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Organization of Invertebrate Motor Systems

Donald Kennedy, William J. Davis

10.1002/cphy.cp010127

Source: Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons

Originally published: 1977

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Properties of Muscle
1.1 Anatomic Organization
1.2 Contraction Speed
1.3 Strength and Extent of Contraction
1.4 Thresholds for Excitation‐Contraction Coupling
1.5 Correlations with Innervation
1.6 Dependence of Tension on Recent History
2 Motor Neurons and the Motor Unit
2.1 Motor Neuron Morphology
2.2 Correlations Between Motor Neuron Morphology and Function
2.3 Neuromuscular Transmission
2.4 Excitation‐Contraction Coupling
2.5 Peripheral Motor Unit Organization
2.6 Matching of Central and Peripheral Properties
2.7 Ontogeny and Regeneration
3 Reflex Organization
3.1 Proprioceptive Reflexes
3.2 Exteroreceptive Reflexes
3.3 Righting Reflexes
3.4 Optomotor Reflexes
3.5 Control of Reflex Excitability
4 Central Organization of Motor Systems
4.1 Structure of Motor Programs
4.2 Storage of Motor Programs
4.3 Release of Motor Programs by Command Elements
4.4 Central Versus Peripheral Control of Motor Output
4.5 Development of Pattern‐Generating Networks
4.6 Complex Behavioral Phenomena
5 Conclusion
Figure 1. Figure 1.

Catch property of arthropod muscle. Membrane potential (upper trace in each record) and tension (lower trace) were recorded from a single barnacle muscle fiber during stepwise depolarizations. Following the second depolarization, the tension remains at a higher level, i.e., it depends on the immediate stimulus history. In B and C, 0.5‐ and 1.0‐s repolarizations are interpolated without influencing the catch.

From Wilson et al. 939
Figure 2. Figure 2.

Morphology of invertebrate motor neurons (B‐E, G, H), cobalt injection (C and D), or combined structural and functional techniques (E). A: lateral giant interneuron of crayfish. B: lobster swimmeret power‐stroke motor neuron. C: locust wing‐elevator motor neuron (no. 113). D: locust wing‐depressor motor neuron (no. 127). E: probably the common inhibitor neuron of the cockroach. F: giant interneuron in the sixth abdominal ganglion of the cockroach. G: leech motor neuron. H: the motor giant of the crayfish. A and B are seen in anterior view, while C‐H are seen from the dorsal aspect.

A, adapted from Selverston & Kennedy 781; B, adapted from Davis 189; C and D, adapted from Burrows 108; E, adapted from Crossman et al. 178; F, adapted from Harris & Smyth 347; G, adapted from Purvis & McMahan 724; H, adapted from Selverston & Kennedy 781
Figure 3. Figure 3.

Soma maps of motor neurons in a variety of invertebrate motor systems showing that antagonistic motor neuron somas tend to be intermingled. C and D are dorsal views, while the remainder are ventral views. A: buccal ganglion of Pleurobranchaea showing somas of motor neurons that withdraw and evert the proboscis as revealed by back injection of nerve roots with CoCl2 followed by physiological confirmation. B: metathoracic ganglion of the locust showing positions of somas of leg motor neurons on one side. C: segmental ganglion of the leech showing motor neurons supplying the body wall muscles. D: mesothoracic ganglion of the locust showing somas of flight motor neurons. E: abdominal ganglion of the lobster showing somas of swimmeret motor neurons. F: abdominal ganglion of the lobster showing somas of abdominal flexor and extensor muscles.

A, adapted from Siegler et al. 793; B, adapted from Burrows & Hoyle 113; C, adapted from Stuart 812; D, adapted from Bentley 55; E, adapted from Davis 190; F, adapted from Otsuka et al. 668
Figure 4. Figure 4.

Properties of a small (A), medium (B), and large (C) motor neuron innervating the main power‐stroke muscle of the lobster Homarus. (1), soma diameters; (2), axonal conduction velocities; (3), amplitudes of action potentials recorded with two extracellular electrodes at different positions on the motor nerve; (4), amplitudes of excitatory junctional potentials (EJP's) recorded from a single muscle fiber (upper trace in each record); (5), adaptation to a maintained intracellular depolarizing current; and (6), facilitation properties of extracellular EJP's (upper trace in each record) during 50‐Hz stimulation. Note antifacilitation of the EJP's produced by the largest motor neuron. Time marks in (5) (lowest trace), 1/10 ms.

From Davis 190
Figure 5. Figure 5.

Inhibitory and excitatory neuromuscular synapses on muscle fibers of the claw opener in a crustacean. A: inhibitory (I) and excitatory (E) axons, the latter forming a neuromuscular synapse (SY); calibration, 1 μm. B: axoaxonal synapse between the inhibitory axon (I) and an excitatory terminal (E); calibration, 0.45 μm. At this magnification, the more elliptical shape of the vesicles in the inhibitory element is clear.

From Sherman & Atwood 787
Figure 6. Figure 6.

Physiological features of crustacean neuromuscular junctions. A: responses from fast (A1) and slow (A2) divisions of the lateral flexor muscle of Squilla. In A1 the top trace is zero membrane potential, the second trace is tension, and the third trace is the membrane potential recorded intracellularly from a single muscle fiber. Vertical calibration, 30 mV; horizontal calibration, 200 ms. In A2 the top traces in each record show tension, and the bottom traces are the membrane potential of a single muscle fiber. The number above each record in A2 gives the stimulus frequency in Hz. Vertical calibration, 30 mV; horizontal calibration, 300 ms. B: range of facilitation properties shown by the terminals of a single motor neuron on different fibers in the claw‐stretcher muscle of the crab Hyas. Top record, a high Fe terminal; bottom record, low Fe terminal. Stimulus frequency in each case, 1 Hz, followed by 10 Hz, then 1 Hz. Vertical calibration, 15 mV; horizontal calibration, 750 ms. C: membrane responses that are intermediate between fast and slow in a claw‐stretcher muscle fiber of the crab Grapsus. Junctions that exhibit facilitation at 10 Hz produce spikes (electrically excitable responses) on adequate depolarization. Vertical calibration, 20 mV; horizontal calibration, 0.5 s. D: changes in membrane potential and conductance caused by stimulation of the peripheral inhibitor axon supplying the slow abdominal flexor of the lobster Homarus. Constant‐current hyperpolarizing pulses were injected into a single muscle fiber before (lower trace) and during (middle trace) stimulation of the inhibitor at 120 Hz. The inhibitory junctional potentials were depolarizing, and the conductance increased approximately fourfold during inhibition. Time marks (upper trace), 10 ms; vertical calibration, 10 mV.

A, from Burrows & Hoyle 112; B, from Sherwood & Atwood 787; C, from Atwood & Bittner 25; D, from Kennedy & Evoy 492
Figure 7. Figure 7.

Types of motor unit organization found in invertebrate muscles. For discussion see text.
Figure 8. Figure 8.

Peripheral arrangements and central reflex connections of stretch or tension receptors (Sr) and skeletal muscles. In each case the tension receptor excites activity in the motor neuron innervating the working muscle. A: parallel arrangement. The muscle responds to imposed load by shortening in the familiar resistance (myotatic) reflex; since the contraction unloads the receptor, the system is unresponsive to loads imposed during active movement. B: series arrangement. The muscle responds to imposed loads by shortening, which further excites the receptor during active contraction, but lacks an absolute length reference. C: stretch receptor in series with specialized receptor muscle, which is coactivated with the working muscle. This arrangement compensates for loads imposed during active contraction and also has an absolute length reference.
Figure 9. Figure 9.

Reflex organization in the swimmeret system of the lobster. ▴, Excitatory connections; ○, inhibitory connections. Sensory influences, proprioceptors, and setae are all activated during the power stroke. The proprioceptors excite all excitatory motor neurons; reciprocity between antagonistic muscles originates in the opposite influences of the setae. Both sensory sources reciprocally influence excitors and peripheral inhibitors to a given muscle.

From Davis 193
Figure 10. Figure 10.

Load‐compensating arrangement of muscle receptor organ (MRO) and extensor muscles in the crayfish abdomen. The shared motoneuron innervates parallel working and receptor muscles, and may be activated selectively by central command interneurons. The muscle receptor organ responds both to lengthening of the receptor muscle and to its contraction, and connects centrally with an identified motoneuron (no. 2) which innervates the working muscle exclusively. Thus loads opposing a commanded extension generate proportional excitation in the load compensating servo loop, which supplies additional tension to the working muscle to overcome the load.

From Kennedy 489. Originally published by the University of California Press; reprinted by permission of The Regents of the University of California
Figure 11. Figure 11.

Equilibrium reactions of the lobster Homarus in response to roll. A and B: compensatory responses of the anterior appendages and eyes, respectively. C–E: righting responses of the claws, swimmerets, and uropods, respectively. Heavy arrows in D show directions of water currents.

Adapted from Davis 191
Figure 12. Figure 12.

A model incorporating demonstrated neuronal components to explain various features of equilibrium reactions in the lobster Homarus. Arrowheads designate excitatory influences. The model explains how either the right or left statocyst can alone control the righting responses of the appendages of one side, even though the afferent responses of the two statocysts to roll in one direction are opposite.

Adapted from Davis 183
Figure 13. Figure 13.

Positive‐feedback optomotor responses in the lobster Homarus. A: treadmill apparatus used to study the responses. The lobster is clamped in place above the striped belt and separated from it by a transparent Plexiglas platform. Thus the animal can see the stripes but cannot feel the belt movements. B–D: limb movements and electromyograms (emg) during backward movement of the belt beneath the animal. B, typical response of a walking leg; C, rapidly diminishing response; D, responses of two motor systems, the legs, and swimmerets (continuous records). In all records the lowest trace shows the treadmill speed (above the horizontal line; 1 vertical mark per cm of belt movement) and time marks (below the line; 1/100 ms). Arrows in D show increments in treadmill velocity; note corresponding increments in locomotor activity.

From Davis & Ayers 194. Copyright 1972 by the American Association for the Advancement of Science
Figure 14. Figure 14.

Summary of types of optomotor responses (left column) and hypothetical neuronal circuitry that can account for the corresponding responses (right column). A: the relatively simple case of forward locomotion only (e.g., flight in some insects). B: the more complex case of bidirectional locomotion (e.g., walking in lobsters). The models consist of lateral and medial motion detectors in the eyes and command centers for forward flight (A) or forward and backward walking (B). Turning is presumed to result from differential power output on the two sides (A) or oppositely directed locomotion on the two sides (B).
Figure 15. Figure 15.

Neural circuits controlling gill movements in Aplysia. Arrowheads represent excitatory synapses, while circles represent inhibitory synapses. A: centrally commanded movements. Int II probably represents several closely coupled interneurons. B: reflex gill‐withdrawal movements. The sensory input from the siphon (Sensory N) is direct (monosynaptic excitation) or mediated by interneuronal excitation and inhibition.

Adapted from Kandel 521. Copyright 1969 by the American Association for the Advancement of Science
Figure 16. Figure 16.

Examples of the major classes of motor programs. A: noncyclic. B: noncyclic, phasic program. C and D; cyclic programs. In A, recordings were made from the segmental superficial flexor nerve of the abdomen in an intact crayfish after removal of leg support (halfway through the upper record). This stimulus causes cessation of activity in flexor excitors 1–4, 6, and activation of the inhibitor 5. Continuous records. Time mark, 1 s. In B, electromyograms were recorded from the raptorial leg of Squilla during the rapid strike. From top to bottom, traces represent lateral flexor activity (ceases at the open arrow), lateral extensor activity, and limb movement (the strike occurs at the closed arrow). C, intracellular recordings from different pairs of somas of neurons involved in the pyloric cycle of the lobster stomatogastric rhythm. D, summary of the lobster stomatogastric rhythm. Upper graph, the pyloric cycle. Lower graph, the gastric cycle.

A, from Larimer & Eggleston 534; B, from Burrows 105; C, from Maynard 582; D, upper graph, adapted from Maynard 582; D, lower graph, adapted from Mulloney & Selverston 635
Figure 17. Figure 17.

Terminology for motor programs. L, latency; P, period. In H, cyclic output is shown at low‐output (left) and high‐output (right) frequencies, with amplitude inversely related to period. See text for further explanation.
Figure 18. Figure 18.

Known neural mechanisms for generating synergism (A) and antagonism (B) in motor systems. Synergism can result from excitatory (▵) coupling between motor neurons [A 1] or from common excitatory inputs to synergic motor neurons [A (2)]. Antagonism can result from reciprocal or unidirectional inhibitory (○) coupling between motor neurons supplying antagonistic muscles [B (1)]; from fixed delays in excitatory couplings between antagonistic motor neurons [B (2)]; or from opposite synaptic inputs from the same presynaptic source. Flex, flexor; ext, extensor. See text for further description.

B (3
Figure 19. Figure 19.

Summary of the neuronal circuitry in the abdominal ganglion controlling the heart and blood pressure of Aplysia. ▵, Excitatory connections; ○, inhibitory ones. The main features of interest are: 1) reciprocal inhibition between two command interneurons in the network (Int. II and the double‐action L10); and 2) lack of interactions at the level of motor neurons, e.g., (LDm).

Adapted from Koester et al. 503
Figure 20. Figure 20.

Demonstrated circuits of neurons that participate in the stomatogastric rhythm of the lobster. A: the pyloric rhythm (cf. Fig. 16D). B: the gastric rhythm (cf. Fig. 16D). The main features illustrated are electrical couplings between synergists (capacitance symbols in A, resistance symbols in B) and in some cases between antagonists (B), and chemical inhibition between antagonists (○ in A, • in B) and in some cases between synergists (A and B).

A, from Maynard 582; B, from Mulloney & Selverston 635
Figure 21. Figure 21.

Identified neuronal circuitry involving two locust flight neurons, namely 113 (a wing elevator) and 127 (a wing depressor). Rectangles represent delays at unknown numbers of synapses. Arrowheads represent excitatory connections, while circles represent inhibitory ones. The main features shown are: 1) delayed excitation between ipsilateral antagonists, and 2) delayed excitation between contralateral synergists, 3) descending excitation of the wing depressor, and 4) descending excitation and inhibition of the wing elevator. The structure of motor neurons 113 and 127 is shown in Figure 2

Adapted from Burrows 107
Figure 22. Figure 22.

Known and hypothetical neural mechanisms for generating rhythmic alternating motor output to antagonistic muscles; flex, flexor; ext, extensor. Arrows indicate excitatory connections; circles represent inhibitory ones. A: oscillation as a property of a single neuron; B: coupled oscillator neurons; C: oscillation as a network property; C (1): a reciprocal inhibitory network; C (2), a neuropilar network in which propagated changes in potential represent the oscillation. As noted in the text, the class of models exemplified in A and B will work only if the extensor motor neurons have a continuous endogenous or exogenous source of excitation.
Figure 23. Figure 23.

Oscillator neuron(s) in the lobster ventilatory system. A: intracellular recording from an oscillator neuron in the subesophageal ganglion while recording associated, spontaneous motor output extracellularly (lower two traces). B: imposed depolarization of the oscillator neuron inhibits activity of one group of motor neurons and excites antagonists. C: imposed hyperpolarization has the opposite effects. Vertical calibration for intracellular records, 34 mV; horizontal calibration, 310 ms.

From Mendelson 598. Copyright 1971 by the American Association for the Advancement of Science
Figure 24. Figure 24.

Central organization underlying swimming in Tritonia. Arrowheads represent chemical excitatory connections; circles, inhibitory connections and capacitance symbols, electrical connections. TGN, trigger neurons; GEN, general excitor neurons; DFN, dorsal flexor neurons; VFN, ventral flexor neurons; TeN, hypothetical terminator neurons. Sensory input is filtered through the network of trigger neurons and thence to dorsal flexion neurons. These activate general excitors, which presumably function to maintain excitation within the network even after the sensory stimulus ends. Terminator neurons are proposed to account for the apparently active termination of bursts.

Adapted from Willows et al. 921
Figure 25. Figure 25.

Schematization of a hypothetical model to account for rhythmic motor output. The sine waves (a–c) represent excitatory input to motor neurons having different thresholds (1–3). The chief features of the model are: 1) the excitation is sinusoidal; 2) the amplitude of the excitation is inversely related to period; and 3) the details of motor activity are determined by differences in motor neuron threshold that are related to motor neuron size.

From Davis 190
Figure 26. Figure 26.

Properties of a swimmeret command interneuron in the lobster Homarus. A: electrical stimulation of the interneuron causes rhythmic, alternating discharge to antagonistic swimmeret muscles. RS, return stroke; PS, power stroke. B: tactile stimulation of the ventral abdomen causes the interneuron (INT) to discharge and also elicits rhythmic swimmeret output. The third and fourth traces are a stimulus monitor and a time base (100 marks/s).

From Davis & Kennedy 196
Figure 27. Figure 27.

Behavioral effects of stimulating command interneurons in the circumeosophageal connectives of the crayfish, based on tracings from single frames of motion pictures. A: posture before (left) and after (right) stimulation of a command fiber for abdominal extension. B: same for claw elevation. C and D: position in one connective of fibers for forward and backward walking, respectively. E: the defense posture, as seen at different times following initiation of command fiber stimulation at 20/s at t + 0 s.

Adapted from Bowerman & Larimer 79,80
Figure 28. Figure 28.

Preeclosion behavior of the silk moth. Upper record, abdominal movements recorded on a kymograph drum. The activity is divided into three characteristic periods, namely: (1) the first hyperactive period; (2) the quiescent period; and (3) the second hyperactive period. Arrow marks the movement of adult emergence. Lower record, integrated electrical activity from an abdominal nerve of a deafferented nerve cord following application of eclosion hormone 40 min before the first burst. Note general similarity to the normal records in the upper record. Calibration refers to lower record.

From Truman & Sokolove 854. Copyright 1972 by the American Association for the Advancement of Science
Figure 29. Figure 29.

The behavioral hierarchy of the mollusc Pleurobranchaea. Unidirectional arrows from one behavioral act to another indicate that the former takes precedence over the latter. Bidirectional arrows indicate mutual compatibility (i.e., the two behavioral acts can occur together). The escape response takes precedence over all other behavioral acts. See text for further description.

From Davis et al. 202


Figure 1.

Catch property of arthropod muscle. Membrane potential (upper trace in each record) and tension (lower trace) were recorded from a single barnacle muscle fiber during stepwise depolarizations. Following the second depolarization, the tension remains at a higher level, i.e., it depends on the immediate stimulus history. In B and C, 0.5‐ and 1.0‐s repolarizations are interpolated without influencing the catch.

From Wilson et al. 939


Figure 2.

Morphology of invertebrate motor neurons (B‐E, G, H), cobalt injection (C and D), or combined structural and functional techniques (E). A: lateral giant interneuron of crayfish. B: lobster swimmeret power‐stroke motor neuron. C: locust wing‐elevator motor neuron (no. 113). D: locust wing‐depressor motor neuron (no. 127). E: probably the common inhibitor neuron of the cockroach. F: giant interneuron in the sixth abdominal ganglion of the cockroach. G: leech motor neuron. H: the motor giant of the crayfish. A and B are seen in anterior view, while C‐H are seen from the dorsal aspect.

A, adapted from Selverston & Kennedy 781; B, adapted from Davis 189; C and D, adapted from Burrows 108; E, adapted from Crossman et al. 178; F, adapted from Harris & Smyth 347; G, adapted from Purvis & McMahan 724; H, adapted from Selverston & Kennedy 781


Figure 3.

Soma maps of motor neurons in a variety of invertebrate motor systems showing that antagonistic motor neuron somas tend to be intermingled. C and D are dorsal views, while the remainder are ventral views. A: buccal ganglion of Pleurobranchaea showing somas of motor neurons that withdraw and evert the proboscis as revealed by back injection of nerve roots with CoCl2 followed by physiological confirmation. B: metathoracic ganglion of the locust showing positions of somas of leg motor neurons on one side. C: segmental ganglion of the leech showing motor neurons supplying the body wall muscles. D: mesothoracic ganglion of the locust showing somas of flight motor neurons. E: abdominal ganglion of the lobster showing somas of swimmeret motor neurons. F: abdominal ganglion of the lobster showing somas of abdominal flexor and extensor muscles.

A, adapted from Siegler et al. 793; B, adapted from Burrows & Hoyle 113; C, adapted from Stuart 812; D, adapted from Bentley 55; E, adapted from Davis 190; F, adapted from Otsuka et al. 668


Figure 4.

Properties of a small (A), medium (B), and large (C) motor neuron innervating the main power‐stroke muscle of the lobster Homarus. (1), soma diameters; (2), axonal conduction velocities; (3), amplitudes of action potentials recorded with two extracellular electrodes at different positions on the motor nerve; (4), amplitudes of excitatory junctional potentials (EJP's) recorded from a single muscle fiber (upper trace in each record); (5), adaptation to a maintained intracellular depolarizing current; and (6), facilitation properties of extracellular EJP's (upper trace in each record) during 50‐Hz stimulation. Note antifacilitation of the EJP's produced by the largest motor neuron. Time marks in (5) (lowest trace), 1/10 ms.

From Davis 190


Figure 5.

Inhibitory and excitatory neuromuscular synapses on muscle fibers of the claw opener in a crustacean. A: inhibitory (I) and excitatory (E) axons, the latter forming a neuromuscular synapse (SY); calibration, 1 μm. B: axoaxonal synapse between the inhibitory axon (I) and an excitatory terminal (E); calibration, 0.45 μm. At this magnification, the more elliptical shape of the vesicles in the inhibitory element is clear.

From Sherman & Atwood 787


Figure 6.

Physiological features of crustacean neuromuscular junctions. A: responses from fast (A1) and slow (A2) divisions of the lateral flexor muscle of Squilla. In A1 the top trace is zero membrane potential, the second trace is tension, and the third trace is the membrane potential recorded intracellularly from a single muscle fiber. Vertical calibration, 30 mV; horizontal calibration, 200 ms. In A2 the top traces in each record show tension, and the bottom traces are the membrane potential of a single muscle fiber. The number above each record in A2 gives the stimulus frequency in Hz. Vertical calibration, 30 mV; horizontal calibration, 300 ms. B: range of facilitation properties shown by the terminals of a single motor neuron on different fibers in the claw‐stretcher muscle of the crab Hyas. Top record, a high Fe terminal; bottom record, low Fe terminal. Stimulus frequency in each case, 1 Hz, followed by 10 Hz, then 1 Hz. Vertical calibration, 15 mV; horizontal calibration, 750 ms. C: membrane responses that are intermediate between fast and slow in a claw‐stretcher muscle fiber of the crab Grapsus. Junctions that exhibit facilitation at 10 Hz produce spikes (electrically excitable responses) on adequate depolarization. Vertical calibration, 20 mV; horizontal calibration, 0.5 s. D: changes in membrane potential and conductance caused by stimulation of the peripheral inhibitor axon supplying the slow abdominal flexor of the lobster Homarus. Constant‐current hyperpolarizing pulses were injected into a single muscle fiber before (lower trace) and during (middle trace) stimulation of the inhibitor at 120 Hz. The inhibitory junctional potentials were depolarizing, and the conductance increased approximately fourfold during inhibition. Time marks (upper trace), 10 ms; vertical calibration, 10 mV.

A, from Burrows & Hoyle 112; B, from Sherwood & Atwood 787; C, from Atwood & Bittner 25; D, from Kennedy & Evoy 492


Figure 7.

Types of motor unit organization found in invertebrate muscles. For discussion see text.



Figure 8.

Peripheral arrangements and central reflex connections of stretch or tension receptors (Sr) and skeletal muscles. In each case the tension receptor excites activity in the motor neuron innervating the working muscle. A: parallel arrangement. The muscle responds to imposed load by shortening in the familiar resistance (myotatic) reflex; since the contraction unloads the receptor, the system is unresponsive to loads imposed during active movement. B: series arrangement. The muscle responds to imposed loads by shortening, which further excites the receptor during active contraction, but lacks an absolute length reference. C: stretch receptor in series with specialized receptor muscle, which is coactivated with the working muscle. This arrangement compensates for loads imposed during active contraction and also has an absolute length reference.



Figure 9.

Reflex organization in the swimmeret system of the lobster. ▴, Excitatory connections; ○, inhibitory connections. Sensory influences, proprioceptors, and setae are all activated during the power stroke. The proprioceptors excite all excitatory motor neurons; reciprocity between antagonistic muscles originates in the opposite influences of the setae. Both sensory sources reciprocally influence excitors and peripheral inhibitors to a given muscle.

From Davis 193


Figure 10.

Load‐compensating arrangement of muscle receptor organ (MRO) and extensor muscles in the crayfish abdomen. The shared motoneuron innervates parallel working and receptor muscles, and may be activated selectively by central command interneurons. The muscle receptor organ responds both to lengthening of the receptor muscle and to its contraction, and connects centrally with an identified motoneuron (no. 2) which innervates the working muscle exclusively. Thus loads opposing a commanded extension generate proportional excitation in the load compensating servo loop, which supplies additional tension to the working muscle to overcome the load.

From Kennedy 489. Originally published by the University of California Press; reprinted by permission of The Regents of the University of California


Figure 11.

Equilibrium reactions of the lobster Homarus in response to roll. A and B: compensatory responses of the anterior appendages and eyes, respectively. C–E: righting responses of the claws, swimmerets, and uropods, respectively. Heavy arrows in D show directions of water currents.

Adapted from Davis 191


Figure 12.

A model incorporating demonstrated neuronal components to explain various features of equilibrium reactions in the lobster Homarus. Arrowheads designate excitatory influences. The model explains how either the right or left statocyst can alone control the righting responses of the appendages of one side, even though the afferent responses of the two statocysts to roll in one direction are opposite.

Adapted from Davis 183


Figure 13.

Positive‐feedback optomotor responses in the lobster Homarus. A: treadmill apparatus used to study the responses. The lobster is clamped in place above the striped belt and separated from it by a transparent Plexiglas platform. Thus the animal can see the stripes but cannot feel the belt movements. B–D: limb movements and electromyograms (emg) during backward movement of the belt beneath the animal. B, typical response of a walking leg; C, rapidly diminishing response; D, responses of two motor systems, the legs, and swimmerets (continuous records). In all records the lowest trace shows the treadmill speed (above the horizontal line; 1 vertical mark per cm of belt movement) and time marks (below the line; 1/100 ms). Arrows in D show increments in treadmill velocity; note corresponding increments in locomotor activity.

From Davis & Ayers 194. Copyright 1972 by the American Association for the Advancement of Science


Figure 14.

Summary of types of optomotor responses (left column) and hypothetical neuronal circuitry that can account for the corresponding responses (right column). A: the relatively simple case of forward locomotion only (e.g., flight in some insects). B: the more complex case of bidirectional locomotion (e.g., walking in lobsters). The models consist of lateral and medial motion detectors in the eyes and command centers for forward flight (A) or forward and backward walking (B). Turning is presumed to result from differential power output on the two sides (A) or oppositely directed locomotion on the two sides (B).



Figure 15.

Neural circuits controlling gill movements in Aplysia. Arrowheads represent excitatory synapses, while circles represent inhibitory synapses. A: centrally commanded movements. Int II probably represents several closely coupled interneurons. B: reflex gill‐withdrawal movements. The sensory input from the siphon (Sensory N) is direct (monosynaptic excitation) or mediated by interneuronal excitation and inhibition.

Adapted from Kandel 521. Copyright 1969 by the American Association for the Advancement of Science


Figure 16.

Examples of the major classes of motor programs. A: noncyclic. B: noncyclic, phasic program. C and D; cyclic programs. In A, recordings were made from the segmental superficial flexor nerve of the abdomen in an intact crayfish after removal of leg support (halfway through the upper record). This stimulus causes cessation of activity in flexor excitors 1–4, 6, and activation of the inhibitor 5. Continuous records. Time mark, 1 s. In B, electromyograms were recorded from the raptorial leg of Squilla during the rapid strike. From top to bottom, traces represent lateral flexor activity (ceases at the open arrow), lateral extensor activity, and limb movement (the strike occurs at the closed arrow). C, intracellular recordings from different pairs of somas of neurons involved in the pyloric cycle of the lobster stomatogastric rhythm. D, summary of the lobster stomatogastric rhythm. Upper graph, the pyloric cycle. Lower graph, the gastric cycle.

A, from Larimer & Eggleston 534; B, from Burrows 105; C, from Maynard 582; D, upper graph, adapted from Maynard 582; D, lower graph, adapted from Mulloney & Selverston 635


Figure 17.

Terminology for motor programs. L, latency; P, period. In H, cyclic output is shown at low‐output (left) and high‐output (right) frequencies, with amplitude inversely related to period. See text for further explanation.



Figure 18.

Known neural mechanisms for generating synergism (A) and antagonism (B) in motor systems. Synergism can result from excitatory (▵) coupling between motor neurons [A 1] or from common excitatory inputs to synergic motor neurons [A (2)]. Antagonism can result from reciprocal or unidirectional inhibitory (○) coupling between motor neurons supplying antagonistic muscles [B (1)]; from fixed delays in excitatory couplings between antagonistic motor neurons [B (2)]; or from opposite synaptic inputs from the same presynaptic source. Flex, flexor; ext, extensor. See text for further description.

B (3


Figure 19.

Summary of the neuronal circuitry in the abdominal ganglion controlling the heart and blood pressure of Aplysia. ▵, Excitatory connections; ○, inhibitory ones. The main features of interest are: 1) reciprocal inhibition between two command interneurons in the network (Int. II and the double‐action L10); and 2) lack of interactions at the level of motor neurons, e.g., (LDm).

Adapted from Koester et al. 503


Figure 20.

Demonstrated circuits of neurons that participate in the stomatogastric rhythm of the lobster. A: the pyloric rhythm (cf. Fig. 16D). B: the gastric rhythm (cf. Fig. 16D). The main features illustrated are electrical couplings between synergists (capacitance symbols in A, resistance symbols in B) and in some cases between antagonists (B), and chemical inhibition between antagonists (○ in A, • in B) and in some cases between synergists (A and B).

A, from Maynard 582; B, from Mulloney & Selverston 635


Figure 21.

Identified neuronal circuitry involving two locust flight neurons, namely 113 (a wing elevator) and 127 (a wing depressor). Rectangles represent delays at unknown numbers of synapses. Arrowheads represent excitatory connections, while circles represent inhibitory ones. The main features shown are: 1) delayed excitation between ipsilateral antagonists, and 2) delayed excitation between contralateral synergists, 3) descending excitation of the wing depressor, and 4) descending excitation and inhibition of the wing elevator. The structure of motor neurons 113 and 127 is shown in Figure 2

Adapted from Burrows 107


Figure 22.

Known and hypothetical neural mechanisms for generating rhythmic alternating motor output to antagonistic muscles; flex, flexor; ext, extensor. Arrows indicate excitatory connections; circles represent inhibitory ones. A: oscillation as a property of a single neuron; B: coupled oscillator neurons; C: oscillation as a network property; C (1): a reciprocal inhibitory network; C (2), a neuropilar network in which propagated changes in potential represent the oscillation. As noted in the text, the class of models exemplified in A and B will work only if the extensor motor neurons have a continuous endogenous or exogenous source of excitation.



Figure 23.

Oscillator neuron(s) in the lobster ventilatory system. A: intracellular recording from an oscillator neuron in the subesophageal ganglion while recording associated, spontaneous motor output extracellularly (lower two traces). B: imposed depolarization of the oscillator neuron inhibits activity of one group of motor neurons and excites antagonists. C: imposed hyperpolarization has the opposite effects. Vertical calibration for intracellular records, 34 mV; horizontal calibration, 310 ms.

From Mendelson 598. Copyright 1971 by the American Association for the Advancement of Science


Figure 24.

Central organization underlying swimming in Tritonia. Arrowheads represent chemical excitatory connections; circles, inhibitory connections and capacitance symbols, electrical connections. TGN, trigger neurons; GEN, general excitor neurons; DFN, dorsal flexor neurons; VFN, ventral flexor neurons; TeN, hypothetical terminator neurons. Sensory input is filtered through the network of trigger neurons and thence to dorsal flexion neurons. These activate general excitors, which presumably function to maintain excitation within the network even after the sensory stimulus ends. Terminator neurons are proposed to account for the apparently active termination of bursts.

Adapted from Willows et al. 921


Figure 25.

Schematization of a hypothetical model to account for rhythmic motor output. The sine waves (a–c) represent excitatory input to motor neurons having different thresholds (1–3). The chief features of the model are: 1) the excitation is sinusoidal; 2) the amplitude of the excitation is inversely related to period; and 3) the details of motor activity are determined by differences in motor neuron threshold that are related to motor neuron size.

From Davis 190


Figure 26.

Properties of a swimmeret command interneuron in the lobster Homarus. A: electrical stimulation of the interneuron causes rhythmic, alternating discharge to antagonistic swimmeret muscles. RS, return stroke; PS, power stroke. B: tactile stimulation of the ventral abdomen causes the interneuron (INT) to discharge and also elicits rhythmic swimmeret output. The third and fourth traces are a stimulus monitor and a time base (100 marks/s).

From Davis & Kennedy 196


Figure 27.

Behavioral effects of stimulating command interneurons in the circumeosophageal connectives of the crayfish, based on tracings from single frames of motion pictures. A: posture before (left) and after (right) stimulation of a command fiber for abdominal extension. B: same for claw elevation. C and D: position in one connective of fibers for forward and backward walking, respectively. E: the defense posture, as seen at different times following initiation of command fiber stimulation at 20/s at t + 0 s.

Adapted from Bowerman & Larimer 79,80


Figure 28.

Preeclosion behavior of the silk moth. Upper record, abdominal movements recorded on a kymograph drum. The activity is divided into three characteristic periods, namely: (1) the first hyperactive period; (2) the quiescent period; and (3) the second hyperactive period. Arrow marks the movement of adult emergence. Lower record, integrated electrical activity from an abdominal nerve of a deafferented nerve cord following application of eclosion hormone 40 min before the first burst. Note general similarity to the normal records in the upper record. Calibration refers to lower record.

From Truman & Sokolove 854. Copyright 1972 by the American Association for the Advancement of Science


Figure 29.

The behavioral hierarchy of the mollusc Pleurobranchaea. Unidirectional arrows from one behavioral act to another indicate that the former takes precedence over the latter. Bidirectional arrows indicate mutual compatibility (i.e., the two behavioral acts can occur together). The escape response takes precedence over all other behavioral acts. See text for further description.

From Davis et al. 202
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Article Title: Organization of Invertebrate Motor Systems
 

How to Cite

Donald Kennedy, William J. Davis. Organization of Invertebrate Motor Systems. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 1023-1087. First published in print 1977. doi: 10.1002/cphy.cp010127