Entomology 3rd edition - C.Gillott - Chapter 13 pps

Wrapped around each axon or groups of smaller axons are other glial Schwann cells Figure 13.3B, These cells effectively isolate axons from the hemolymph in which they are bathed, However

of the stimulus Only very rarely does a stimulus act directly on the effector system; almostalways a stimulus is received by an appropriate sensory structure and taken to the cen-tral nervous system, which “determines” an appropriate response under the circumstances.When a response is immediate, that is, achieved in a matter of seconds or less, it is the ner-vous system that transfers the message to the effector system Such responses are usuallytemporary in nature Delayed responses are achieved through the use of chemical messages(viz., hormones) and are generally longer-lasting The nervous and endocrine systems of

an individual are, then, the systems that coordinate the response with the stimulus chemicals, which constitute another chemical regulating system, coordinate behavior anddevelopment among individuals They comprise pheromones (intraspecific coordinators)and allelochemicals (interspecific coordinators), which include kairomones and allomones

Semio-2 Nervous System

Like that of other animals, the nervous system of insects consists of nerve cells (neurons)and glial cells Each neuron comprises a cell body (perikaryon) where a nucleus, manymitochondria, and other organelles are located, and a cytoplasmic extension, the axon,which is usually much branched, the branches being known as neurites Axons may belong, as in sensory neurons, motor neurons, and principal interneurons, or very short,

as in local interneurons Often, insect neurons are monopolar, lacking the dendritic treecharacteristic of vertebrate nerve cells, though bipolar and multipolar neurons do occur(Figure 13.1) Motor (efferent) neurons, which carry impulses from the central nervoussystem, are monopolar, and their perikarya are located within a ganglion Sensory (afferent)neurons are usually bipolar but may be multipolar, and their cell bodies are adjacent to

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FIGURE 13.1. Neurons found in the sect nervous system Arrows indicate direc- tion of impulse conduction (A) Monopolar; (B) bipolar; and (C) multipolar [After R F.

in-Chapman, 1971, The Insects: Structure and

Function.By permission of Holland, Inc., and the author.]

Elsevier/North-the sense organ Interneurons (also called internuncial or association neurons) transmitinformation from sensory to motor neurons or other interneurons; they may be mono- orbipolar and their cell bodies occur in a ganglion Interneurons may be intersegmental andbranched, so that the variety of pathways along which information can travel and, therefore,the variety of responses are increased

Neurons are not directly connected to each other or to the effector organ but are separated

by a minute space, the synapse or neuromuscular junction, respectively Impulses may betransferred across the synapse either electrically or chemically (Section 2.3) The normaldiameter of axons is 5µm orµµ less; however, some interneurons within the ventral nervecord, the so-called “giant fibers,” have diameters up to 60µm These giant fibers may runµµthe length of the nerve cord without synapsing and are unbranched except at their termini.They are well suited, therefore, for very rapid transmission of information from sense organ

to effector organ; that is, they facilitate a very rapid but stereotyped response to a stimulusand for some insects are important in escape reactions (Hoyle, 1974; Ritzmann, 1984).Neurons are aggregated into nerves and ganglia Nerves include only the axonal com-ponent of neurons, whereas ganglia include axons, perikarya, and dendrites The typicalstructures of a ganglion and interganglionic connective are shown in Figure 13.2 In a gan-glion there is a central neuropile that comprises a mass of efferent, afferent, and associationaxons Frequently visible within the neuropile are groups of axons running parallel, known

as fiber tracts The perikarya of motor and association neurons are normally found in clustersadjacent to the neuropile

Surrounding the neurons are glial cells, which are differentiated according to theirposition and function The peripheral glial (perineural) cells, which form the perineurium,

NERVOUS AND CHEMICAL INTEGRATION

FIGURE 13.2. Cross-sections through (A) abdominal ganglion and (B) interganglionic connective to show

general structure [A, after K D Roeder, 1963, Nerve Cells and Insect Behaviour By permission of Harvard

University Press B, after J.E Treherne and Y Pichon, 1972, The insect blood-brain barrier, Adv Insect Physiol.

9:257–313 By permission of Academic Press Ltd., London, and the authors.]

are very closely associated by tight junctions, forming the blood-brain barrier (Carlson et al.,

2000; Kretzschmar and Pflugfelder, 2002) This barrier is critical in isolating the nervous

system from the hemolymph whose composition is both highly variable and inappropriate

for neuronal function (see Chapter 17, Section 4) However, the barrier itself creates two

potential problems, namely, obtaining adequate supplies of oxygen and nutrients for the

neural elements The former is solved by having tracheae running deeply into the ganglia,

the latter by the ability of the perineural cells to transfer materials between the hemolymph

and neurons In addition, they secrete the neural lamella, a protective sheath that contains

collagen fibrils and mucopolysaccharide The lamella is freely permeable, enabling the

perineural cells to accumulate nutrients from the hemolymph The inner glial cells occur

among the perikarya into which they extend fingerlike extensions of their cytoplasm, the

trophospongium (Figure 13.3A) The function of these cells is to transport nutrients from

perineural cells to the perikarya Once in the perikarya, nutrients are transported to their

site of use by cytoplasmic streaming

Wrapped around each axon or groups of smaller axons are other glial (Schwann) cells

(Figure 13.3B), These cells effectively isolate axons from the hemolymph in which they are

bathed, However, in contrast to the situation in vertebrates, the glial cells are not compacted

to form a myelin sheath but rather are loosely wound around the axons, Further, in insect

nerves there are no distinct nodes of Ranvier (the regions between adjacent glial cells);

hence, saltatory conduction of impulses does not occur (Section 2.3)

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FIGURE 13.3. (A) Cell body of motor neuron showing trophospongium; and (B) cross-section through axons

and surrounding Schwann cells [A, after V B Wigglesworth, 1965, The Principles of Insect Physiology, 6th ed.,

Methuen and Co By permission of the author B, after J E Treherne, and Y Pichon, 1972, The insect blood-brain

barrier, Adv Insect Physiol 9:257–313 .By permission of Academic Press Ltd., London, and the authors.]

Structurally, the nervous system may be divided into (1) the central nervous systemand its peripheral nerves and (2) the visceral nervous system

2.1 Central Nervous System

The central nervous system arises during embryonic development as an ectodermaldelamination on the ventral side (Chapter 20, Section 7.3) Each embryonic segment in-cludes initially a pair of ganglia, though these soon fuse In addition, varying degrees of

NERVOUS AND CHEMICAL INTEGRATION

FIGURE 13.4. (A) Lateral view of anterior central nervous system, stomatogastric nervous system, and

en-docrine glands of a typical acridid; (B) diagrammatic dorsal view of brain and associated structures to show

paths of neurosecretory axons and relationship of corpora cardiaca and corpora allata; (C) dorsal view of corpora

cardiaca to show distinct storage and glandular zones; and (D,E) transverse sections through corpora cardiaca

at levels a–a and b–b, respectively [A, after F O Albrecht, 1953, The Anatomy of the Migratory Locust By

permission of The Athlone Press B–E, after K C Highnam, and L Hill, 1977, The Comparative Endocrinology

of the Invertebrates, 2nd ed By permission of Edward Arnold Publishers Ltd.]

anteroposterior fusion occur so that composite ganglia result Thus, in an adult insect the

central nervous system comprises the brain, subesophageal ganglion, and a varied number

of ventral ganglia

The brain (Figure 13.4A) is probably derived from the ganglia of three segments and

forms the major association center of the nervous system It includes the protocerebrum,

deutocerebrum, and tritocerebrum The protocerebrum, the largest and most complex region

of the brain, contains both neural and endocrine (neurosecretory) elements Anteriorly it

forms the proximal part of the ocellar nerves (the only occasion on which the cell bodies

of sensory neurons are located other than adjacent to the sense organ), and laterally is

fused with the optic lobes Within the protocerebrum is a pair of corpora pendunculata,

the mushroom bodies, so-called because of their outline in cross-section The mushroom

bodies are important association centers, receiving sensory inputs, especially olfactory and

visual, and relaying the information to other protocerebral centers (Strausfeld et al., 1998;

Gronenberg, 2001) Further, they play a central role in learning and memory (Section 2.4),

and their size can be broadly correlated with the development of complex behavior patterns

They are most highly developed in the social Hymenoptera In worker ants, for example,

they make up about one-fifth the volume of the brain The median central body is an

other important association center, one function of which appears to be the coordination

to possess polarized light-sensitive interneurons, suggesting a role for these centers in

navigation (Vitzthum et al., 2002) Each optic lobe contains three neuropilar masses in

which light stimuli, including those generated by polarized light, are assessed and forwarded

to other brain centers

The deutocerebrum is largely composed of the paired antennal lobes (Homberg

et al., 1989; Hannson and Anton, 2000) These two neuropiles include both sensory and

motor neurons and are responsible for initiating both responses to antennal stimuli, cially olfactory and mechanosensory, and movements of the antennae In species wherefemales produce sex-pheromones the antennal lobes often show sexual dimorphism, beinglarger with additional interneurons in males From the antennal lobes, interneurons convey

NERVOUS AND CHEMICAL INTEGRATION

information to association centers in both the protocerebrum and thoracic ganglia Together

with the mushroom bodies, the antennal lobes are essential in learned olfactory behavior

The transfer of mechanosensory inputs to the ventral ganglia is likely related to perception

and avoidance of objects encountered during walking

The tritocerebrum is a small region of the brain located beneath the deutocerebrum and

comprises a pair of neuropiles that contain axons, both sensory and motor, leading to/from

the frontal ganglion and labrum

The subesophageal ganglion is also composite and includes the elements of the

embry-onic ganglia of the mandibular, maxillary, and labial segments From this ganglion, nerves

containing both sensory and motor axons run to the mouthparts, salivary glands, and neck

The ganglion also appears to be the center for maintaining (though not initiating) locomotor

activity

In most insects the three segmental thoracic ganglia remain separate Though details

vary from species to species, each ganglion innervates the leg and flight muscles (direct and

indirect), spiracles, and sense organs of the segment in which it is located

The maximum number of abdominal ganglia is eight, seen in the adult bristletail

Machilis and larvae of many species, though even in these insects the terminal ganglion

is composite, including the last four segmental ganglia of the embryonic stage Varying

degrees of fusion of the abdominal ganglia occur in different orders and sometimes there is

fusion of the composite abdominal ganglion with the ganglia of the thorax to form a single

thoracoabdominal ganglion (Chapters 5–10 contain the details for individual orders.)

2.2 Visceral Nervous System

The visceral (sympathetic) nervous system includes three parts: the stomatogastric

system, the unpaired ventral nerves, and the caudal sympathetic system The stomatogastric

system, shown partially in Figure 13.4, arises during embryogenesis as an invagination of

the dorsal wall of the stomodeum Generally, it includes the frontal ganglion, recurrent nerve

which lies mediodorsally above the gut, hypocerebral ganglion, a pair of inner esophageal

nerves, a pair of outer esophageal (gastric) nerves, each of which normally terminates in

an ingluvial (ventricular) ganglion situated alongside the posterior foregut, and various fine

nerves from these ganglia that innervate the foregut and midgut, and, in some species, the

heart A single median ventral nerve arises from each thoracic and abdominal ganglion in

some insects The nerve branches and innervates the spiracle on each side In species

where this nerve is absent, paired lateral nerves from the segmental ganglia innervate

the spiracles The caudal sympathetic system, comprising nerves arising from the composite

terminal abdominal ganglion, innervates the hindgut and sexual organs Nerves within

the stomatogastric system both collect mechanosensory and chemical information from,

and regulate the muscular activity of, the organs they supply In the frontal ganglion, at

least, the neuropile has a central pattern generator (Section 2.3) that controls rhythmic

motor activity of the foregut (Ayali et al., 2002).

2.3 Physiology of Neural Integration

As noted in the Introduction to this chapter, an insect’s nervous system is constantly

receiving stimuli of different kinds both from the external environment and from within

its own body The subsequent response of the insect depends on the net assessment of

these stimuli within the central nervous system The processes of receiving, assessing, and

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FIGURE 13.5. Cross-section to show major areas of brain [After R F Chapman, 1971, The Insects: Structure

and Function By permission of Elsevier/North-Holland, Inc., and the author.]

responding to stimuli collectively constitute neural integration Neural integration includes,therefore, the biophysics of impulse transmission along axons and across synapses, the reflexpathways (in insects, intrasegmental) from sense organ to effector organ, and coordination

of these segmental events within the central nervous system

Impulse transmission along axonal membranes and across synapses appears to be sentially the same as in other animals and will not be discussed here in detail However, theabsence of a myelin sheath and nodes of Ranvier precludes the phenomenon of saltatoryconduction seen in vertebrates Following the arrival of a stimulus of sufficient magnitude,

es-an action potential is generated es-and the impulse travels along the axon as a wave of polarization The speed of impulse transmission is a function of axonal diameter so that

de-in giant axons values of 3–7 m per sec have been recorded while de-in average-sized axonsthe speed is 1.5–2.3 m per sec In addition to “spiking” neurons (i.e., those in which anaction potential can be generated), there are in the insect central nervous system intragan-glionic “non-spiking” interneurons unable to produce action potentials Rather, the amount

of neurotransmitter released at their synapses (see below) is proportional to the size of theirendogenous membrane permeability changes; in other words, they release neurotransmitter(and affect the postsynaptic neuron) in a graded manner These non-spiking interneuronsmay have wide importance in the initiation of rhythmic behaviors such as walking, swim-ming, and chewing (see below)

Transmission across a synapse, depending as it does on diffusion of molecules throughfluid, is relatively slow and may take up about 25% of the total time for conduction of

an impulse through a reflex arc Rarely, when a synaptic gap is narrow (i.e., pre- andpostsynaptic membranes are closely apposed), the ionic movements across the presynapticmembrane are sufficient to directly induce depolarization of the postsynaptic membrane

NERVOUS AND CHEMICAL INTEGRATION

(Huber, 1974) Mostly, however, when an impulse reaches a synapse, it causes release

of a chemical (a neurotransmitter) from membrane-bound vesicles The chemical diffuses

across the synapse and, in excitatory neurons, brings about depolarization of the

postsy-naptic membrane Acetylcholine is the predominant neurotransmitter liberated at excitatory

synapes, including those of interneurons and afferent neurons from mechanosensilla and

taste sensilla (Homberg, 1994) 5-Hydroxytryptamine (serotonin), histamine, octopamine,

and dopamine function as central nervous system excitatory neurotransmitters in specific

situations on occasion These, and other amines, have an excitatory effect when applied in

low concentrations to the heart, gut, reproductive tract, etc., and it may be that they also

serve as neurotransmitters in the visceral nervous system

Sometimes a single nerve impulse arriving at the presynaptic membrane does not

stimulate the release of a sufficient amount of neurotransmitter Thus, the magnitude of

depolarization of the postsynaptic membrane is not large enough to initiate an impulse in

the postsynaptic axon If additional impulses reach the presynaptic membrane before the

first depolarization has decayed, sufficient additional neurotransmitter may be released so

that the minimum level for continued passage of the impulse (the “threshold” level) is

ex-ceeded This additive effect of the presynaptic impulses is known as temporal summation

A second form of summation is spatial, which occurs at convergent synapses Here, several

sensory axons synapse with one internuncial neuron A postsynaptic impulse is initiated

only when impulses from a sufficient number of sensory axons arrive at the synapse

si-multaneously Divergent synapses are also found where the presynaptic axon synapses with

several postsynaptic neurons In this arrangement the arrival of a single impulse at a synapse

may be sufficient to initiate impulse transmission in, say, one of the postsynaptic neurons

The arrival of additional impulses in quick succession will lead to the initiation of impulses

in other postsynaptic neurons whose threshold levels are higher Thus, synapses play an

important role in selection of an appropriate response for a given stimulus

Eventually, an impulse reaches the effector organ, most commonly muscle Between

the tip of the motor axon and the muscle cell membrane is a fluid-filled space, comparable to

a synapse, called a neuromuscular junction Again, to achieve depolarization of the muscle

cell membrane and, ultimately, muscle contraction, a chemical released from the tip of the

axon diffuses across the neuromuscular junction In insect skeletal muscle, this chemical is

L-glutamate; in visceral muscles, glutamate, serotonin, and the pentapeptide proctolin have

all been suggested as candidate neurotransmitters

In addition to stimulatory (excitatory) neurons, inhibitory neurons whose

neurotrans-mitter causes hyperpolarization of the postsynaptic or effector cell membrane are also

impor-tant in neural integration When inhibition occurs at a synapse within the central nervous

sys-tem, it is known as central inhibition Central inhibition is the prevention of the normal

stimu-latory output from the central nervous system and may arise spontaneously within the system

or result from sensory input For example, copulatory movements of the abdomen in the male

mantis, which are regulated by a segmental reflex pathway located within the terminal

ab-dominal ganglion, are normally inhibited by spontaneous impulses arising within the brain

and passing down the ventral nerve cord.In the fly Protophormia the stimulation of stretch

receptors during feeding results in decreased sensitivity to taste caused by central inhibition

of the positive stimuli received by the brain from the tarsal chemoreceptors When inhibition

of an effector organ occurs it is known as peripheral inhibition At both synapses and

neuro-muscular junctions, the hyperpolarizing chemical isγ-aminobutyric acid (Homberg, 1994)

Mention must also be made of neuromodulators, a group of chemicals that can

modify the effects of neurotransmitters (Orchard, 1984; Homberg, 1994) Typically,

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neuromodulators are released from the tip of an adjacent neuron (less commonly as aneurohormone released into the hemolymph) and act on the presynaptic or postsynapticmembrane adjacent to, but not within, the synaptic gap or neuromuscular junction Theireffects include reduction in the amount of neurotransmitter released and inhibition of the ac-tion of the neurotransmitter Amines, especially octopamine, and some neuropeptides (e.g.,proctolin) are likely to be important neuromodulators, though in many instances definitiveevidence is still lacking A probable neuromodulator of a special kind may be nitric oxide.This very short-lived, rapidly diffusing gas was discovered in nervous tissues of locusts,

honey bees, and Drosophila in the early 1990s Production of nitric oxide is especially rich

in interneurons in the antennal and optic lobes, as well as in antennal chemosensory cells

of some species, following appropriate olfactory and visual stimulation, suggesting thatthis unconventional neuromodulator may have roles in olfactory information processing,olfactory memory, and vision (M¨uller, 1997; Bicker, 1998)

In insects reflex responses are segmental, that is, a stimulus received by a sense organ

in a particular segment initiates a response that travels via an interneuron located in thatsegment’s ganglion to an effector organ in the same segment This is easily demonstrated byisolating individual segments For example, in an isolated thoracic segment preparation of

a grasshopper, touching the tarsus causes the leg to make a stepping movement Of course,

in an intact insect such a stimulus also leads to compensatory movements of other legs tomaintain balance or to initiate walking, activities that are coordinated via association centers

in the subesophageal ganglion Touching the tip of the isolated ovipositor in Bombyx, for

example, initiates typical egg-laying movements, provided that the terminal ganglion andits nerves are intact In other words, each segmental ganglion possesses a good deal of reflexautonomy

Nervous activity of the type described above, which occurs only after an appropriatestimulus is given, is said to be exogenous However, an important component of nervousactivity in insects is endogenous, that is, does not require sensory input but is based onneurons with intrinsic pacemakers Such neurons (non-spiking neurons) possess specializedmembrane regions that undergo periodic, spontaneous changes in excitability (permeability)and where impulses are thereby initiated A wide variety of motor responses are organized,

in part, by endogenous activity For example, ventilation movements of the abdomen areinitiated by endogenous activity in individual ganglia Even walking and stridulation aremotor responses under partially endogenous control (Huber, 1974) An obvious question

to ask, therefore, is “Why don’t insects walk or stridulate continuously?” The answer isthat these and all other motor responses are “controlled” by higher centers, specificallythe brain and/or subesophageal ganglion These association centers assess all informationcoming in via sensory neurons and, on this total assessment, determine the nature of theresponse In addition, the centers coordinate and modify identical segmental activities,such as ventilation movements, so that they operate most efficiently under a given set ofconditions

Early evidence for the role of the brain and subesophageal ganglion as coordinatingcenters came from fairly crude experiments in which one or both centers were removed andthe resultant behavior of an insect observed More recent experiments involving localizeddestruction or stimulation of parts of these centers have confirmed and added significantly

to the general picture obtained by earlier authors To illustrate the complexity of nation and control of motor activity, walking will be used as an example This rhythmicstepping movement of each leg is controlled by a network of non-spiking neurons (calledthe central pattern generator and located in each half ganglion) whose endogenous activity

NERVOUS AND CHEMICAL INTEGRATION

sends signals (via motor neurons) alternately to the extensor and flexor leg muscles

(Chap-ter 14, Section 3.2.1) The signals may be excitatory or inhibitory and, in effect, serve to

switch on or off the muscles Intraganglionic and intersegmental coordination among the

central pattern generators, and ultimately leg movements, is achieved via normal

interneu-rons This is readily shown by cutting even one connective of the pair between adjacent

ganglia when coordinated stepping is disrupted Though the overall control of walking, that

is, starting, stopping, turning, and change of speed, resides in the brain, the subesophageal

ganglion is also involved Removal of the latter, for example, sensitizes some insects so that

they walk incessantly in response to even slight stimuli In the brain the mushroom bodies

and central body play major roles in the regulation of walking Impulses originating in the

mushroom bodies inhibit locomotor activity, presumably by decreasing the excitability of

the subesophageal ganglion Moreover, reciprocal inhibition may occur between the

mush-room body on each side of the brain, and this is the basis of the turning response In contrast,

the central body appears to be an important excitatory system in locomotion, because its

stimulation evokes fast running, jumping, and flying in some species As yet, however, the

interaction between these two cerebral association centers is not understood

Superimposed on the central control of walking is the influence of sensory stimuli

received by the insect; that is, the insect adjusts its walking pattern to suit environmental

conditions such as movement uphill or downhill, along a slope, or over rough terrain To

this end, the legs are equipped with a variety of mechanoreceptors that provide information

on their position, loading, and movement (Chapter 12, Section 2) In a walking Colorado

potato beetle, contact between the antennae and an obstacle causes the insect to modify its

body angle The extent to which the body angle is changed is proportional to the height

of the obstacle, allowing the beetle to extend the reach of the prothoracic leg so as to step

up on to the obstacle Insects that use running to escape predators receive information via

other sensory pathways For example, in the cockroach escape reaction, even the slightest

air movements stimulate hairs on the cerci that are both velocity- and direction-sensitive

The information received travels via giant axons in the ventral nerve cord to the thoracic

ganglia to initiate both the running and the turning away responses within 0.5 msec of the

stimulus being received

At the outset, insect behavior is dependent on the environmental stimuli received,

though, as noted earlier, not all behavior patterns originate exogenously; many common

patterns have a spontaneous, endogenous origin Axons may be branched; synapses may be

convergent or divergent; temporal or spatial summation of impulses may occur at synapses;

neurons may be excitatory or inhibitory in their effects Thus, an enormous number of

potential routes are open to impulses generated by a given set of stimuli The eventual

routes taken and, therefore, the motor responses that follow, depend on the size, nature, and

frequency of these stimuli

2.4 Learning and Memory

The translation of sensory input into a motor response takes place within a matter of

milliseconds and thereby fits well into the broad definition of “nervous control.” However,

another important aspect of neural physiology is learning, which, along with the related

event, memory, may occupy time intervals measured in hours, days, or even years Learning

is the ability to associate one environmental condition with another; memory is the ability

to store information gathered by sense organs Within this broad definition of learning,

several phenomena can be included Habituation, perhaps the simplest form of learning, is

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adaptation (eventual failure to respond) of an organism to stimuli that are not significant toits well-being For example, as noted above, a cockroach normally shows a striking escapereaction when air is blown over the cerci If, however, this treatment is continued for a period

of time, the insect eventually no longer responds to it Conditioning is learning to respond

to a stimulus that initially has no effect Related to this is trial-and-error learning where

an animal learns to respond in a particular way to a stimulus, having initially attempted torespond in other ways for which acts it received a negative reaction

The most complex form of learning in insects, latent learning, is the ability to relatetwo or more environmental stimuli, though this does not confer an immediate benefit Forinsects, visual and chemosensory (especially olfactory) cues are especially important in

latent learning For example, Microplitis spp learn to associate color, shape, and pattern with successful oviposition; Locusta associates odor or visual cues with food quality; and

mosquitoes learn to recognize (and return to) sites where they have successfully fed and/oroviposited (McCall and Kelly, 2002) Perhaps the best-studied example of latent learning isthe recognition and use of landmarks by social Hymenoptera, enabling these insects to return

to their nest or a food source Foraging honey bees, wasps, and ants, on leaving a newlydiscovered food source, undertake a series of “turn-back-and-look” (TBL) manoeuvres(Lehrer, 1991; Judd and Collett, 1998; Lehrer and Bianco, 2000) In this activity the insect,when just a few centimeters from the food source, repeatedly turns and looks back at it.Likewise, inexperienced workers carry out similar learning flights on first leaving the nest

to forage It has been proposed that the TBL activity enables the insect to take a series of

“snapshots” of the landmarks adjacent to the food source or nest These pictures, memorizedwithin the optic lobes, are then matched with the current image seen on the next trip Whenthe match is “exact,” the insect has reached its goal

As noted, the TBL method facilitates “close-up” landmark recognition However, nition of landmarks is often also used as insects move between the nest and a food source.For example, insects may learn to steer to one side of a landmark to stay on the correctpath; they may go directly over landmarks that are on the flight path; and by recognizing(matching) a scene, they are able to compensate for unexpected displacement of their po-sition provided that they have experienced the “new” position at a previous point in time(Collett, 1996)

recog-It is not always possible to use landmark recognition to navigate between nest andfood source as the terrain may be featureless Under such conditions, path integration isemployed (Collett and Collett, 2000) Essentially, path integration requires that an insecthas the ability to monitor and record changes in its position over time, that is, to measuredistance traveled, speed of travel, and direction traveled The insect must then compute thisinformation to set (or reset) a course toward the nest or food source For many insects, pathintegration incorporates the insect’s ability to navigate using polarized light (Chapter 12,Section 7.1.4), including a mechanism for measuring and compensating for elapsed time,necessitated by the sun’s ever-changing position

Circadian rhythms are also a form of learning Many organisms perform particularactivities at set times of the day, and these activities are initially triggered by a certainenvironmental stimulus, for example, the onset of darkness Even if this stimulus is removed,

by keeping an animal in constant light or dark, the activity continues to be initiated at thenormal time

Though there is no doubt that insects are able both to learn and to memorize, thephysiological/molecular basis for these events is not known However, some generalizedstatements can be made The mushroom bodies are the center where complex behavior is

NERVOUS AND CHEMICAL INTEGRATION

learned, and, these structures occupy a relatively greater proportion of the brain volume in

insects such as the social Hymenoptera (particularly the worker caste), which exhibit the

greatest learning capacity A group of pacemaker cells responsible for the generation of

circadian rhythms in Drosophila have been identified in the central brain (Saunders, 1997).

There is evidence that simpler forms of learning can occur in other ganglia, for example,

those of the thorax Headless insects and even individual, isolated thoracic ganglia

prepa-rations can learn to keep a leg in a certain position so as to avoid repeated electric shocks

Intact animals retain this ability for several days after the training period whereas in headless

insects the retention time is only 1–2 days However, subsequent removal of the head of

insects that have learned while intact does not reduce retention time, suggesting that intact

animals learn more readily than headless ones or isolated ganglia A variety of

pharmaco-logical experiments have been undertaken in attempts to establish the molecular basis of

learning and memory, including application of protein or nucleic acid synthesis-inhibiting

drugs, assays of protein and nucleic acid synthesis in ganglia before and after training,

measurement of cholinesterase levels, and application of cyclic AMP inhibitors However,

the results obtained are sometimes conflicting and difficult to interpret (see Eisenstein and

Reep, in Kerkut and Gilbert, 1985)

3 Endocrine System

Insects, like vertebrates, possess both epithelial endocrine glands (the corpora allata and

molt glands, derived during embryogenesis from groups of ectodermal cells in the region of

the maxillary pouches) and glandular nerve cells (neurosecretory cells), which are found in

all ganglia of the central nervous system and in parts of the visceral nervous system Their

axons terminate in storage and release sites (neurohemal organs) or run directly to their

target organ In addition, the gonads and some other structures of certain species produce

hormones

The functions of hormones are many, and discussion of these is best treated in

con-junction with specific physiological systems In this chapter, therefore, only the structure

of the glands, the nature of their products, and the principles of neuroendocrine integration

will be examined

3.1 Neurosecretory Cells and Corpora Cardiaca

The best-studied neurosecretory cells are the median neurosecretory cells (mNSC) of

the protocerebrum They occur in two groups, one on each side of the midline, and their axons

(which form the NCC I) pass down through the brain, crossing over en route, and normally

terminate in a pair of neurohemal organs, the corpora cardiaca, where neurosecretion is

stored (Figure 13.4) In some species, for example, Musca domestica, some neurosecretory

axons do not terminate in the corpora cardiaca but pass through them to the corpora allata In

many Hemiptera-Heteroptera, the axons bypass the corpora cardiaca and, instead, terminate

in the adjacent aorta wall In aphids, some neurosecretory axons transport their product

directly to the target organ And the axons of the mNSC which produce bursicon terminate in

the fused thoracoabdominal ganglion of higher Diptera and in the last abdominal ganglion of

cockroaches and locusts (Highnam and Hill, 1977) The corpora cardiaca are closely apposed

to the dorsal aorta into which neurosecretion and intrinsic products of the corpora cardiaca

are released when the neurosecretory cell membranes are depolarized The NCC I also

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contain ordinary neurons that innervate the intrinsic cells of the corpora cardiaca (see below),causing them to release their product More than 40 years ago, it was noted that different

mNSC take up characteristic stains Further, destruction of the cells affects a wide range

of physiological processes (see later chapters), leading to the proposal that they produce

a variety of hormones This was confirmed through the use of immunohistochemistry,following purification of specific neurosecretory hormones Also in the protocerebrum are

two groups of lateral neurosecretory cells (lNSC) whose axons do not cross but travel to

the corpus cardiacum of the same side However, there is almost no information on theirfunction

The corpora cardiaca arise as invaginations of the foregut during embryogenesis at thesame time as the stomatogastric nervous system and are, in fact, modified nerve ganglia.Though their main function is to store neurosecretion, many of their intrinsic cells alsoproduce hormones In some species, for example, the desert locust, the neurosecretorystorage zone and glandular zone (zone of intrinsic cells) are distinct (Figure 13.4C–E); inothers, the neurosecretory axons terminate among the intrinsic cells

Neurosecretory cells are also found in all of the ventral ganglia, and their axons, whichcontain stainable droplets, can be traced to a series of segmental neurohemal organs, theperisympathetic organs adjacent to the unpaired ventral nerve In addition, there are manyreports of multipolar neurosecretory cell bodies lying on peripheral nerves innervating theheart, gut, etc However, it should be noted that, for both the neurosecretory cells of theventral ganglia and those associated with peripheral nerves, only rarely has experimentalevidence for their function been obtained

Many functions have been ascribed to neurosecretory hormones and the intrinsic mones produced by the corpora cardiaca, but for relatively few of these is there good experi-

hor-mental evidence Products of the mNSC include prothoracicotropic hormone (PTTH), which

activates the molt glands (Chapter 21, Section 6.1); allatotropic and allatostatic hormones,whose primary function is to regulate the activity of the corpora allata (Chapter 19, Sec-tion 3.1.3 and Chapter 21, Section 6.1); diuretic hormone, which affects osmoregulation(Chapter 18, Section 5); ovarian ecdysiotropic hormone (OEH) (formerly egg developmentneurosecretory hormone) (Chapter 19, Section 3.1.3); ovulation- or oviposition-inducinghormone (Chapter 19, Sections 5 and 7.2); and testis ecdysiotropin (TE) (Chapter 19, Sec-tion 3.2) Bursicon, which is important in cuticular tanning (Chapter 11, Section 3.4), hasbeen localized in the mNSC in some species, though is principally found in the abdom-inal ganglia from which it is released via abdominal perivisceral organs Neurosecretion

from the mNSC also affects behavior, though in many cases this is certainly an indirect

action, and is important in protein synthesis Eclosion hormone (EH), important in ecdysis(Chapter 21, Section 6.2), is produced by neurosecretory cells in the tritocerebrum Theintrinsic cells of the corpora cardiaca produce hyperglycemic and adipokinetic hormones(AKH) important in carbohydrate and lipid metabolism (Chapter 16, Sections 5.2 and 5.3)and hormones that stimulate heartbeat rate (Chapter 17, Section 3.2), gut peristalsis, andwrithing movements of Malpighian tubules It appears, however, that the mNSC may beinvolved in the elaboration of these materials because extracts of these cells exert simi-lar, though less strong, effects on these processes Neurosecretion from the subesophagealganglion is, in cockroaches, synthesized and released regularly and controls the circadianrhythm of locomotor activity In many female moths, pheromone biosynthesis activatingneuropeptide (PBAN) (Section 4.1) is produced in three groups of neurosecretory cells inthe subesophageal ganglion (in some species also other ventral ganglia) The PBAN syn-thesized in the subesophageal ganglion appears to be released via the corpora cardiaca In

NERVOUS AND CHEMICAL INTEGRATION

FIGURE 13.6. (A) Locust juvenile hormone (C16JH = JHIII); and (B) β-ecdysone.

female pupae* of Bombyx, two large neurosecretory cells in the subesophageal ganglion

produce a diapause hormone which promotes the development of eggs that enter diapause

(see Chapter 22, Section 3.2.3) In Rhodnius, diuretic hormone is produced not by the

cere-bral neurosecretory cells but by the hindmost group of neurosecretory cells in the fused

ganglion of the thoracic and first abdominal segments

All neurosecretory factors characterized to date are peptides (sometimes glycosylated),

an observation that is entirely in keeping with those from other animals They range in

molecular weight from the tens of thousands down to a thousand or less Examples are

bur-sicon (M.W about 40,000), diuretic hormone (M.W 1500–2000), OEH (6500), TE (2500),

diapause hormone (2500), and AKH (a decapeptide) The PTTH of Drosophila is a

gly-cosylated polypeptide (M.W 66,000) Curiously, the moth Manduca sexta produces two

forms of PTTH: the smaller form (M.W 7000) comes from the mNSC, whereas the larger

form (M.W 28,000) is a product of the lNSC The two forms have quite different structures,

yet in larvae are about equally active

3.2 Corpora Allata

Typically the corpora allata are seen as a pair of spherical bodies lying one on each

side of the gut, behind the brain (Figure 13.4A,B) However, in some species, the glands

may be fused in a middorsal position above the aorta, or each gland may fuse with the

corpus cardiacum on the same side In larvae of cyclorrhaph Diptera the corpora allata,

corpora cardiaca, and molt glands fuse to form a composite structure, Weismann’s ring,

which surrounds the aorta Each gland receives a nerve (NCA I) from the corpus cardiacum

on its own side, though the axons that form this nerve are probably those of mNSC, and

also a nerve from the subesophageal ganglion (NCA II)

The corpora allata produce a hormone known variously as juvenile hormone,

metamorphosis-inhibiting hormone, or neotenin, with reference to its function in

juve-nile insects (Chapter 21, Section 6.1), and gonadotropic hormone to indicate its function

in adults (Chapter 19, Sections 3.1.3 and 3.2) Juvenile hormone is a terpenoid compound

(Figure 13.6A) and, to date, six naturally occurring forms (JH-O, JH-I, 4-methyl-JH-I,

JH-II, JH-III, and JHB3) have been identified In all insects investigated, except Hemiptera,

Lepidoptera, and higher Diptera, only JH-III has been obtained Though JH-III is reputedly

synthesized in some Hemiptera, Numata et al (1992) report that JH-I is the only form

produced in the bean bug, Riptortus clavatus In Lepidoptera the first five forms of JH listed

* In many Lepidoptera, including Bombyx, egg development begins in the pupa.