Comprehensive Physiology Wiley Online Library

Invertebrate Nervous Systems

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Abstract

The sections in this article are:

1 Overview of Invertebrate Systems
1.1 Plants and Unicellular Microbes
1.2 Parazoa: Sponges
1.3 Diploblastic Metazoa: Anemones, Jellyfish, and Comb Jellies
1.4 The First Brains: Flatworms, Flukes, and Tapeworms (Platyhelminthes)
1.5 Nemertines, Pseudocoelomates, and Others
1.6 Nematodes
1.7 Annelids, Arthropods, and Molluscs
1.8 Echinoderms
1.9 Chaetognaths
1.10 Invertebrate Chordates
2 Principle‐Oriented Vignettes
2.1 Voltage‐Gated Ion Channels and Membrane Biophysics
2.2 Synaptic Transmission and Neurosecretion
2.3 Selected Neuronal Circuits
2.4 Long‐Term Plasticity of Invertebrate Neuronal Circuits
2.5 Sensory Representation and Processing
2.6 Olfaction
2.7 Vision
2.8 Mechanosensation
Figure 1. Figure 1.

Excitability in plants and unicellular microbes. A: Action potentials elicited by touch in touch‐sensitive plants, Mimosa pudica (upper) and Venus's‐flytrap, Dionaea muscipula (lower) (after ). B: Responses to mechanical stimulation of anterior and posterior ends of the ciliated protozoan Paramecium caudatum. Stimulation to the anterior end produces graded depolarization and a reversal of ciliary beat that results in a change in the direction of swimming. Stimulation of the posterior end causes transient hyperpolarization that results in an acceleration of the rate of ciliary beating and faster forward swimming (from ). C: Single‐channel patch clamp recordings of Ba2+ currents in outside out patches of sugar beets (Beta vulgaris) tonoplast membranes. Patches were continuously polarized to the values shown on the left. Channel openings and closings were observed at membrane potentials more negative than 0 mV. The presence of more than one channel in the patch was indicated by multiple opening events (from ). D: Activities of two types of ion channel reconstituted into liposomes from the bacterium Escherichia coli. The open probability of a mechanosensitive channel (upper) was increased by applying increasing suction pressures via the recording pipette. Pipette voltage was +40 mV. Voltage‐dependent channels (lower) were identified in a membrane patch held at −50 mV. Open and maximally closed levels (corresponding to the closure of seven conductance units) are indicated on the left.

from
Figure 2. Figure 2.

Regenerative depolarizing and hyperpolarizing action in the dinoflagellate Noctiluca in response to injection of current into the flotation vacuole in Ca2+ ‐deprived artificial seawater. Upper traces, membrane potential; lower traces, injected current. A, D: Current injected when membrane was more or less hyperpolarized after negative spike. B, C: Current injected when membrane was more or less depolarized after positive spike. A, B: Outward current. C, D: Inward current.

from
Figure 3. Figure 3.

Hypostomal nerve net and ring of Hydra oligactis. Whole‐mount of a head stained with an antiserum against RFamide, demonstrating the presence of a nerve ring in the hypostome. a: Side view of the head shows the hypostome and the basal parts of several tentacles. Tentacles emerge from the tentacle zone below the hypostome. The dark spot in the midst of the stained cells well above the ring is the mouth region, which is the apex of the hypostome. b: View from above the hypostome shows the dark mouth region in the center surrounded by a large number of epidermal sensory cells. Arrow shows a typical ganglion cell outside the nerve ring. Bars indicate 200 μm (a) and 100 μm (b).

From
Figure 4. Figure 4.

Bidirectional excitatory chemical synapse between elements of the motor nerve net in the jellyfish Cyanea capillata. All records from the same cell pair with stimuli being applied to the cell on the upper trace. A: Approximately 1 ms after the peak of the action potential in the postsynaptic cell (lower trace), a distinct notch (arrow) appears on the action potential in the presynaptic cell (upper trace). This notch is absent when only an excitatory postsynaptic potential (EPSP) appears in the postsynaptic cell (B). When a delayed spike was evoked from the postsynaptic cell, a clear EPSP (arrow) was evoked from the presynaptic cell (C).

Modified from
Figure 5. Figure 5.

Two sizes of action potential produced during swimming by the motor giant axon of the jellyfish Aglantha digitale. A: Scale drawing from a photograph of A. digitale, apex at the top. B: Schematic of the layout of ring giant, motor giant axons, and myoepithelium in the circumumbrellar margin of the body wall. C: Regenerative impulses recorded from isolated motor giant axon shortened to 700 μm. Axon penetrated with two micropipettes to inject current and record membrane voltage. Traces superimposed to show overshooting action potential and low‐threshold spike elicited by successive depolarizing current pulses. Current reduced by ∼0.1 nA between pulses; action potential elicited by higher current. Axon resting potential, −67 mV.

A: from ; B: modified from ; C: modified from
Figure 6. Figure 6.

A: Spontaneous plateau potentials recorded in the cell body of an AVF‐like interneuron in Ascaris suum. Arrow marks an inflection from a depolarizing ramp to a plateau potential. B: Injection of hyperpolarizing current of sufficient magnitude suppresses the production of plateau potentials. C: Brief depolarizations superimposed upon the sustained hyperpolarization activate plateaus at a discrete threshold. D: Brief (100 ms) pulse of depolarizing current resets the rhythm of spontaneous plateaus. I, current monitor trace.

From
Figure 7. Figure 7.

Schematic showing synaptic connections among the motoneurons and large interneurons in the segmentally repeating arrays of Ascaris suum. The synaptic connectivities of all three types of dorsal excitatory motoneuron are similar, so they have been combined (DE), as have the putative ventral excitors (VE). Excitatory synapses are represented by open triangles and inhibitory synapses by filled triangles. No direct recording has been made from VE motoneurons, so the signs of the synapses they make and receive are predictions based on their anatomical similarities to DE motoneurons. Dorsal inhibitory motoneuron, DI; ventral inhibitory motoneuron, VI.

From
Figure 8. Figure 8.

Lack of A‐current in shaker mutant muscle fibers. Voltage clamp recordings from larval muscle fibers of Drosophila. Note that the initial fast outward current in the normal, wild‐type fiber is absent in the fiber from a shaker mutant (Shks133).

Adapted from
Figure 9. Figure 9.

Plasticity at the crayfish neuromuscular junction. A: Time course of long‐term facilitation (LTF) shows a pretest period during which evoked excitatory postsynaptic potentials (EPSPs) are measured during 5 Hz stimulation once every 10 min, a tetanic phase during which induction of LTF takes place, and a long‐lasting phase of LTF. B: Demonstration of LTF produced by local depolarizing pulses applied to the axon terminal by intracellular stimulation. Depolarizing pulses of 60 nA were applied (presynaptic) and the resulting EPSPs recorded in a muscle cell (postsynaptic). Arrows indicate current pulse artifacts. Stimulation of the terminal at 20 Hz for 10 min. in the presence of normal Ca2+ produced a large enhancement of the evoked EPSPs without alteration of the presynaptic response during the tetanus, and a long‐lasting phase (LLP) at 60 min following the tetanus.

From
Figure 10. Figure 10.

Reciprocal control of motor neurons by a local nonspiking interneuron in a locust. Two motor neurons, the fast extensor (Ext. mn) and a fast flexor (Flex, mn) of the tibia, were recorded intracellularly, along with a nonspiking interneuron (int). A: A pulse of current injected into a neuropilar process of the interneuron evokes a sustained depolarization of the extensor and a sustained hyperpolarization of the flexor motor neuron. B–D: With more current, there is a progressive and graded increase in the amplitude of the voltage changes in the motor neurons. E: Relationship between current injected into the interneuron and the resulting voltage changes in the two motor neurons. F: Two groups of multiple sweeps at the start of a pulse of current reveal that voltage changes of opposite polarity begin at the same time in the two motor neurons. Calibration: vertical interneuron, 40 mV; fast extensor motor neuron, 4 mV; flexor, 8 mV; current, 30 nA; horizontal (A–D). 400 ms, (F) 64 ms.

From
Figure 11. Figure 11.

Stomatogastric ganglion activity pattern and circuit diagram. A: Diagram of stomatogastric ganglion preparation as it looks when pinned out in a sylgard‐lined chamber. Peripheral nerves (mvn, pdn, Ipn, pyn) contain the axons of motor neurons that innervate muscles of the pyloris and gastric mill. Two commissural ganglia (CG), esophageal ganglion (OG), and stomatogastric ganglion (STG) are shown, along with stomatogastric nerve (stn). Asterisk indicates the position where sucrose blocks are applied to remove descending influences on the STG. B: Burst pattern of the pyloric network. These extracellular recordings were obtained from preparations as shown in A. C: Synaptic connectivity circuit diagram of the pyloric network. Inhibitory chemical synapses are indicated by black dots and electrotonic synapses by resistor symbols. Dashed lines indicate weak synapses, solid lines strong synapses.

From
Figure 12. Figure 12.

Stomatogastric ganglion neurons involved in the pyloric rhythm are conditional oscillators. A: Simultaneous intracellular recordings from four pyloric neurons in an intact network. B: Same neuron types after synaptic isolation from other pyloric neurons with pharmacological and cell killing techniques. Intact input from other ganglia via the stomatogastric nerve. C: Same neurons no longer oscillate when axons within the stomatogastric nerve are blocked.

From
Figure 13. Figure 13.

Effects of different modulators on synaptically isolated pyloric neurons. Bath‐applied dopamine, octopamine, or serotonin produces very different effects on different neurons. (From .) AB, Anterior bouton; PD, pyloric dilator,; VD, ventricular dilator; LP, lateral pyloric; PY, pyloric; IC, inferior cardiac

Figure 14. Figure 14.

Both the medial protolinergic neuron (MPN) and proctolin (PROC) can activate the pyloric rhythm. A: Cancer Borealis preparation. MPN was depolarized by intracellular current injection, resulting in activation of the pyloric rhythm. Ivn, lateral ventricular nerve; pdn, pyloric dilator nerve; LP, lateral pyloric. Bars = 0.5 s, 10 mV. B: Proctolin added to the bath in another preparation activated the rhythm. Bars = 1 s, 6 mV.

From
Figure 15. Figure 15.

(LG) Lateral gastric neuron can move from the pyloric to the gastric rhythm. Pyloric rhythm is monitored in the bottom traces (LP, VD) of each panel; gastric rhythm is monitored on the dgn in the upper traces. LG spontaneously shows a purely pyloric rhythm (A), a hybrid pattern (B), and a strong gastric pattern (C). Bars = 5 s for A and C; 2.5 for B: 16 mV for LG, 20 mV for LP in A and B; 26 mV for LG, 18 mV for VD in C. dgn, dorsal gastric nerve.

From
Figure 16. Figure 16.

Crayfish tail flip flow diagram. Block diagram of major relations among components of the escape response. Horizontal, dotted rectangle encloses components of the first, giant‐mediated tail flip; vertical, dotted rectangle encloses components of the swimming central pattern generator (CPG). The three sensory processors (a, b, c) are designated by their functions and may have elements in common. Numbers on lines refer to sequence of events. Arrows indicate excitation and dots indicate inhibition. LG, lateral giant neuron.

From
Figure 17. Figure 17.

Synaptic connectivity in the leech heartbeat central pattern generator. A: Schematic showing inhibitory synapses from identified premotor HN (heart) interneurons to HE (heart excitor) motoneurons. Open circles represent neurons (each numbered according to the ganglion in which it resides), lines represent their processes, and filled circles indicate inhibitory chemical synapses. B: Schematic showing all of the inhibitory synapses among the identified HN interneurons. HN cells with similar inputs, outputs, and properties are lumped together. C: Simultaneous intracellular recordings showing the normal activity of two reciprocally inhibitory HN interneurons of the timing oscillator [HN(L, 4)] and an HE motoneuron [HE(R, 5)] innervated by one of them. Dashed lines indicate a membrane potential of −50mV.

From
Figure 18. Figure 18.

Dendritic changes of motor neurons during insect metamorphosis. Morphology of abdominal motor neurons at different stages of life in Manduca. Camera lucida drawings of neuron injected with Co2+ in the larva, early pupa, and adult. A:MN‐1, a motor neuron that innervates different muscles in the larval and adult stages. During metamorphosis a new dendritic field develops contralateral to the axon. B:MN‐7, a motor neuron that innervates the same ventral muscle in all three stages of life. Dendritic structure is largely conserved, but there is growth of existing processes. This neuron and its target die following adult emergence. Drawing to the left shows relative positions of the two neurons in an abdominal ganglion.

From
Figure 19. Figure 19.

Activity‐dependent facilitation of a monosynaptic excitatory postsynaptic potential (EPSP) in the neuronal circuit for the withdrawal reflex of Aplysia. A1, A2: Experimental arrangement and protocol. Shading indicates that spike activity in the neuron is paired with unconditioned stimulus (US; conditional stimulus, CS). Fac, facilitator interneuron. B: Examples of EPSPs produced in a common postsynaptic siphon motor neuron (M.N.) by action potentials in a paired and an unpaired sensory neuron (S.N.) before (Pre) and 1 h after (Post) training. Facilitation of the EPSP from the paired sensory neuron was greater than that of the EPSP from the unpaired sensory neuron in the same experiment. C: Comparison of average cellular data showing differential facilitation of EPSPs and behavioral data showing differential conditioning of withdrawal reflex. Postsynaptic potential data are pooled from two types of experiment: paired vs. unpaired and paired vs. US alone. Facilitation of EPSPs from paired neurons was significantly greater than that of EPSPs from control neurons. Behavioral data are from experiments on conditioning of withdrawal reflex with the same protocol and parameters as cellular experiments. Testing was carried out 15 min after five training trials in both types of experiment.

From
Figure 20. Figure 20.

Olfactory integration pathways. A: Distributed projections into the brain of the cockroach from the antennal lobes, vr, dr, ventral and dorsal roots of antenno‐glomerular tracts (ACT) supplied by projection neurons arising from glomeruli of the antennal lobes. (From .) B: Generalist and specialist interneurons in moth antennal lobe. Each pair of traces shows the intracellular response of an identified olfactory interneuron to pulses of odor. In the first trace, a phasic response is evoked by single or blended components of the female pheromone of Manduca. In the second trace, the same combinations evoke inhibition in an interneuron. In the third trace, another interneuron responds only to one component and the blend in which that component is present. In the bottom trace, a fourth type of interneuron responds to pulses of one component of the blend. (From .) C: Responses by a uniquely identified glomerulus output neuron to trans‐2‐hexenal and isoamyl acetate (lower four traces and graphs, upper right), some at different concentrations. This neuron, which resides in a sexually isomorphic glomerulus, failed to respond to pheromonal odors (upper two traces). The neuron, reconstructed from a Lucifer yellow fill, invades the mushroom body calyx (Ca) and part of the lateral brain (LH), as diagrammed in the outline of the moth brain. (From .) Other abbreviations: cb, neuron cell body; P posterior; L laterol; MGC male‐specific “macroglomerular complex; G, glomeruli.” D: Summary of known connections deduced from electron microscopy of the glomeruli of the cockroach, Periplaneta americana. Afferents (RN) terminate on GABAergic local interneurons (GABA‐ir IN), unidentified profiles, and output neurons (uPN), which also receive additional inputs from local interneurons and provide outputs onto other unidentified profiles.

From
Figure 21. Figure 21.

Eye types and visual pathways. A; Comparison of superposition and neural superposition eyes. In the first, light enters through many facets and is focused by the cones (CC) onto a single receptor's rhabdome (Rh), reaching it through the clear zone (CZ). In the second (left), light reaches the tips of coaxial receptors in ommatidia that are screened from each other by light‐absorbing pigments. Axons from similarly aligned receptors terminate in a single column in the neuropil beneath. Below (right) are shown (1) ray paths through a crystalline cone of the apposition eye. Two types of open rhabdomere neural superposition retinas (2) contrast the asymmetric arrangements in evolutinarily advanced brachyceran flies (upper) with the radially symmetric arrangement in more primitive nematocerans (lower; ommatidial receptor cross sections, left). Their respective spacing of similarly aligned photoreceptors (closed profiles) in the retina are compared in 3 (from ). B: Comparison of electrical responses, dynamic ranges, and first‐order interneuron responses of a fly eye and salamander (Necturus) retina. In both insect and vertebrate, working ranges of the receptor are comparable, though one depolarizes to illumination and the other hyperpolarizes. In the lamina, the sign is reversed and the monopolar cell hyperpolarizes. In the vertebrate, the sign‐conserving synapse results in bipolar hyperpolarization. (From .) C: Cell organization from the deep optic neuropil in a fly. (a) Isomorphic neuronal assemblies subtend the whole visual field. In (b), (c), and (d), local assemblies subtend polarized light‐receptive zone of the retina, area of binocular overlap, and male‐specific area of high resolution (e), respectively. Heterolateral connections (f) link left and right optic lobes to provide connections for binocular perception of rotational panoramic stimuli. In (g), giant motion‐sensitive interneurons, characteristic of some flies, provide accessible elements for studying panoramic motion responses associated with visual control of flight.

From
Figure 22. Figure 22.

Motion computation and behavioral consequences. A: Upper left: Retinal sampling showing preferred direction of motion (filled arrows) along the retinal axes, v, h, x, y, compared to the dorsal (d) and anterior (a) body axes. Lower left: Hypothetical elementary motion‐detecting circuits (EMDs). Each has two input channels from two neighboring sampling units. These are linked by a connection containing a low‐pass filter (F), with the connections converging at a multiplier (M). The preferred direction is indicated by a plus sign providing excitation of a deeper collector interneuron. Middle: organization of directionally selective small‐ (SF) or large (LF) field‐collector neurons that channel information about rotational motion to downstream pathways that either excite or inhibit flight motor circuits (M) via hypothesized frequency filters (F). Upper right: Hypothetical model of control pathways responsible for spatial tuning of LF and SF systems. Excitatory or inhibitory outputs of EMDs are integrated by direction‐selective neurons (DSN). These represent LF or SF elements. EMDs are thought to branch to provide inputs to directionally selective inhibitory local interneurons (INH). INH provide shunting inhibition to EMDs (S) so that in the case of the LF system (lower right 1) the output of the DSN (R) increases proportional to the number of EMDs activated or decreases (lower right 2) after a certain number of EMDs have been activated, to provide the SF system. B: Encoding of directional motion in the lobula complex (left) and medulla (right). LF collector neurons (VS, lower left) show direction‐dependent DC depolarizations or hyperpolarizations. SF inputs to these cells (T5, upper left) show similar but lower amplitude responses. The inputs to T5 (Tm 1, right) have distinct responses to motion and flicker, and motion responses are direction‐dependent (vertical arrows, lower right). Reconstructions are from intracellular staining of the recorded cells (middle, T5; far right, Tm1; L2, L1, T4, T5 refer to neuropil layers). C: Excitatory or inhibitory interactions among wide‐field heterolateral or local interneurons of the lobula plate suggested to provide descending pathways with information about rotation, roll, and pitch of the visual panorama. Letters and numbers refer to cell types. Preferred directions are given above or below each.

A and C from . B from
Figure 23. Figure 23.

Coprocessing and synergy of visual, proprioceptive, and exteroreceptive information. Intracellular recordings from a uniquely identified descending neuron show its negligible response (A) to roll deviation simulated by a tilting horizon in the frontal part of the locust's visual field. In the dark, the neuron shows weak phasic responses (B) but reacts tonically and vigorously to wind onto the front of the head (C). Oscillating roll deviation stimuli modulates the response to wind (D). Modification is synergistically enhanced by head roll with roll deviation (E) but is unaffected by head roll alone (F). (From .) G: Schematic of convergence of sensory inputs onto two flight motor interneurons ( and ) that are presynaptic onto wing elevator flight motor neurons. Inhibitory synapses are shown as filled circles; depressor interneuron is activated by convergence of some identified descending neurons and inhibited by others. When activated, 302 inhibits wing elevator motor neurons, whereas 204 excites them and is driven by a different combination of descending elements. H: Corrective steering is controlled by a variety of different pathways, each registering coincident events that occur during deviation from forward flight. Each pathway coactivates neck (NMN), flight (FMN), leg (LMN), and abdominal (AMN) motor neurons when these receive excitatory drive from oscillator circuits (OSC). Other abbreviations are DN (descending) and AN (ascending) plurisegmental interneurons and IN, local spiking interneuron receiving afferents from the proesternum and abdomen.

From
Figure 24. Figure 24.

Control of posture in the locust. A: Constituent neurons: hair afferents, motor neuron, spiking, and nonspiking interneuron. Processes are shown within a thoracic ganglion. B: Double recording from hair (lower trace) and spiking interneuron (upper trace) demonstrating different amplitudes of generated excitatory postsynaptic potentials (EPSPs) in the postsynaptic interneuron. Positions of exteroreceptors from proximal to distal and dorsal to ventral are relected by EPSPs of different amplitudes in the spiking local interneuron. (From ) C: Double recording showing that when an appropriate exteroreceptor is stimulated (arrow) the evoked spikes in the spiking local interneuron are precisely followed by inhibitory postsynaptic potentials in the nonspiking local interneuron. D: Double recording from two nonspiking interneurons showing that increasing current injected into one causes graded inhibition in another. Spikes are recorded extracellularly from a motor neuron that is presumably postsynaptic to the excitatory depolarizing nonspiking local interneuron. Nonspiking local interneurons can either inhibit or activate motor neurons. In E, current injected into nonspiking interneurons gives rise to hyperpolarization on depolarization and a concomitant graded excitation or inhibition of a motor neuron.

From
Figure 25. Figure 25.

Control of posture. A: Schematic showing excitatory (triangles) convergence of exteroreceptive afferents onto anteromedial and midline spiking local interneurons. The latter make inhibitory connections (filled circles) with nonspiking local interneurons which inhibit or excite motor neurons or inhibit each other. Motor neurons are also excited by anteromedial spiking local interneurons and, in rare cases, by afferents themselves (For example, proprioceptors). A second class of efferents, intersegmental interneurons, receive comparable excitatory and inhibitory inputs directly from spiking local interneurons. (From .) B: Circuit diagram showing control through local interneurons of excitation of synergistic, and inhibition of antagonistic motor neurons involved in tibial extension and tarsal depression.

From


Figure 1.

Excitability in plants and unicellular microbes. A: Action potentials elicited by touch in touch‐sensitive plants, Mimosa pudica (upper) and Venus's‐flytrap, Dionaea muscipula (lower) (after ). B: Responses to mechanical stimulation of anterior and posterior ends of the ciliated protozoan Paramecium caudatum. Stimulation to the anterior end produces graded depolarization and a reversal of ciliary beat that results in a change in the direction of swimming. Stimulation of the posterior end causes transient hyperpolarization that results in an acceleration of the rate of ciliary beating and faster forward swimming (from ). C: Single‐channel patch clamp recordings of Ba2+ currents in outside out patches of sugar beets (Beta vulgaris) tonoplast membranes. Patches were continuously polarized to the values shown on the left. Channel openings and closings were observed at membrane potentials more negative than 0 mV. The presence of more than one channel in the patch was indicated by multiple opening events (from ). D: Activities of two types of ion channel reconstituted into liposomes from the bacterium Escherichia coli. The open probability of a mechanosensitive channel (upper) was increased by applying increasing suction pressures via the recording pipette. Pipette voltage was +40 mV. Voltage‐dependent channels (lower) were identified in a membrane patch held at −50 mV. Open and maximally closed levels (corresponding to the closure of seven conductance units) are indicated on the left.

from


Figure 2.

Regenerative depolarizing and hyperpolarizing action in the dinoflagellate Noctiluca in response to injection of current into the flotation vacuole in Ca2+ ‐deprived artificial seawater. Upper traces, membrane potential; lower traces, injected current. A, D: Current injected when membrane was more or less hyperpolarized after negative spike. B, C: Current injected when membrane was more or less depolarized after positive spike. A, B: Outward current. C, D: Inward current.

from


Figure 3.

Hypostomal nerve net and ring of Hydra oligactis. Whole‐mount of a head stained with an antiserum against RFamide, demonstrating the presence of a nerve ring in the hypostome. a: Side view of the head shows the hypostome and the basal parts of several tentacles. Tentacles emerge from the tentacle zone below the hypostome. The dark spot in the midst of the stained cells well above the ring is the mouth region, which is the apex of the hypostome. b: View from above the hypostome shows the dark mouth region in the center surrounded by a large number of epidermal sensory cells. Arrow shows a typical ganglion cell outside the nerve ring. Bars indicate 200 μm (a) and 100 μm (b).

From


Figure 4.

Bidirectional excitatory chemical synapse between elements of the motor nerve net in the jellyfish Cyanea capillata. All records from the same cell pair with stimuli being applied to the cell on the upper trace. A: Approximately 1 ms after the peak of the action potential in the postsynaptic cell (lower trace), a distinct notch (arrow) appears on the action potential in the presynaptic cell (upper trace). This notch is absent when only an excitatory postsynaptic potential (EPSP) appears in the postsynaptic cell (B). When a delayed spike was evoked from the postsynaptic cell, a clear EPSP (arrow) was evoked from the presynaptic cell (C).

Modified from


Figure 5.

Two sizes of action potential produced during swimming by the motor giant axon of the jellyfish Aglantha digitale. A: Scale drawing from a photograph of A. digitale, apex at the top. B: Schematic of the layout of ring giant, motor giant axons, and myoepithelium in the circumumbrellar margin of the body wall. C: Regenerative impulses recorded from isolated motor giant axon shortened to 700 μm. Axon penetrated with two micropipettes to inject current and record membrane voltage. Traces superimposed to show overshooting action potential and low‐threshold spike elicited by successive depolarizing current pulses. Current reduced by ∼0.1 nA between pulses; action potential elicited by higher current. Axon resting potential, −67 mV.

A: from ; B: modified from ; C: modified from


Figure 6.

A: Spontaneous plateau potentials recorded in the cell body of an AVF‐like interneuron in Ascaris suum. Arrow marks an inflection from a depolarizing ramp to a plateau potential. B: Injection of hyperpolarizing current of sufficient magnitude suppresses the production of plateau potentials. C: Brief depolarizations superimposed upon the sustained hyperpolarization activate plateaus at a discrete threshold. D: Brief (100 ms) pulse of depolarizing current resets the rhythm of spontaneous plateaus. I, current monitor trace.

From


Figure 7.

Schematic showing synaptic connections among the motoneurons and large interneurons in the segmentally repeating arrays of Ascaris suum. The synaptic connectivities of all three types of dorsal excitatory motoneuron are similar, so they have been combined (DE), as have the putative ventral excitors (VE). Excitatory synapses are represented by open triangles and inhibitory synapses by filled triangles. No direct recording has been made from VE motoneurons, so the signs of the synapses they make and receive are predictions based on their anatomical similarities to DE motoneurons. Dorsal inhibitory motoneuron, DI; ventral inhibitory motoneuron, VI.

From


Figure 8.

Lack of A‐current in shaker mutant muscle fibers. Voltage clamp recordings from larval muscle fibers of Drosophila. Note that the initial fast outward current in the normal, wild‐type fiber is absent in the fiber from a shaker mutant (Shks133).

Adapted from


Figure 9.

Plasticity at the crayfish neuromuscular junction. A: Time course of long‐term facilitation (LTF) shows a pretest period during which evoked excitatory postsynaptic potentials (EPSPs) are measured during 5 Hz stimulation once every 10 min, a tetanic phase during which induction of LTF takes place, and a long‐lasting phase of LTF. B: Demonstration of LTF produced by local depolarizing pulses applied to the axon terminal by intracellular stimulation. Depolarizing pulses of 60 nA were applied (presynaptic) and the resulting EPSPs recorded in a muscle cell (postsynaptic). Arrows indicate current pulse artifacts. Stimulation of the terminal at 20 Hz for 10 min. in the presence of normal Ca2+ produced a large enhancement of the evoked EPSPs without alteration of the presynaptic response during the tetanus, and a long‐lasting phase (LLP) at 60 min following the tetanus.

From


Figure 10.

Reciprocal control of motor neurons by a local nonspiking interneuron in a locust. Two motor neurons, the fast extensor (Ext. mn) and a fast flexor (Flex, mn) of the tibia, were recorded intracellularly, along with a nonspiking interneuron (int). A: A pulse of current injected into a neuropilar process of the interneuron evokes a sustained depolarization of the extensor and a sustained hyperpolarization of the flexor motor neuron. B–D: With more current, there is a progressive and graded increase in the amplitude of the voltage changes in the motor neurons. E: Relationship between current injected into the interneuron and the resulting voltage changes in the two motor neurons. F: Two groups of multiple sweeps at the start of a pulse of current reveal that voltage changes of opposite polarity begin at the same time in the two motor neurons. Calibration: vertical interneuron, 40 mV; fast extensor motor neuron, 4 mV; flexor, 8 mV; current, 30 nA; horizontal (A–D). 400 ms, (F) 64 ms.

From


Figure 11.

Stomatogastric ganglion activity pattern and circuit diagram. A: Diagram of stomatogastric ganglion preparation as it looks when pinned out in a sylgard‐lined chamber. Peripheral nerves (mvn, pdn, Ipn, pyn) contain the axons of motor neurons that innervate muscles of the pyloris and gastric mill. Two commissural ganglia (CG), esophageal ganglion (OG), and stomatogastric ganglion (STG) are shown, along with stomatogastric nerve (stn). Asterisk indicates the position where sucrose blocks are applied to remove descending influences on the STG. B: Burst pattern of the pyloric network. These extracellular recordings were obtained from preparations as shown in A. C: Synaptic connectivity circuit diagram of the pyloric network. Inhibitory chemical synapses are indicated by black dots and electrotonic synapses by resistor symbols. Dashed lines indicate weak synapses, solid lines strong synapses.

From


Figure 12.

Stomatogastric ganglion neurons involved in the pyloric rhythm are conditional oscillators. A: Simultaneous intracellular recordings from four pyloric neurons in an intact network. B: Same neuron types after synaptic isolation from other pyloric neurons with pharmacological and cell killing techniques. Intact input from other ganglia via the stomatogastric nerve. C: Same neurons no longer oscillate when axons within the stomatogastric nerve are blocked.

From


Figure 13.

Effects of different modulators on synaptically isolated pyloric neurons. Bath‐applied dopamine, octopamine, or serotonin produces very different effects on different neurons. (From .) AB, Anterior bouton; PD, pyloric dilator,; VD, ventricular dilator; LP, lateral pyloric; PY, pyloric; IC, inferior cardiac



Figure 14.

Both the medial protolinergic neuron (MPN) and proctolin (PROC) can activate the pyloric rhythm. A: Cancer Borealis preparation. MPN was depolarized by intracellular current injection, resulting in activation of the pyloric rhythm. Ivn, lateral ventricular nerve; pdn, pyloric dilator nerve; LP, lateral pyloric. Bars = 0.5 s, 10 mV. B: Proctolin added to the bath in another preparation activated the rhythm. Bars = 1 s, 6 mV.

From


Figure 15.

(LG) Lateral gastric neuron can move from the pyloric to the gastric rhythm. Pyloric rhythm is monitored in the bottom traces (LP, VD) of each panel; gastric rhythm is monitored on the dgn in the upper traces. LG spontaneously shows a purely pyloric rhythm (A), a hybrid pattern (B), and a strong gastric pattern (C). Bars = 5 s for A and C; 2.5 for B: 16 mV for LG, 20 mV for LP in A and B; 26 mV for LG, 18 mV for VD in C. dgn, dorsal gastric nerve.

From


Figure 16.

Crayfish tail flip flow diagram. Block diagram of major relations among components of the escape response. Horizontal, dotted rectangle encloses components of the first, giant‐mediated tail flip; vertical, dotted rectangle encloses components of the swimming central pattern generator (CPG). The three sensory processors (a, b, c) are designated by their functions and may have elements in common. Numbers on lines refer to sequence of events. Arrows indicate excitation and dots indicate inhibition. LG, lateral giant neuron.

From


Figure 17.

Synaptic connectivity in the leech heartbeat central pattern generator. A: Schematic showing inhibitory synapses from identified premotor HN (heart) interneurons to HE (heart excitor) motoneurons. Open circles represent neurons (each numbered according to the ganglion in which it resides), lines represent their processes, and filled circles indicate inhibitory chemical synapses. B: Schematic showing all of the inhibitory synapses among the identified HN interneurons. HN cells with similar inputs, outputs, and properties are lumped together. C: Simultaneous intracellular recordings showing the normal activity of two reciprocally inhibitory HN interneurons of the timing oscillator [HN(L, 4)] and an HE motoneuron [HE(R, 5)] innervated by one of them. Dashed lines indicate a membrane potential of −50mV.

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Figure 18.

Dendritic changes of motor neurons during insect metamorphosis. Morphology of abdominal motor neurons at different stages of life in Manduca. Camera lucida drawings of neuron injected with Co2+ in the larva, early pupa, and adult. A:MN‐1, a motor neuron that innervates different muscles in the larval and adult stages. During metamorphosis a new dendritic field develops contralateral to the axon. B:MN‐7, a motor neuron that innervates the same ventral muscle in all three stages of life. Dendritic structure is largely conserved, but there is growth of existing processes. This neuron and its target die following adult emergence. Drawing to the left shows relative positions of the two neurons in an abdominal ganglion.

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Figure 19.

Activity‐dependent facilitation of a monosynaptic excitatory postsynaptic potential (EPSP) in the neuronal circuit for the withdrawal reflex of Aplysia. A1, A2: Experimental arrangement and protocol. Shading indicates that spike activity in the neuron is paired with unconditioned stimulus (US; conditional stimulus, CS). Fac, facilitator interneuron. B: Examples of EPSPs produced in a common postsynaptic siphon motor neuron (M.N.) by action potentials in a paired and an unpaired sensory neuron (S.N.) before (Pre) and 1 h after (Post) training. Facilitation of the EPSP from the paired sensory neuron was greater than that of the EPSP from the unpaired sensory neuron in the same experiment. C: Comparison of average cellular data showing differential facilitation of EPSPs and behavioral data showing differential conditioning of withdrawal reflex. Postsynaptic potential data are pooled from two types of experiment: paired vs. unpaired and paired vs. US alone. Facilitation of EPSPs from paired neurons was significantly greater than that of EPSPs from control neurons. Behavioral data are from experiments on conditioning of withdrawal reflex with the same protocol and parameters as cellular experiments. Testing was carried out 15 min after five training trials in both types of experiment.

From


Figure 20.

Olfactory integration pathways. A: Distributed projections into the brain of the cockroach from the antennal lobes, vr, dr, ventral and dorsal roots of antenno‐glomerular tracts (ACT) supplied by projection neurons arising from glomeruli of the antennal lobes. (From .) B: Generalist and specialist interneurons in moth antennal lobe. Each pair of traces shows the intracellular response of an identified olfactory interneuron to pulses of odor. In the first trace, a phasic response is evoked by single or blended components of the female pheromone of Manduca. In the second trace, the same combinations evoke inhibition in an interneuron. In the third trace, another interneuron responds only to one component and the blend in which that component is present. In the bottom trace, a fourth type of interneuron responds to pulses of one component of the blend. (From .) C: Responses by a uniquely identified glomerulus output neuron to trans‐2‐hexenal and isoamyl acetate (lower four traces and graphs, upper right), some at different concentrations. This neuron, which resides in a sexually isomorphic glomerulus, failed to respond to pheromonal odors (upper two traces). The neuron, reconstructed from a Lucifer yellow fill, invades the mushroom body calyx (Ca) and part of the lateral brain (LH), as diagrammed in the outline of the moth brain. (From .) Other abbreviations: cb, neuron cell body; P posterior; L laterol; MGC male‐specific “macroglomerular complex; G, glomeruli.” D: Summary of known connections deduced from electron microscopy of the glomeruli of the cockroach, Periplaneta americana. Afferents (RN) terminate on GABAergic local interneurons (GABA‐ir IN), unidentified profiles, and output neurons (uPN), which also receive additional inputs from local interneurons and provide outputs onto other unidentified profiles.

From


Figure 21.

Eye types and visual pathways. A; Comparison of superposition and neural superposition eyes. In the first, light enters through many facets and is focused by the cones (CC) onto a single receptor's rhabdome (Rh), reaching it through the clear zone (CZ). In the second (left), light reaches the tips of coaxial receptors in ommatidia that are screened from each other by light‐absorbing pigments. Axons from similarly aligned receptors terminate in a single column in the neuropil beneath. Below (right) are shown (1) ray paths through a crystalline cone of the apposition eye. Two types of open rhabdomere neural superposition retinas (2) contrast the asymmetric arrangements in evolutinarily advanced brachyceran flies (upper) with the radially symmetric arrangement in more primitive nematocerans (lower; ommatidial receptor cross sections, left). Their respective spacing of similarly aligned photoreceptors (closed profiles) in the retina are compared in 3 (from ). B: Comparison of electrical responses, dynamic ranges, and first‐order interneuron responses of a fly eye and salamander (Necturus) retina. In both insect and vertebrate, working ranges of the receptor are comparable, though one depolarizes to illumination and the other hyperpolarizes. In the lamina, the sign is reversed and the monopolar cell hyperpolarizes. In the vertebrate, the sign‐conserving synapse results in bipolar hyperpolarization. (From .) C: Cell organization from the deep optic neuropil in a fly. (a) Isomorphic neuronal assemblies subtend the whole visual field. In (b), (c), and (d), local assemblies subtend polarized light‐receptive zone of the retina, area of binocular overlap, and male‐specific area of high resolution (e), respectively. Heterolateral connections (f) link left and right optic lobes to provide connections for binocular perception of rotational panoramic stimuli. In (g), giant motion‐sensitive interneurons, characteristic of some flies, provide accessible elements for studying panoramic motion responses associated with visual control of flight.

From


Figure 22.

Motion computation and behavioral consequences. A: Upper left: Retinal sampling showing preferred direction of motion (filled arrows) along the retinal axes, v, h, x, y, compared to the dorsal (d) and anterior (a) body axes. Lower left: Hypothetical elementary motion‐detecting circuits (EMDs). Each has two input channels from two neighboring sampling units. These are linked by a connection containing a low‐pass filter (F), with the connections converging at a multiplier (M). The preferred direction is indicated by a plus sign providing excitation of a deeper collector interneuron. Middle: organization of directionally selective small‐ (SF) or large (LF) field‐collector neurons that channel information about rotational motion to downstream pathways that either excite or inhibit flight motor circuits (M) via hypothesized frequency filters (F). Upper right: Hypothetical model of control pathways responsible for spatial tuning of LF and SF systems. Excitatory or inhibitory outputs of EMDs are integrated by direction‐selective neurons (DSN). These represent LF or SF elements. EMDs are thought to branch to provide inputs to directionally selective inhibitory local interneurons (INH). INH provide shunting inhibition to EMDs (S) so that in the case of the LF system (lower right 1) the output of the DSN (R) increases proportional to the number of EMDs activated or decreases (lower right 2) after a certain number of EMDs have been activated, to provide the SF system. B: Encoding of directional motion in the lobula complex (left) and medulla (right). LF collector neurons (VS, lower left) show direction‐dependent DC depolarizations or hyperpolarizations. SF inputs to these cells (T5, upper left) show similar but lower amplitude responses. The inputs to T5 (Tm 1, right) have distinct responses to motion and flicker, and motion responses are direction‐dependent (vertical arrows, lower right). Reconstructions are from intracellular staining of the recorded cells (middle, T5; far right, Tm1; L2, L1, T4, T5 refer to neuropil layers). C: Excitatory or inhibitory interactions among wide‐field heterolateral or local interneurons of the lobula plate suggested to provide descending pathways with information about rotation, roll, and pitch of the visual panorama. Letters and numbers refer to cell types. Preferred directions are given above or below each.

A and C from . B from


Figure 23.

Coprocessing and synergy of visual, proprioceptive, and exteroreceptive information. Intracellular recordings from a uniquely identified descending neuron show its negligible response (A) to roll deviation simulated by a tilting horizon in the frontal part of the locust's visual field. In the dark, the neuron shows weak phasic responses (B) but reacts tonically and vigorously to wind onto the front of the head (C). Oscillating roll deviation stimuli modulates the response to wind (D). Modification is synergistically enhanced by head roll with roll deviation (E) but is unaffected by head roll alone (F). (From .) G: Schematic of convergence of sensory inputs onto two flight motor interneurons ( and ) that are presynaptic onto wing elevator flight motor neurons. Inhibitory synapses are shown as filled circles; depressor interneuron is activated by convergence of some identified descending neurons and inhibited by others. When activated, 302 inhibits wing elevator motor neurons, whereas 204 excites them and is driven by a different combination of descending elements. H: Corrective steering is controlled by a variety of different pathways, each registering coincident events that occur during deviation from forward flight. Each pathway coactivates neck (NMN), flight (FMN), leg (LMN), and abdominal (AMN) motor neurons when these receive excitatory drive from oscillator circuits (OSC). Other abbreviations are DN (descending) and AN (ascending) plurisegmental interneurons and IN, local spiking interneuron receiving afferents from the proesternum and abdomen.

From


Figure 24.

Control of posture in the locust. A: Constituent neurons: hair afferents, motor neuron, spiking, and nonspiking interneuron. Processes are shown within a thoracic ganglion. B: Double recording from hair (lower trace) and spiking interneuron (upper trace) demonstrating different amplitudes of generated excitatory postsynaptic potentials (EPSPs) in the postsynaptic interneuron. Positions of exteroreceptors from proximal to distal and dorsal to ventral are relected by EPSPs of different amplitudes in the spiking local interneuron. (From ) C: Double recording showing that when an appropriate exteroreceptor is stimulated (arrow) the evoked spikes in the spiking local interneuron are precisely followed by inhibitory postsynaptic potentials in the nonspiking local interneuron. D: Double recording from two nonspiking interneurons showing that increasing current injected into one causes graded inhibition in another. Spikes are recorded extracellularly from a motor neuron that is presumably postsynaptic to the excitatory depolarizing nonspiking local interneuron. Nonspiking local interneurons can either inhibit or activate motor neurons. In E, current injected into nonspiking interneurons gives rise to hyperpolarization on depolarization and a concomitant graded excitation or inhibition of a motor neuron.

From


Figure 25.

Control of posture. A: Schematic showing excitatory (triangles) convergence of exteroreceptive afferents onto anteromedial and midline spiking local interneurons. The latter make inhibitory connections (filled circles) with nonspiking local interneurons which inhibit or excite motor neurons or inhibit each other. Motor neurons are also excited by anteromedial spiking local interneurons and, in rare cases, by afferents themselves (For example, proprioceptors). A second class of efferents, intersegmental interneurons, receive comparable excitatory and inhibitory inputs directly from spiking local interneurons. (From .) B: Circuit diagram showing control through local interneurons of excitation of synergistic, and inhibition of antagonistic motor neurons involved in tibial extension and tarsal depression.

From
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E. A. Arbas, R. B. Levine, N. J. Strausfeld. Invertebrate Nervous Systems. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 751-852. First published in print 1997. doi: 10.1002/cphy.cp130211