmental interneurones with axons that project to adjacent ganglia in the segmental chain. Axons from interneurones that receive sensory stimuli from other legs and other parts of the body also project to this ganglion. These are the neurones that provide the basic framework from which the local networks must be organised.

Processing the afferent signals

Tactile hairs are stimulated when a leg bumps into an external obstacle and their afferents elicit an appropriate adaptive response. Each of these hairs is innervated by a single sensory neurone whose spikes can be recorded from the cut end of a hair shaft. The terminals of these sensory neurones forn1 a three dimensional map of the surface of the leg within an area of ventral neuropil (Newland, 1991). Which neurones process this initial barrage of sensory signals? Spiking local interneurones with cell bodies in a ventral midline (Siegler and Burrows, 1984) or antero-medial group (Nagayama, 1989) receive direct excitatory inputs from these and other afferents (Siegler and Burrows, 1983; Nagayama and Burrows, 1990). The gain of this first synapse between the afferents and the interneurones can be high so that each afferent spike can evoke a spike in the interneurone. Each interneurone receives inputs from a particular array of receptors, and these comprise its receptive field. Not all the receptors in a field contribute equally, some forming high gain synapses, others of lower gain (Burrows, 1992). These interneurones form a map of the surface of the leg, by virtue of the arrays of direct connections formed by the particular afferents. The interneurons have two fields of branches within the ganglion: on in ventral neuropil to which the afferent neurones project, and one in more dorsal neuropil where motor neurones and other interneurons have branches. The ventral branches correspond to the afferent map and to the receptive field of the interneuron (Burrows and Newland, 1993). Thus for example, an interneuron with a receptive field on the tarsus has branches only in a posterior region of neuropil to which the tarsal hair afferents project. Two important features of these receptive fields emerge; first one region of the leg is represented by several interneurones so that there is parallel processing within this class of interneurone. Second, the specificity of the connections ensures that spatial information provided by the receptors is preserved in separate channels.

The exteroceptive afferents do not, however, simply connect with these interneurones. Many also connect with intersegmental interneurones so that information is conveyed to ganglia that control the movements of the other legs (Laurent, 1988; Laurent and Burrows, 1988). A few also connect directly with non spiking interneurones (Burrows, Laurent and Field, 1988; Laurent and Burrows, 1988), but most of the input to these interneurones is first processed by the spiking local interneurones. Some afferents bypass the circuitry formed by the local interneurones and synapse directly with motor neurones (Weeks and Jacobs, 1987; Laurent and Hustert, 1988). There is therefore divergence of the afferent signals to several classes of neurone and parallel distributed processing.

Many of the same neurones and the same pathways are involved in processing the input from the proprioceptors. A major difference is that many of these afferents synapse directly on the motor neurones themselves (Burrows, 1987b). In addition to these direct pathways, parallel pathways involving the spiking and the non spiking interneurones also exist. Considerable processing also occurs in the terminals of these afferents (Burrows and Laurent, 1993). Afferents that respond to a particular movement of the joint excite an unidentified group of interneurones that then evoke depolarising inhibitory synaptic potentials in the terminals of other afferents responding to the same movement. The result is a reduced efficacy of transmission by the afferent to its postsynaptic motor neurone (Burrows and Matheson, 1993).

Out1mt connections of the local interneurones

What happens to the signals after they have been processed by the local interneurones? The midline spiking local interneurones make inhibitory output connections (Burrows and Siegler, 1982), whereas the antero-medial interneurones make excitatory connections (Nagayama and Burrows, 1990). All the effects revealed so far are mediated by spikes, so that each spike in an interneurone is followed by either an IPSP or an EPSP in the postsynaptic neurone. Members of the midline group make a restricted number of inhibitory connections with motor neurones (Burrows and Siegler, 1982), but more widespread connections with non spiking interneurones (Burrows, 1987a), with intersegmental interneurones (Laurent 1987b) and with antero-medial spiking interneurones (Nagayama and Burrows, 1990). Many of the members of this group of spiking local interneurones stain with an antibody raised against GABA and their inhibitory actions can be blocked by a GABA antagonist (Watson and Burrows, 1987).

Non spiking interneurones make either excitatory or inhibitory output connections, but they do so without the intervention of spikes. Their effects on postsynaptic neurones are mediated by the graded release of chemical transmitter (Burrows and Siegler, 1978). They exert profound effects on the spiking patterns of motor neurones which they organise into sets that are appropriate for the execution of normal movements of a leg (Burrows, 1980). They also make inhibitory connections with other non spiking interneurones in lateral inhibitory networks (Burrows, 1979).

Properties of the local interneuroncs

From this information about the two physiological classes of local interneurones the following conclusions can be drawn.

Midline spiking local interneurones

1. Collate afferent information from arrays of receptors whilst preserving spatial information.
2. Reverse the sign of the afferent signal from excitatory to inhibitory in their output connections with many other types of neurone.
3. Limit the receptive fields of non spiking and intersegmental interneurones and enhance the borders through lateral inhibition.
4. Exclude the action of non spiking interneurones whose motor effects would be inappropriate, and disinhibit those whose action would be appropriate.

Non spiking interneurones

1. Release chemical transmitter in a graded manner in response to small changes in their voltage. This means that they exert a precise control over the membrane potential and spike frequency of their postsynaptic neurones.
2. Exclude the action of interneurones with inappropriate actions for a particular movement through lateral inhibition.
3. Control groups of motor neurones in sets appropriate for normal locomotion. Each interneurone synapses on several motor neurones, and in turn each motor neurone receives inputs from several non spiking interneurones.

Adjusting the motor output

What are the key elements that have been identified so far in the circuits that are responsible for adjusting the motor output so that it is appropriate to the prevailing behavioural circumstances? Non spiking interneurones, by virtue of their connections with pools of motor neurones, their inputs from afferents and their interactions with local interneurones appear crucial for the execution of a local reflex. Manipulating the membrane potential of one of these interneurones alters the effectiveness of a local reflex in a graded manner. Therefore, despite the parallel and distributed processing, a single interneurone can play a substantial role in a reflex pathway. From this observation it would be expected that any synaptic inputs to a non spiking interneurone might be able to change a reflex, and that this might be the way that intersegmental inputs place a local response in the appropriate behavioural context. Members of a population of intersegmental interneurones with cell bodies in the mesothoracic ganglion receive inputs from a middle leg and have axons that project to the metathoracic ganglion (Laurent, 1987a). The receptive fields of these interneurones are shaped by the same series of connections as for the local interneurones: direct excitation from afferents, inhibition by spiking local interneurones (Laurent, 1987b). In the ganglion controlling the hind legs these intersegmental interneurones connect with non spiking interneurones and with some motor neurones (Laurent and Burrows, 1989a). The connections are specific and are related to the receptive field of the intersegmental interneurone and to the output connections of the non spiking interneurone. The effect of these connections is to alter the output of a non spiking interneurone and thus its participation in a local reflex (Laurent and Burrows, 1989b).

Reflex pathways

The pathways used for local reflex movements of a hind leg can thus be defined in detail that is sufficient to allow a sensory signal to be followed through its various integrative stages to its emergence as an adaptive motor response. Moreover, it is possible to pin-point some of the crucial elements in these pathways where modifications can occur. For example, the role of non spiking interneurones in adjusting the motor output and acting as the summing points for both intra- and intersegmental effects has been highlighted. The following characteristics of the networks can be recognised:

1. There is considerable convergence from the afferents to the first interneuronal layer, but spatial information is nevertheless preserved.
2. The afferent signals diverge to make excitatory connections with different classes of neurones. Therefore, parallel distributed processing of the same signals b...

Table of contents

• Cover
• Half Title
• Title Page
• Copyright Page
• Table of Contents
• Reviews
• Reports of Current Research: Neuroanatomy and Neural Function
• Signalling Within the Nervous System
• Insect Neuropeptide Research
• Adipokinetic Hormone
• Allatoregulatory Peptides
• Fmrfamide
• Pheromone Biosynthesis Activating Neuropeptide
• Proctolin
• Peptides Affecting Development
• Peptides Affecting Reproduction
• New Neuropeptides
• Neuropeptide Metabolism
• Receptor Studies
• Subject Index
• Author Index
• Conference Attendees