Download Sensory Regeneration in Arthropods: Implications of Homoeosis

AMER. ZOOL., 28:1155-1164 (1988)
Sensory Regeneration in Arthropods: Implications of
Homoeosis and of Ectopic Sensilla1
JOHN S. EDWARDS
Department of Zoology, University of Washington,
Seattle, Washington 98195
SYNOPSIS. The seemingly antithetic attributes of rigorous connectivity on one hand and
vigorous regeneration on the other, are combined in the arthropod nervous system. This
apparent paradox is largely resolved by the comparison of normal postembryonic development with regeneration, which is also restricted to immature stages. It is also becoming
apparent that growth and interaction between neurons is more flexible than had been
assumed.
Normal sensory regeneration in situ is highly specific in restoring lost function. The
crucial event in regeneration, as in embryonic development, is the establishment of first
contacts between periphery and center. Thereafter regeneration follows an accelerated
recapitulation of normal postembryonic development.
Data from ectopic grafts, homoeotic mutants, and homoeotic regenerates address four
components of sensory development and regeneration: a) Positional information in the
epidermis determines receptor type and central projection, b) Passage from periphery to
ganglion is non-specific. Ectopic neurons reach mismatched ganglia, c) Within neuropile
the specific projection is a product of interaction between intrinsic programs of the neuron
and pathways expressed as specific surface markers, d) Fine tuning of synaptic relationships
can occur in response to changed milieu. The current elucidation of the genetic basis of
metameric segment determination, and the identification of specific gene products as
markers of pathways open the way to the understanding of neural specificity in development and regeneration at the molecular level.
The seeming paradox of rigorous connectivity
versus vigorous regeneration in
An element of paradox was there, virtually unnoticed, for decades: arthropods arthropods is partially resolved with the
have long had the reputation for fixity of recognition that much of the normal develneural function and yet they were cele- opment of the arthropod is post-embrybrated for their capacity to replace lost onic. Regeneration, too, is restricted to the
parts. Lost parts generally include nerves sequence of post-embryonic molts which
and because regenerated parts generally successively add increasing numbers of
get to function appropriately, they must sensory cells, each growing to the CNS and
have regenerated appropriate neural con- making new synapses. Sensory regeneranections, be they sensory, motor, or both. tion recapitulates and accelerates normal
New synapses must have been formed. ontogeny. The crucial event is in the pasThen, superimposing the conceptual sage of the first regenerating neurons
framework of the fixed, parsimonious ner- through the post-embryonic landscape.
vous system, tightly wired for fixed action Once connection is achieved the normal
patterns, upon the capacity for neural spatial and temporal determinants of proregeneration, it was arguable that arthro- jection are evidently activated. Regenerpods must manifest the tightest specificity ating motor nerves, on the other hand, are
in restoring neural connections. They were faced with the process of cell recognition
thus seen as a source of model systems for in the periphery (Denburg, 1988) but centhe analysis of regeneration that might tral connections need not be reworked, for
stand in instructive contrast with the com- the number of motor neurons remains constant during larval development; growth is
plex and flexible vertebrates.
by volume. It is true that the massive reorganisation of the nervous system at meta1
morphosis in Holometabola involves the
From the Symposium on Nervous System Regeneration in the Invertebrates presented at the Annual Meet- death of sensory and motor nerves, the
ing of the American Society of Zoologists, 27-30 remodeling of some motor nerves, the regPERSPECTIVE
December 1986, at IVashville, Tennessee.
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JOHN S. EDWARDS
ulated revival of neuroblasts and the differentiation of new sensory structures from
imaginal disks, but throughout this process
cellular continuity is maintained between
periphery and center; adult sensory and
motor neurons follow preexisting paths
(Edwards, 1969; Bate, 1978).
None of the developmental patterns cited
above significantly challenge the implied
rigid specificity within the invertebrate
CNS and this reputation is still widely
accepted (e.g., Easter et al., 1985). The last
few years have, however, seen a changing
view of fixity in the arthropod nervous system. Metabolic, behavioral and developmental studies have increasingly revealed
adaptive change in the CNS, and fixity of
connectivity is being reassessed (Edwards
etal., 1984; Palka, 1985; Murphey, 1986).
What seemed a relatively rigid and unresponsive system is proving to be quite flexible and reactive, and it has become clear
that earlier emphasis on the capacity to
regenerate highly specific functional connections during normal regeneration
tended to underestimate or overlook the
capacity of neurons in the CNS for active
response to changed milieu and of peripheral nerves to be somewhat flexible in their
growth patterns and synaptic distribution
(Murphey, 1985).
Plasticity notwithstanding, the emphasis
here will be on approaches to the general
mechanisms by which regenerating sensory neurons, arising de novo in regenerated structures establish functional central
connections. Some topics arising from
experimental manipulations of sensory
nerves are discussed below. Not all are
immediately concerned with regeneration
but, together with the changing evaluation
of rigidity in neural architecture in arthropods alluded to above, they provide materials for a contemporary view of pathway
selection in sensory regeneration by
arthropods.
sory regeneration. In essence all experimental approaches to pathway selection are
based on the analysis of responses to altering the location or form of peripheral
receptors and exploring the consequences
for the modified neurons as they seek (or
are guided to) central targets.
Three main variants of this general protocol are available: 1) the creation of ectopic
grafts of limbs or selected sensilla; 2) the
use of homoeotic mutants; and 3) the use
of heteromorphic (homoeotic) regenerates.
ECTOPIC GRAFTS
Because sensory neurons survive transplantation along with the surrounding
integument, their capacity to grow to central targets, and the pathways taken by
newly formed sensory neurons formed
within the grafted epidermis are open to
investigation. Entire or partial appendages
or areas of integument can be transplanted
in arthropods. Transplants survive well and
become incorporated into the host site. An
extensive literature on such grafts provides
the basis for models of pattern formation
in the integument (French et al., 1976;
Palka, 1979) which depend on the capacity
of epidermal cells to sense their place in
the context of the two dimensional monolayer of epidermal cells. Epidermal cells
are born in that context and it evidently
determines the character of specialised
cells, including sensilla and associated
afferent neurons that are generated from
epidermal cells. The question then arises
of the mechanism by which their sensory
axons reach appropriate central target
interneurons. It is now well established that
in normal post-embryonic development
successive additions of new sensory axons,
produced during each stadium, follow
existing nerves to the CNS where they terminate on growing interneurons. Original
pathways are established in the embryo by
pioneer fibres whose behavior in the
periphery is now well documented, and
PATH SELECTION IN THE PERIPHERY
while emphases differ, depending on the
The organisation of the arthropod ner- system under observation, there is general
vous system, with its sensory cells in periph- agreement that pathways from the peripheral location where they differentiate from ery to the CXS are built by pioneer fibres
epidermal cells, confers a prim a facie sim- that follow stereotyped routes. They are
plicity to the experimental analysis of sen-
SENSORY REGENERATION IN ARTHROPODS
1157
able to recognise specific guide cells or epithelial pathways based on differential
adhesivity or recognition molecules (Bastiani et al., 1986; Palka, 1986).
The key question for understanding the
process of regeneration is how post-embryonic neurons, arising de novo and deprived
of their normal contact guidance cues, can
reach appropriate central contacts. It has
been known for some years that regenerates developing in situ can indeed exactly
restore specific functional connections,
even in late post-embryonic development
after prolonged absence of an appendage
(Edwards et al, 1974; Palka et al., 1974).
Cues must therefore exist for the first sensory axons to leave the newly formed epidermis of the blastema and traverse postembryonic territory to reach the CNS. The
behavior of the pioneer regenerate neurons remains to be fully documented; it
seems that they grow beyond the periphery
of the blastema and there pick the first
intact neural pathway to the CNS that they
encounter. They have not so far been
observed in the initial stages of outgrowth,
but contact guidance appears to be the cue,
for regenerating nerves invariably grow to
the native ganglion in preference to
implanted target ganglia situated closer to
the blastema (McLean et al., 1976). For the
regenerate or implanted sensory axon it
seems that any pathway to the CNS will do.
But that does not guarantee successful contact with CNS targets.
implanting a younger cercus does not prevent a normal topographic projection by
regenerating axons. At least in this system
relative age of center and periphery does
not hinder specific regeneration (Palka et
al., 1974; Murphey et al., 1981). Cerci can
also be grafted ectopically to leg stumps.
Their sensory neurons grow to the nearest
segmental ganglion, where their synaptic
connections elicit action potentials in giant
interneurons when cereal mechanoreceptors are stimulated (Edwards et al., 1967).
It was originally thought that connections
were made with the more anterior regions
of the same giant interneurons (the MGI
and LGI) whose normal input from cereal
mechanoreceptors occurs in the terminal
abdominal ganglion. Subsequent more
refined analysis showed however that the
connections are not with the original target cells but with others of the giant fiber
population (Murphey et al., 1983). The
specificity of the cereal mechanoreceptor
neurons proved to be less rigid than had
been thought. The latter study not only
showed that the cereal afferents failed to
connect with their normal target cells when
they encountered them outside the normal
milieu of the terminal ganglion, perhaps
because of the absence of potential sites
for input, but also demonstrated that the
cereal nerve projection in thoracic segments was consistent in organisation and
preserved spatial relationships in each thoracic ganglion as if responding to segmentally repeated cues.
CENTRAL PATHWAYS
More sensitive tests of projection patterns come from transplants of specific sensilla rather than whole appendages. A clear
demonstration that cues concerning location in the periphery impart positional
information which in turn determines the
character of the sensory axon as evaluated
by its pattern of central projection, came
from the transplantation of different types
of wind-sensitive hairs on the head of the
locust (Anderson, 1985). Reciprocally
transplanted neurons grew to the CNS via
the nerve normally followed from the host
site, but developed a central arborization
in the subesophageal ganglion characteristic of their site of origin. When transplanted to thoracic segments the head hair
Having reached a central ganglion by
the nearest intact route, how do regenerating axons find their targets? The efficacy
of transplantation surgery opens many possibilities for testing the response of sensory
neurons to changed environments. The
abdominal cerci of Ache ta discussed above
provide relevant examples. Cut sensory
axons regenerate when a cercus is reimplanted, or transposed from left to right
and in most cases neurons reach their
appropriate ipsilateral target, even through
they approached their terminals by altered
routes (Murphey?/ al., 1981). Further, age
mismatch of regenerates achieved by causing partial (distal) regeneration or by
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JOHN S. EDWARDS
neurons found their way to the nearest segmental ganglion but there made no functional connections with the appropriate
giant interneurons (Anderson, 1985).
The cricket cercus has, in the hands of
Murphey and colleagues (Walthall et al.,
1986) provided a clear and elegant demonstration of the role of difFerentiative
events in the integument as determinants
of specificity in central projection. Based
on cell-by-cell resolution of the somatotopic map of cereal receptors within the
cereal glomerulus of the terminal ganglion, and taking advantage of pigment differences between compatible cricket species
to distinguish implant from host integument, projections of ectopic sensilla and of
new-formed sensilla in the graft-host interface zone were mapped. It was shown that
positional information at the site of differentiation of a sensillum from an epidermal
precursor cell determines the character of
the central projection.
Transplantation of imaginal disks in
Holometabola also provides an instructive
source of ectopic sensory structures. The
importance of segmental organisation and
serial homology is emphasised by recent
work in which imaginal disks of Drosophila
were transplanted to ectopic sites on the
abdomen (Stocker et al., 1985; Schmid et
al., 1986). Sensory axons arising from these
grafts enter the CNS at metamorphosis
through the main abdominal nerve, and
terminate in abdominal and thoracic neuropile. It is thus possible to move sensory
structures to segments far from their
normal sites, and since dorsally situated
appendages, e.g., wings, have characteristically different patterns of central projection than ventral appendages, e.g., legs, it
is possible to test for the effect of interchanging position on the dorso-ventral axis
of a given segment. The results are complex but it is clear that sensory axons arising from homologous transplants generate
similar central projections, while those
from heterologous (i.e., ventral to dorsal
and vice versa) transplants do not. The
results are consistent with a model in which
the homologous appendages on the one
hand and the segmental central targets on
the other share serially repeated surface
markers.
HOMOEOSIS AND NEURAL
SPECIFICITY
Transplants are not the only approach
open to the analysis of neuronal growth.
Nature offers the developmental neurobiologist a range of ectopic sensory neurons in arthropods, either as developmental mutants or as the consequence of
misdirected differentiation of regenerates.
The term homoeosis was coined by Bateson (1894) to denote the replacement of
one member of the segmental series of
appendages by another of the series.
HOMOEOTIC MUTANTS
Homoeotic mutants are best known from
the Drosophila series, but they also occur in
other pterygote insects (Ouweneel, 1976),
e.g., the so-called prothoracic wingflaps of
the cockroach Blatella germanica (Ross,
1964), the labiopedia mutant of Tribolium
confusum in which the labial legs are said
to be fully differentiated, with normal musculature (Daly and Sokoloff, 1965) and in
lepidopteran larvae where thoracic legs
develop on abdominal segments (Tanaka,
1953; Booker and Truman, 1986). In all
such mutants an appendage is replaced by
another from the homologous segmental
series. As such they provide the neurobiologist with a range of ectopic sensilla
that send afferent fibers to the CNS in
abnormal segmental contexts.
It was first shown that afferent fibers
from the mesothoracic leg that replaces the
antenna in the homoeotic mutant Antennapedia of Drosophila terminate in the
antennal glomerulus of the brain, essentially as do normal antennal sensilla, except
that the mutant projection is ipsilateral,
while the normal projects to both centers
(Stocker et al., 1976). Similar results were
obtained with another mutant, Spineless
aristapedia, in which distal parts of the
antenna are transformed to tarsus. Again,
the projection of sensory neurons corresponded to that of antennal fibers, with the
exception of a novel projection to the proboscis center in the sub-esophageal gan-
SENSORY REGENERATION IN ARTHROPODS
1159
glion (Stocker and Lawrence, 1981). The is the haltere, a club shaped sensory
anatomical results are consistent with the organ of equilibration. In certain bithorax
interpretation that sensory neurons of mutants the haltere is transformed into a
transformed ectopic appendages recognise wing, from which mechanoreceptors reach
the central pathways of the relevant seg- the thoracic ganglia through the normal
ment. It is, however, tantalising to find that metathoracic point of entry. From there
contact stimulation of the homoeotic tarsi on, within the neuropile, three types of
with sugar solution evokes the proboscis projections are recognised. Axons that
extension feeding reflex as do normal tho- originate from sensilla with no obvious
racic tarsi, but not normal antennae (Deak, homolog on the haltere either form a local1976; Stocker, 1977). A potential source ised bushy projection in metathoracic neuof input to the proboscis center has been ropile comparable to that associated with
shown anatomically in Spineless aristapedia, the normal wing in the mesothoracic neubut not in Antennapedia.
ropile, or follow the same longitudinal paths
In a further temperature sensitive as their mesothoracic counterparts except
homoeotic mutant involving head append- that they enter them from the posterior,
ages, proboscipedia, the proboscis is trans- as if they read their guide book backwards.
formed into a tarsus or an arista (an anten- A second category of sensillum which is
nal structure), depending on ambient represented on both wings and halteres, is
temperature during development. The associated with axons that project as if they
ectopic tarsal and aristal neurons reach the came from haltere sensilla. There are comsuboesophageal ganglion, via the labial or plexities, beyond the scope of this paper,
neighboring peripheral nerves. There they to the interpretation of the extent of transproject, as might be expected from the formation by bithorax genes but it is clear
foregoing, to the proboscis center as if they that the ectopic projections are orderly and
were normal proboscis sensilla, but also to repeatable, and that they show elements
the antennal glomerulus with a projection comparable to the head transformations in
pattern comparable to the homoeotic that some axons respond to a mismatched
spineless aristapedia tarsus. Overall, the ganglion as they would in their own, while
homoeotic mutants discussed above sug- others pick up plurisegmental pathways.
gest that sensory neurons from segmenGiven the fundamental role of the
tally homologous appendages recognise homoeotic genes in determining segmencentral pathways appropriate to that seg- tal identity during development (Gehring,
ment, but that does not exclude the for- 1985) and the segment-specific expression
mation of connections that override a of homoeotic genes in the CNS (Beachey
strictly segmental rule, for extra projec- etal, 1985) the prospects are good for tractions occur within the tightly fused and ing the determinants of pathway formation
compressed segments of the brain and to the molecular level (Doe and Goodman,
suboesephageal ganglion, some of which 1985).
are functional {e.g., the feeding reflex
evoked by antennapedia tarsi).
HOMOEOTIC REGENERATES
Less well known than homoeotic mutants
The bithorax homoeotic mutant series
in which segments are variously trans- are the homoeotic appendages that grow
formed to others of the three very dif- as heteromorphic regenerates when cerferent thoracic segments, or to abdominal tain arthropod appendages are severed. Of
segments, have also been explored from the numerous examples cited by Needham
the perspective of neural specificity (1965) only two have been examined from
(reviews: Palka, 1982; Palka et ai, 1982). a neurobiological point of view. One of
The value of the bithorax series stems from these, the antennule formed on a severed
the dipteran characteristic that only the eyestalk in decapod Crustacea is historinormal mesothorax bears wings while the cally significant as the first arthropod syshomologous appendage of the metathorax tem to be explored in terms of neural spec-
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JOHN S. EDWARDS
ificity (Herbst, 1896). First reported by regenerates in Carausius has been examMilne Edwards (1867), the uniramous eye- ined in several studies over the years since
stalk antennule, which mimics in form the it was first described in some detail by
external flagellum of the normal anten- Brecher (1924). Borchardt (1927), worknule, develops and forms functional cen- ing in Herbst's lab noted the absence of
tral connections when an eyestalk is sev- normal muscles in regenerates and demered and the optic ganglia are ablated onstrated neural connection with the deutocerebrum but central projections of their
(Herbst, 1896, 1917).
Lissman and Wolsky (1933) recog- sensory nerves were unknown until the
nised similarities between the behavioral present study (Edwards et al., 1986). Her
responses to stimulation of the hetero- work is of further interest in proposing that
morph antennule and those of the normal. normal antennal regeneration depends on
Their analysis was further refined in elec- an influence of Johnston's Organ, the
trophysiological studies by Maynard and aggregation of mechanoreceptors in the
Cohen (1965; Maynard, 1965) who noted second antennal segment. A parallel was
remarkably similar responses of normal and drawn with Herbst's conclusion that antenheteromorph antennules to standard stim- nule regeneration on the eyestalk of decauli, and detected deutocerebral interneu- pods arises from a dual potential of the
rons that were excited by stimulation eyestalk epidermis which under neural
of the heteromorph antennule. Hetero- influence from the optic nerve stalk is
morph stimulation elicited both a gener- directed toward compound eye formation,
alised withdrawal response and a specific but which in its absence differentiates
depression of the ipsilateral antennule. an antennule. A morphogenetic role for
They concluded that at least one afferent Johnston's Organ was subsequently disfiber component from heteromorph and proven by Urvoy (1959) and other claims
normal antennule terminated on the same for neural influence on the differentiation
interneurons, and avoided others. In the of the epidermis in regeneration, summaabsence of appropriate neuron tracing rized in Edwards (1967) are now dismethods at that time their inferences con- counted. The periphery is autonomous
cerning connections were based on behav- (Anderson et al., 1980), and other mechioral and electrophysiological observa- anisms must be sought to explain the phetions, and they stressed the difficulty of nomena of regeneration homoeosis. A
drawing such inferences without adequate remarkable feature of the otherwise fully
anatomical correlates. Sandeman and Luff formed tarsus of the heteromorph is the
(1974) similarly found specific responses to invariable absence of one tarsal segment,
electrical stimulation of crayfish hetero- a deficiency that is also characteristic of
morph antennules that were characteris- regenerate tarsi formed on legs, not only
tically antennular in character, and not in Carausius, but also in cockroaches (e.g.,
Brindley, 1898; Kunkel, 1981). While this
related to eyestalk cleaning behavior.
deficiency plays no significant part in neural
The occurrence of heteromorph legs on studies it is noted here as a challenge for
antennal stumps in the walking stick insect models of pattern formation in regenerCarausius morosus has also been known for ates since it implies shared patterns of gene
many years (Schmidt-Jensen, 1913). They activation in the differentiation of normal
arise occasionally in crowded cultures, pre- leg regenerates and of homoeotic appendsumably as a result of damage inflicted dur- ages.
ing the molt, but can be produced reliably
and with highest frequency by severing the
Central projections of the heteromorph
antenna in the mid to distal part of the nerve in Carausius have been examined by
second antennal segment (Borchardt, means of cobalt filling of sensory fibres
1927). Appropriate antennal amputation from tarsal sensilla (Edwards et al., 1986).
in hatchling walking sticks gives rise to well- These enter the olfactory lobe as a comformed leg segments by late instar and adult pact nerve similar in form, but more slenstages. The structure of antennapedia der and with fewer axons than the normal
SENSORY REGENERATION IN ARTHROPODS
antennal nerve. The majority, or perhaps
all fibres from the antennapedia heteromorph terminate in a tightly bound knot
in the region of the glomeruli of the normal antennal lobe. No trace of the very
characteristic pattern of tarsal sensillar
projection from legs to thoracic ganglia is
evident in the apparently disorganised
olfactory lobe. In this case the ectopic
afferents show no sign of autonomy in the
brain, as was also found for the aristapedia
mutant of Drosophila (Stocker and Lawrence, 1981). As in normal animals there
are no connections to the contralateral
olfactory lobe. In some heteromorph preparations however a small number of fibres
appear to emerge from the glomeruli of
the olfactory lobe and continue, sometimes
for a considerable distance within the brain,
to terminate in the region of the calyx of
the ipsilateral corpus pedunculatum, or to
wander more widely and to terminate in
lateral protecerebrum adjacent to the optic
lobes. It is possible that these wandering
fibres which, it should be stressed, are never
encountered in fills of the normal antennal
nerve, are first order interneurons that
have picked up cobalt transneuronally from
the tangle of afferent fibres rather than
primary afferents. The question remains
open but, whatever the nature of these
occasional stray fibres, we can conclude at
this stage that the great majority of afferent fibers from sensilla of the tarsal segments, which are thought to be principally
mechanoreceptors, terminate within the
olfactory lobe. So far we have found no
consistent behavioral response to mechanical stimulation of the heteromorph, but
stimulation of the normal antenna has few
consistent consequences, so the question of
whether any synaptic input arises from the
heteromorph is as yet undecided.
1161
details of projection of the eye stalk antennular heteromorph in decapods are not
known, it is clear that some afferent fibres
do make appropriate central synapses
evoking cleaning behavior, as is the case
with feeding responses evoked by chemical
stimulation of homoeotic tarsi in Drosophila.
CONCLUSIONS
Some aspects of the development and
regeneration of specific sensory projections are summarised in Figure 1.
The precision of normal neural regeneration in arthropods implies a high degree
of neural specificity, but that does not preclude a capacity for flexibility in response
to modifications of center or periphery.
The capacity to regenerate functional neuronal circuitry is closely tied to the events
of normal postembryonic development, and
this in turn to the moulting cycle (Kunkel,
1981).
Four components may be distinguished
in the process of setting up normal or
regenerated circuitry: a) Sensillar quality
and central projection patterns of sensory
neurons are determined by position in the
spatial array of the epidermis during sensillar differentiation, b) Passage from the
integument to the CNS is by contact guidance on preexisting nerves; original pathways having been set up in the embryo with
the aid of marked cells and/or regional
specification of the epidermal substrate as
proposed for vertebrates (Singer et al.,
1979). For the post embryonic regenerate
any path to a ganglion will do. Paths to
foreign ganglia get ectopic afferents to the
CNS but not necessarily to functional contacts, even when they encounter their
appropriate target cell out of context, c)
Within the central neuropile afferent fibers
obey
intrinsic programs in selecting pathData concerning the specificity of
ways.
Afferents from transplanted appendhomoeotic regenerates are sparse, as yet,
but they do imply significant similarities ages, for example, maintain consistent spawith homoeotic mutants in two respects. tial relationships when they enter foreign
First: the Carausius antennapedia regen- ganglia. Ectopic dorsal and ventral
erate projects predominantly to the anten- appendages {e.g., wings or legs of Drosophnal glomerulus, as in Drosophila; neither ila) manifest that identity when transshow any manifestation of the character- posed. On the other hand, homoeotic
istic form of the normal tarsal projection mutant appendages and heteromorphic
in thoracic ganglia. Second, while the regnerates recognise the central pathways
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JOHN S. EDWARDS
FIG. 1. Schematic representation of two adjacent
insect ganglia and associated areas of integument,
illustrating some aspects of sensory regeneration discussed in the text. A sensory neuron (S, lower right)
develops from the progeny of an epidermal cell which
also produce the cuticular sensory bristle (in this case
a mechanoreceptor) to which the dendrite of S is
attached. The identity of the sensillar components is
determined according to positional information
imparted by the epidermal monolayer (A) in which
the sensillum differentiates. The sensory axon associates by contact guidance with an axon bundle which
aggregates with embryonic pioneer fibres and which
follows surface markers to central terminations in the
neuropile of the segmental ganglion (G). Within the
neuropile the axon of S follows a plurisegmental tract
(T) from which it establishes synaptic contact with an
arborization of a specific interneuron I, whose cell
body lies in the contralateral cortex of the ganglion.
If S is destroyed during post embryonic development
a regenerate neuron arises de novo in the regenerated
epidermis. Instructed by positional information
equivalent to that of the original neuron it acquires
the same identity and its axon reaches the ganglion
by association with a nearby intact afferent bundle.
Axons from a homoeotic mutant or regenerate
appendage arising in the same region follow the pathway to equivalent regions of termination. If neuron
S is transplanted to a different relative position on
another segment (A,) a new axon is regenerated, which
responds to the ganglion (G,) as if it were in its native
ganglion, but fails to make synaptic contact with its
normal target (interneuron I) in the neuropile of that
segment. New sensory neurons formed in intercalary
epidermis between host and graft (not shown) respond
predictably to positional information at the site of
differentiation and project to neuropile N, accordingly.
followed by the homolog native to the neuropile of their segment {e.g., antennapedia
and aristopedia mutants and antennapedia
heteromorph regnerates) and project to the
segmentally appropriate center without
manifesting central patterns characteristic
of the appendage at its normal site. That
does not however exclude the possibility
that some functional contacts are formed,
as shown by the labellar feeding response
to chemical stimulation of antennapedia
tarsal receptors in Drosophila and cleaning
movements appropriate to antennules in
eyestalk heteromorphs of decapods. These
functional inputs from ectopic sensilla
occur in the brain where metameric
compression and consequent close juxtaposition of centers may provide for escape
from the strict modular organisation of
segmental ganglia. Ectopic afferents do not
necessarily make synaptic contacts with
their normal target cells when they are
encountered away from the normal context. Absence of potential post-synaptic
sites on interneurons may be decisive in
this respect, d) Fine tuning within neuropile can occur in response to changed
milieu, e.g., asymmetry, activity levels, maturation, metamorphosis.
For the future, the elucidation of the
genetic basis of segment formation and differentiation, and the potential of probes
for the detection of specific pathway markers and their genes may together provide
keys to the molecular mechanisms underlying the generation and regeneration of
specific sensory connections.
ACKNOWLEDGMENTS
My work described above was supported
by NIH grant NB07778. Dr. John Palka's
critique, especially concerning bithoracic
matters, was indispensable. I have cited
recent reviews, where relevant, in order to
condense literature citations; I apologise to
any whose work may seem to be underrepresented as a result.
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SENSORY REGENERATION IN ARTHROPODS
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