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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. 1155 1156 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 1158 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- 1160 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 1162 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. 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