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M Burrows

Publications and source records attributed to M Burrows.

At least 73 records · Page 4Linked to original sources

Spiking local interneurones in the mesothoracic ganglion of the locust: homologies with metathoracic interneurones.

Two bilaterally symmetrical groups of spiking local interneurones have been characterized in the mesothoracic ganglion of the locust. The cell bodies of one group, the "midline group," lie at the ventral midline. Their primary neurites run in the ventral loop of ventral commissure II to form extensive branches in the neuropile of one-half of the ganglion. A dorso-ventral process in the perpendicular tract links two distinct fields of branches, one ventral and consisting of numerous fine branches of a uniform texture that arise from stout secondary neurites, and the other more dorsal consisting of fewer branches of a varicose appearance. Cell bodies of the second, the "anterior-lateral" group, lie close to the lateral edge of an anterior connective. Their primary neurites run in a more anterior ventral commissure and their neuropilar branches are divided into two fields by a process in a more anterior dorso-ventral tract. Within the two groups, each interneurone has its own distinctive shape that is an elaboration on these basic plans. Each interneurone also has its own characteristic physiology, being excited by a particular array of mechanoreceptors on the middle leg on the same side of the body as its neuropilar branches. The receptive fields of the interneurones, defined in this way, can be extensive and cover a particular surface of all parts of the leg, or restricted to one surface of, for example, the tarsus. These interneurones therefore bear a striking resemblance to two groups of spiking local interneurones in the adjacent segmental ganglion of the metathorax.

Action Potentials↗

Processing by local interneurons of mechanosensory signals involved in a leg reflex of the locust.

At the distal end of the tibia of a locust hind leg are 2 pairs of movable spurs that can be moved by contact with external objects--as, for example, when the body sways from side to side and loads one leg unevenly or when the foot is placed on rough ground--but not by direct muscular action. Movements imposed on a spur evoke phasic bursts of spikes in the axon of a single receptor cell at its base. If the displacement is maintained, however, the response adapts within a few seconds. The afferents from these spur receptors excite particular spiking local interneurons with cell bodies at the ventral midline of the metathoracic ganglion. Each afferent spike is consistently followed at a constant latency by a depolarizing potential in one of these interneurons. The potential can evoke a spike, and its amplitude is enhanced by a hyperpolarization applied to the interneuron. The central delay to this chemically mediated EPSP, which also includes conduction time to synaptic sites, probably indicates a direct connection. Some spiking local interneurons are excited by the 2 anterior spurs but are unaffected by the 2 posterior ones, while others receive the converse pattern of inputs. The receptive fields of these interneurons also include regions on either the anterior or posterior surfaces of the tibia with excitatory inputs from hair afferents. A reliable inhibitory reflex effect on the single levator tarsi is evoked by movement of any of the 4 spurs. The inhibitory potentials are not caused directly by the sensory afferents but involve the spiking local interneurons upon which the afferents synapse. The receptive field of this motor neuron therefore results from the convergence of inputs from a few interneurons. Motor neurons of other tarsal muscles are unaffected by movement of the spurs, but those of some more proximal muscles may be excited. These reflex effects should enhance the traction of the tarsus with the ground.

Afferent Pathways↗

Receptive fields of motor neurons underlying local tactile reflexes in the locust.

The receptive fields of motor neurons to a hind leg were mapped by recording intracellularly from their cell bodies or from the muscle fibers they innervate while stimulating mechanoreceptors on the surface of that leg. Each motor neuron is affected by a specific array of receptors that make up its receptive field. Boundaries along the anteroposterior or dorsoventral axes of the leg divide the receptive fields into excitatory and inhibitory regions. Proximodistal boundaries may correspond to the articulations between parts of the leg. Motor neurons that innervate antagonistic muscles have complementary receptive fields, so that the region that is excitatory for one is inhibitory for the other. The receptive fields of the motor neurons overlap. Tactile stimulation therefore leads to a specific local reflex that involves the coordinated movement of the segments of a leg. Five local reflexes are described, each of which moves the leg away from the site of stimulation. Afferents from the external mechanoreceptors do not synapse directly on the motor neurons, but instead on spiking local interneurons, some of which then synapse directly on motor neurons. These local interneurons have smaller receptive fields delineated by the same boundaries, so that the receptive fields of the motor neurons can be constructed from appropriate combinations of them. It is suggested that receptive fields are organized as "functional maps" that are appropriate for particular behavioral responses rather than solely to preserve or refine spatial information.

Animals↗

The distribution of synapses on the two fields of neurites of spiking local interneurones in the locust.

Spiking local interneurones in the metathoracic ganglion of the locust have two fields of neuropilar branches linked by a single process. One, with numerous fine neurites of relatively uniform diameter, is in a ventral area of neuropile where the afferents from hairs on a hind leg also terminate. The other, with sparser and varicose neurites, is in a more dorsal area of neuropile where the motor neurones of the leg muscles have many neurites. Physiological studies have shown that these interneurones receive direct inputs from some hair afferents and in turn synapse directly upon some leg motor neurones (Burrows and Siegler, '82; Siegler and Burrows, '83). The distribution of synapses in these two fields was revealed by injecting HRP intracellularly into an interneurone following its physiological characterization. In the ventral field, the majority of synapses are input synapses. Many are from profiles with round agranular vesicles of similar diameter to those of known afferents. Other presynaptic profiles contain pleomorphic agranular, or large round granular, vesicles. There are also some output synapses, each with only a small population of vesicles. Most input synapses are made onto small-diameter neurites, whereas the majority of outputs are made from the larger-diameter neurites. In the dorsal field, the majority of synapses are output synapses. They are made from vesicle-filled varicosities onto postsynaptic profiles of small diameter. A single varicosity can be the site of many output synapses. Input synapses are few in number, but occur close to the output synapses. The absence of varicosities in the ventral field cannot therefore be correlated with a lack of output synapses and while the dorsal varicosities can be the sites of output, they can also receive input synapses.

Action Potentials↗

The structure of locust nonspiking interneurones in relation to the anatomy of their segmental ganglion.

The morphology of eight nonspiking local interneurones in the metathoracic ganglion of the locust is described in relation to known tracts, commissures, regions of neuropile, and identified motor neurones. They are compared with the spiking local interneurones in the same ganglion. Each nonspiking local interneurone was injected intracellularly with cobalt, following characterization of its physiological effects on identified leg motor neurones. The shapes of the nonspiking interneurones are diverse, although all have processes restricted to one ganglion and lack an axon. Their cell bodies are distributed in the ventral and dorsal cortex of the ganglion. Interneurones with cell bodies in similar places have similar basic structures, with primary neurites in the same commissure or tract, and major branches in the same tracts. The fine branches of all the interneurones have the same texture throughout, and occur in the same lateral region of neuropile, dorsal to the prominent neurite of the fast extensor tibiae motor neurone. Some interneurones have branches that extend both to the midline and to the dorsal boundary of the neuropile, but none have branches in the ventral, medial neuropile. This distribution of branches corresponds with two known features of the physiology of these interneurones: they make what appear physiologically to be direct connections with motor neurones, and have branches in the same region of the neuropile as the motor neurones. They do not appear to receive direct inputs from hair afferents, and they have no branches in the ventral neuropile to which these afferents project.

Action Potentials↗

The morphology and ultrastructure of common inhibitory motor neurones in the thorax of the locust.

The morphologies of three common inhibitory motor neurones which innervate muscles of a hind leg and the homologous three neurones which innervate muscles in a middle leg are described in relation to known commissures, tracts, and areas of neuropile in their ganglia. The neurones were stained individually by the intracellular injection of cobalt, and the ultrastructure of common inhibitor 1 (CI1) in the metathoracic ganglion was revealed by the intracellular injection of horseradish peroxidase. Homologous inhibitory motor neurones in the meso- and metathoracic ganglia have similar shapes. CI1 has axons in nerves 3, 4, and 5, but common inhibitors 2 and 3 (CI2, CI3) have only a single axon in nerve 5. They nevertheless all share many features in common. All have large (60 70 micron diameter) cell bodies in the ventral cortex near the midline, well separated from those of the excitatory leg motor neurones. Their primary neurites run dorsally and laterally and send many fine branches into the dorsal and lateral neuropile, and some fine branches medially. None enter the ventral neuropile. CI1 and CI2 have a small branch that arises close to the cell body and arborises on either side of the midline. When examined with the electron microscope, CI1 was not found to make any output synapses, even though some of its fine branches are varicose and end in bulbous swellings. These were seen to be packed with mitochondria but not vesicles. Input synapses tend to be grouped together on the secondary neurites and, more especially, on the finer branches and their spines. The majority of processes presynaptic to CI1 contain round agranular vesicles.

Animals↗

Organization of receptive fields of spiking local interneurons in the locust with inputs from hair afferents.

The receptive fields of spiking local interneurons in the locust were defined by making intracellular recordings from them while stimulating mechanoreceptors on the surface of a hindleg. All the interneurons tested have their cell bodies near the ventral midline, in the so-called "midline" group. Those described here receive inputs only from external mechanoreceptors; others receive inputs from internal proprioceptors alone or from receptors of both kinds. The receptors on the surface of a hindleg that contribute to the receptive field of an interneuron may be clustered together in a discrete area or be distributed in separate regions that provide either excitation or inhibition. An interneuron may have a receptive field that is wholly excitatory or one with both excitatory and inhibitory regions. Excitatory but not inhibitory effects are mediated by direct connections between afferents and interneurons. The longitudinal boundaries of most receptive fields occur along one of the major axes of the leg. For example, hairs on the anterior half of a leg can be excitatory, while hairs on the posterior half are inhibitory; or those on the dorsal half are excitatory, and those on the ventral half are inhibitory. The proximal-distal boundaries of a receptive field often correspond to the articulations between the segments of a leg, although they may also occur within a segment of a leg where there are no other obvious anatomical discontinuities. The receptive fields of these interneurons often overlap, and an individual afferent from a hair excites more than one interneuron. In this way a particular region on the surface of a hindleg may be mapped onto as many as 12 interneurons. The size of a receptive field is not correlated with its position along the proximal-distal axis of the leg, but the smallest fields occur on the distal tibia or span the femorotibial joint.

Animals↗

The processing of mechanosensory information by spiking local interneurons in the locust.

The responses and receptive fields of a group of spiking local interneurons in the metathoracic ganglion of the locust were defined by making intracellular recordings from them while moving joints of a hindleg and stimulating external mechanoreceptors. Some interneurons respond both to inputs from internal mechanoreceptors (proprioceptors) at particular joints and to inputs from an array of external mechanoreceptors. The effects of both types of receptor can be excitatory or inhibitory. Other interneurons respond to proprioceptive input alone. There is a spectrum of responses. At one extreme are interneurons that respond tonically, the frequency of their spikes being determined by the angle of a particular joint. At the other extreme are interneurons that respond phasically to imposed movements of a joint in any direction. Inbetween are interneurons that respond with either a rapidly or a more slowly adapting change in the frequency of their spikes to the displacement of a joint in only one direction. Each movement of a particular joint excites or inhibits several interneurons with a range of different response characteristics. An interneuron typically receives inputs from only one joint, though some are excited by both femoral and tibial receptors. The interneurons spike during active movements of a leg elicited by direct stimulation of individual motor neurons, and during movements elicited by tactile stimulation of other parts of the body.

Animals↗

Innervation patterns of inhibitory motor neurones in the thorax of the locust.

The innervation pattern of inhibitory motor neurones of the locust has been revealed by intracellular recording from their cell bodies in the meso- and metathoracic ganglion and simultaneous recording from muscle fibres in a middle, or in a hind leg. Three neurones in each ganglion, the common inhibitor (CI = CI1), the anterior inhibitor (AI = CI2), and the posterior inhibitor (PI = CI3) innervate several muscles in one leg and are thus common inhibitory neurones. Metathoracic CI innervates 13 muscles in one hind leg and mesothoracic CI innervates 12 muscles in one middle leg. The muscles are all in the proximal parts of the legs and move the coxa, the trochanter and the tibia. Metathoracic AI and PI innervate four muscles in the more distal parts of one hind leg that move the tibia, the tarsus and the unguis. None of these muscles is innervated by CI. Each inhibitor innervates muscles that have different and often antagonistic actions during movements of a leg. AI and PI receive many synaptic inputs in common and show similar patterns of spikes during imposed movements of a tibia. Tests fail, however, to reveal evidence for any electrical or synaptic coupling between them. A revised scheme of nomenclature for these inhibitory neurones is proposed.

Animals↗

The morphology of two groups of spiking local interneurons in the metathoracic ganglion of the locust.

Two bilaterally symmetrical groups of spiking local interneurons are described in a segmental ganglion of the locust. Interneurons in both groups are excited by specific sets of sensory receptors on one leg. The cell bodies of the anterior-lateral group lie amongst approximately 40 small cell bodies at the anterior of the ganglion, close to the lateral edge of an anterior connective. Interneurons in this group have primary neurites in Ventral Commissure I ( VCI ), and dorsoventral processes in the Oblique Tract, which divide the extensive neuropilar branches into distinct ventral and dorsal regions. Cell bodies of the midline group lie amongst a group of approximately 100 small cell bodies near the ventral midline. Interneurons in this group have primary neurites in Ventral Commissure II ( VCII ), and dorsoventral processes in the Perpendicular Tract, which divide the neuropilar branches into dorsal and ventral regions. The ventral branches of interneurons in both groups are numerous and of a uniform texture, whereas the dorsal branches are sparse and varicose. The ventral branches project to the same ventral areas of neuropil as the afferents from some hairs on a hind leg. The dorsal branches of a midline interneuron and the branches of a leg motor neuron that it affects project to the same dorsal area of neuropil. Some midline interneurons receive direct inputs from leg hair afferents and make direct connections with leg motor neurons.

Animals↗

The morphological diversity and receptive fields of spiking local interneurons in the locust metathoracic ganglion.

Twenty-one types of spiking local interneurons are described in a segmental ganglion of the locust. All have their cell bodies in a group at the ventral midline of the metathoracic ganglion. The interneurons are characterized by their shape as revealed by intracellular injection of dye, and by their physiology as revealed by intracellular recording. Each interneuron conforms to a basic plan, but the characteristic shape of each is derived from the elaboration of branches in some regions of the neuropil and by their absence in other regions. Some interneurons have ventral branches that extend over most of one-half of the metathoracic neuropil, whilst others have ventral branches restricted to a small region of neuropil. A few interneurons have dorsal branches that enter the first abdominal neuromere . Each type of interneuron is excited by a specific array of mechanoreceptors on the hind leg ipsilateral to its neuropilar branches. Some interneurons have a wide receptive field that encompasses most of the dorsal surfaces of the distal three parts of a leg, whilst others have a field limited to the spurs at the distal end of the tibia. The relationship between the shape of an interneuron and the size or orientation of its receptive field is discussed.

Afferent Pathways↗

The morphology, ultrastructure, and distribution of synapses on an intersegmental interneuron of the locust.

The structure and synaptic relationships of an intersegmental interneurone in the mesothoracic ganglion of the locust were studied by intracellular labelling for light and electron microscopy. Before labelling, the interneurone was characterized physiologically. It is depolarized and produces spikes when either of the two forewings are elevated, and by sensory inputs from the tarsi of the middle legs. The gross morphology of the interneurone is quite distinctive. Its cell body is on the ventral surface of the ganglion near the midline and its primary neurite lies in the T-tract. Its axon performs a characteristic lateral loop around the lateral dorsal tract before entering an anterior connective and ascending at least as far as the prothoracic ganglion. Within the mesothoracic ganglion, the interneurone gives rise to a profusion of branches. Ultrastructural examination and reconstruction of three regions of the interneurone from serial sections shows that input and output synapses are present in approximately equal numbers, and often are close to each other. There is no evidence for separate input and output regions. Output synapses are characterized by the presence of a presynaptic bar and a population of 500-2,000 round, electron-lucent vesicles. Most of the estimated 10(5)-10(6) synapses occur on the smaller diameter processes or on spines. The spines are of uniform diameter along their lengths, and are pre- or postsynaptic or both, but the postsynaptic spines are of smaller diameter than the others.

Animals↗

Spiking local interneurons as primary integrators of mechanosensory information in the locust.

A population of spiking local interneurons in the metathoracic ganglion of the locust is vigorously excited by particular sensory stimuli from the hindlegs and participates in local postural reflexes. We examined the inputs from singly innervated mechanoreceptors (hairs and campaniform sensilla) to these spiking local interneurons, to nonspiking local interneurons, and to motor neurons that are also elements of local reflex pathways. Recordings were made intracellularly from the interneurons and motor neurons and extracellularly from afferent fibers. The physiological evidence is consistent with the spiking local interneurons being excited by direct, chemically mediated synaptic inputs from the afferents. Each afferent spike is followed at a constant latency by an excitatory postsynaptic potential (EPSP) in a spiking local interneuron, even at instantaneous frequencies as high as 300 Hz. The estimated synaptic delay is 1.5 ms, similar to that measured at other presumed monosynaptic connections within the same ganglion. Cobalt stains of individual interneurons, and of the central projections of afferent fibers show that both branch within the same ventral region of neuropil. Afferents from several hairs and campaniform sensilla converge on an individual spiking local interneuron. One interneuron is shown to receive inputs from at least seven hairs and four campaniform sensilla, but these represent only a tiny fraction of the total number of such sensilla on a hindleg. Practical limitations to the number of sensilla that can be tested for each interneuron means that the degree of convergence is likely to be considerably underestimated. We found no evidence that nonspiking local interneurons or motor neurons receive direct inputs from the afferents tested. Neurons of both types are, however, affected by stimulation of individual hairs, and the resulting pattern of postsynaptic potentials (PSPs) is similar to the pattern of spikes evoked in the spiking local interneurons. We infer from the evidence presented here and elsewhere (10, 11) that the spiking local interneurons are involved in at least two types of pathways for local interactions: 1) sensory neuron-spiking local interneuron-motor neuron, and 2) sensory neuron-spiking local interneuron-nonspiking local interneuron-motor neuron. We conclude that the spiking local interneurons are major elements in the primary integration of inputs from external receptors on the hindlegs.

Animals↗

Spiking local interneurons mediate local reflexes.

A local spiking interneuron in the locust is excited by particular sensory stimulation of a hind leg and forms an inhibitory connection with one hind leg motor neuron. Its behavioral effect is to mediate a local postural reflex. This interneuron is one of a population of interneurons with similar morphology and physiology that participate in the same local circuits as the better known nonspiking local interneurons.

Animals↗

The ultrastructure of identified locust motor neurones and their synaptic relationships.

Motor neurones in the thoracic ganglia of the locust were impaled with microelectrodes and identified according to the muscle they innervated and their other physiological properties. They were then labeled by intracellular injection of horseradish peroxidase and processed for electron microscopy. The nature and distribution of synapses on each motor neurone was examined and, by the use of reconstruction from serial sections, their spatial relationships revealed. The metathoracic fast extensor tibiae and mesothoracic tergosternal flight motor neurones have both output and input synapses on their neuropilar branches. These synapses are involved in serial, reciprocal, and recurrent relationships showing that the structural equivalent of a physiological synapse may be complex. The metathoracic slow extensor tibiae and anterior fast flexor tibiae motor neurones apparently have only input synapses within the neuropile.

Animals↗