Summary
The paired lanterns of the larval fireflyPhoturis versicolor are bilaterally innervated by four dorsal unpaired median (DUM) neurons the somata of which are found in the terminal abdominal ganglion (A8) and which stain with Neutral Red (Fig. 1A). Both intra- and extracellularly recorded activity in these neurons is always associated with a bilateral glow response, or BGR (Figs. 3 and 4). Luminescence cannot be initiated or maintained in the absence of DUM neuron excitation. Furthermore, there is a linear causative relationship between the frequency of DUM neuron activity and the amplitude of the resultant BGR (Figs. 6 and 7).
Due to the intrinsic bilateral morphology, firefly DUM neurons may be antidromically activated through either lantern nerve, resulting in the initiation of luminescence in the contralateral lantern (Figs. 8 and 9). This activation is unaffected by high Mg++ saline indicating that the DUM neurons provide a direct pathway for conduction through the ganglion (Fig. 9). The DUM neurons receive synaptic input from axons descending through both anterior connectives, however, stimulation of only one connective results in a BGR since excitation is carried to both sides of the periphery through the bilateral axons.
Firefly DUM neurons exhibit physiological qualities typical of neurosecretory cells: spikes are characterized by a slow time course and a long and deep afterhyperpolarization (Fig. 10). This is consistent with the observation that spontaneous firing rates are usually below 3 Hz, but nevertheless elicit a strong BGR (Figs. 3 and 5). The physiological evidence presented in this study correlates well with the morphological, pharmacological and biochemical evidence compiled from previous studies, which indicates that the four DUM neurons represent the sole photomotor output from the central nervous system to the larval lanterns. Evidence is discussed which indicates that these effects are mediated throught the release of octopamine, long presumed to be the lantern neurotransmitter. These results, therefore, describe a novel and unexpected role for DUM neurons in regulating an unusual invertebrate effector tissue and further expands the growing list of functions for octopamine in neural control mechanisms.
Similar content being viewed by others
Abbreviations
- A1-A7 :
-
first through seventh abdominal ganglia
- A8 :
-
terminal abdominal ganglion
- DUM :
-
dorsal unpaired median
- BGR :
-
bilateral glow response
References
Bennett MVL (1972) Neuronal control of smooth muscle. In: Bennett MVL (ed) Autonomic neuromuscular transmission. Cambridge University Press, London New York, pp 217–235
Bentley DR (1973) Postembryonic development of insect motor systems. In: Young D (ed) Developmental neurobiology of arthropods. Cambridge University Press, London New York, pp 147–177
Buck J, Case JF (1961) Control of flashing in fireflies. 1. The lantern as a neuroeffector organ. Biol Bull 121:234–256
Carlson AD (1968a) Effect of adrenergic drugs on the lantern of the larvalPhoturis firefly. J Exp Biol 48:381–387
Carlson AD (1968b) Effect of drugs on luminescence in larval fireflies. J Exp Biol 49:195–199
Carlson AD (1981) Neural control of the malePhoturis versicolor firefly flash. J Exp Biol 92:165–172
Case JF, Strause LG (1978) Neurally controlled luminescent systems. In: Herring PJ (ed) Bioluminescence in action. Academic Press, London, pp 331–366
Chang JJ (1956) On the similarity of response of muscle tissue and of lampyrid light organs. J Cell Comp Physiol 47:489–492
Christensen TA (1980) Identified DUM neurons in the firefly: Morphology, physiology and control of the lantern. Neurosci Abstr 6:370
Christensen TA, Carlson AD (1981a) Symmetrically organized dorsal unpaired median (DUM) neurones and flash control in the male firefly,Photuris versicolor. J Exp Biol 93:133–147
Christensen TA, Carlson AD (1981b) Evidence for non-modulatory octopaminergic transmission mediating luminescence in larval fireflies. Neurosci Abstr 7:413
Crossman AR, Kerkut GA, Pitman RM, Walker RJ (1971) Electrically excitable nerve cell bodies in the central ganglia of two insect speciesPeriplaneta americana andSchistocerca gregaria. Investigation of cell geometry and morphology by intracellular dye injection. Comp Biochem Physiol [A] 40:579–594
Davis NT, Alanis J (1979) Morphological and electrophysiological characteristics of a dorsal unpaired median neuron of the cricket,Acheta domesticus. Comp Biochem Physiol [A] 62:777–788
Downer RGH (1979) Induction of hypertrehalosemia by excitation inPeriplaneta americana. J Insect Physiol 25:59–63
Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317–473
Evans PD, O'Shea M (1977) The identification of an octopaminergic neuron which modulates neuromuscular transmission in the locust. Nature 270:257–259
Evans PD, O'Shea M (1978) The identification of an octopaminergic neurone and the modulation of a myogenic rhythm in the locust. J Exp Biol 73:235–260
Ghiradella H (1977) Fine structure of the tracheoles of the lantern of a photurid firefly. J Morphol 153:187–204
Ghiradella H (1978) Reinforced tracheoles in three firefly lanterns: Further reflections on specialized tracheoles. J Morphol 157:281–300
Gole JWD, Downer RGH (1979) Elevation of adenosine 3′,5′-monophosphate by octopamine in fat body of the american cockroach,Periplaneta americana L. Comp Biochem Physiol [C] 64:223–226
Goodman CS, Spitzer NC (1979) Embryonic development of identified neurones: differentiation from neuroblast to neurone. Nature 280:208–214
Heitier WJ, Goodman CS (1978) Multiple sites of spike initiation in a bifurcating locust neuron. J Exp Biol 76:63–84
Hess WN (1922) Origin and development of the lightorgan ofPhoturispennsylvanica DeGeer. J Morphol 36:245–277
Hoyle G (1975) Evidence that insect dorsal unpaired median (DUM) neurones are octopaminergic. J Exp Zool 193:425–431
Hoyle G (1978) The dorsal, unpaired, median (DUM) neurons of the locust metathoracic ganglion. J Neurobiol 9:43–57
Hoyle G, Dagan D (1978) Physiological characteristics and reflex activation of DUM (octopaminergic) neurons of locust metathoracic ganglion. J Neurobiol 9:59–79
Hoyle G, Dagan D, Moberly B, Colquhoun W (1974) Dorsal unpaired median insect neurons make neurosecretory endings on skeletal muscle. J Exp Zool 187:159–165
Hoyle G, Colquhoun W, Williams M (1980) Fine structure of an octopaminergic neuron and its terminals. J Neurobiol 11:103–126
Matthews JR, Downer RGH (1974) Origin of stress-induced hyperglycaemia in the american cockroach,Periplaneta americana. Can J Zool 52:1005–1010
Nathanson JA (1977) Cyclic nucleotides and nervous system function. Physiol Rev 57:157–256
Nathanson JA, Hunnicutt EJ (1979) Neural control of light emission inPhoturis larvae: identification of octopamine-sensitive adenylate cyclase. J Exp Zool 208:255–262
Nelson S, Carlson AD, Copeland J (1975) Mating-induced behavioural switch in female fireflies. Nature 255:628–629
Oertel D, Case JF (1976) Neural excitation of the larval firefly photocyte: slow depolarization possibly mediated by a cyclic nucleotide. J Exp Biol 65:213–227
Oertel D, Linberg KA, Case JF (1975) Ultrastructure of the larval firefly light organ as related to control of light emission. Cell Tissue Res 164:27–44
Orchard I, Loughton BG, Webb RA (1981) Octopamine and short-term hyperlipaemia in the locust. Gen Comp Endocrinol 45:175–180
O'Shea M, Evans PD (1979) Potentiation of neuromuscular transmission by an octopaminergic neurone in the locust. J Exp Biol 79:169–190
Peterson MK (1970) The fine structure of the larval firefly light organ. J Morphol 131:103–116
Peterson MK, Buck J (1968) Light organ fine structure in certain asiatic fireflies. Biol Bull 135:335–348
Plotnikova SI (1969) Effector neurons with several axons in the ventral nerve cord of the Asian grasshopperLocusta migratoria. J Evol Biochem Physiol 5:276–278
Robertson HA, Carlson AD (1976) Octopamine: presence in firefly lantern suggests a transmitter role. J Exp Zool 195:159–164
Smith DS (1963) The organization and innervation of the luminescent organ in a firefly,Photuris pennsylvanica (Coleoptera). J Cell Biol 16:323–359
Stewart WW (1978) Functional connections between cells as revelaed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759
Stuart AE, Hudspeth AJ, Hall ZW (1974) Vital staining of specific monoamine-containing cells in the leech nervous system. Cell Tissue Res 153:55–61
Usherwood PNR (1967) Insect neuromuscular mechanisms. Am Zool 7:553–582
Wallace BG, Talamo BR, Evans PD, Kravitz EA (1974) Octopamine: selective association with specific neurons in the lobster nervous system. Brain Res 74:349–355
Zorn LP, Carlson AD (1978) Effect of mating on response of femalePhoturis firefly. Anim Behav 26:843–847
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Christensen, T.A., Carlson, A.D. The neurophysiology of larval firefly luminescence: Direct activation through four bifurcating (DUM) neurons. J. Comp. Physiol. 148, 503–514 (1982). https://doi.org/10.1007/BF00619788
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00619788