Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T09:49:26.842Z Has data issue: false hasContentIssue false
  • English
  • Français

Visual efference in Limulus: In vitro temperature-dependent neuromodulation of photoreceptor potential timing by octopamine and substance P

Published online by Cambridge University Press:  18 February 2008

CORRINNE C.M. LIM-KESSLER ,
AMANDA R. BOLBECKER ,
JIA LI  and
GERALD S. WASSERMAN
CORRINNE C.M. LIM-KESSLER
Affiliation:
Department of Psychology, Monmouth College, Monmouth, Illinois
AMANDA R. BOLBECKER
Affiliation:
Department of Psychology and Brain Science, Indiana University, Indianapolis, Indiana
JIA LI
Affiliation:
Sensory Coding Laboratory, Department of Psychological Sciences, Purdue University, Lafayette, Indiana
GERALD S. WASSERMAN
Affiliation:
Sensory Coding Laboratory, Department of Psychological Sciences, Purdue University, Lafayette, Indiana
Get access Rights & Permissions [Opens in a new window]

Abstract

Efferents from the brain of Limulus course toward its lateral eye and release octopamine and substance P into it. These neurotransmitters have previously been found to act as neuromodulators in this visual system by altering the size of its responses to light. We report here that both also modulate the timing of the receptor potentials (RPs) evoked by brief light flashes and that these timing effects are temperature dependent. Specifically: We extend our previous report that octopamine prolongs ambient RPs in a categorical fashion and here demonstrate that it does the same at colder temperatures. Categorical means that a given RP is either clearly prolonged in a dramatic fashion or its duration is otherwise unremarkable. Octopamine also accelerates the onsets of RPs when they are evoked by weak flashes under cold temperatures. Contrariwise, substance P accelerates RPs at all temperatures and this acceleration dramatically reduces the sluggishness that is otherwise typically present at low temperatures. Quantitative analysis of intensity-response functions also demonstrated that light sensitivity under substance P is significantly augmented. The plain temporal antagonism between these two modulators demonstrates that the visual system of Limulus possesses a well-poised mechanism which could be used to adjust the timing of its neural processing to interface well with the temporal characteristics of those visual stimuli that are currently present.

Keywords

IntracellularPerfusionInfusionCircadian rhythmSelective attention
Type
Research Article
Information
Visual Neuroscience , Volume 25 , Issue 1 , January 2008 , pp. 83 - 94
Copyright
© 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adolph, A.R. (1968). Thermal and spectral sensitivities of discrete slow potentials in Limulus eye. Journal of General Physiology 52, 584–599.Google Scholar
Adolph, A.R. (1973). Thermal sensitivity of lateral inhibition in Limulus eye. Journal of General Physiology 62, 392–406.Google Scholar
Armington, J.C. & Adolph, A.R. (1984). Temperature effects on the electroretinogram of the isolated carp retina. Acta Ophthalmologica 62, 498–409.Google Scholar
Astrand, K., Hamalainen, H., Alexandrov, Y. & Järvilehto, T. (1986). Response characteristics of peripheral mechanoreceptive units in man: Relation to the sensation magnitude and to the subject's task. Electroencephalography and Clinical Neurophysiology 64, 438–446.Google Scholar
Barlow, R.B., Jr. (1983). Circadian rhythms in the Limulus visual system. Journal of Neuroscience 3, 856–870.Google Scholar
Barlow, R.B., Jr., Bolanowski, S.J., Jr. & Brachman, M.L. (1977). Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science 197, 86–89.Google Scholar
Barlow, R.B., Jr., Chamberlain, S.C. & Levinson, J.Z. (1980). Limulus brain modulates the structure and function of the lateral eyes. Science 210, 1037–1039.CrossRefGoogle Scholar
Barlow, R.B., Jr., Ireland, L.C. & Kass, L. (1982). Vision has a role in Limulus mating behaviour. Nature 296, 65–66.CrossRefGoogle Scholar
Battelle, B.-A. (2002). Circadian efferent input to Limulus eyes: Anatomy, circuitry and impact. Microscopy Research and Technique 58, 345–355.CrossRefGoogle Scholar
Battelle, B.-A., Calman, B.G. & Hart, M.K. (1999). Cellular distributions and functions of histamine, octopamine, and serotonin in the peripheral visual system, brain, and circumesophageal ring of the horseshoe crab Limulus polyphemus. Microscopy Research and Technique 44, 70–80.3.0.CO;2-V>CrossRefGoogle Scholar
Battelle, B.-A. & Evans, J.A. (1982). Efferent fibers to Limulus eyes synthesize and release octopamine. Science 216, 1250–1252.CrossRefGoogle Scholar
Bolbecker, A.R., Lewis, A.R., Swan, A.A., Carlson, K., Fleet, J.R., Beck, K.E. & Wasserman, G.S. (2006). Stable bellows cup electrode demonstrates low-frequency properties of long-term electroretinographic recordings in the Limulus lateral eye. http://dx.doi.org/10.1016/j.jneumeth.2006.07.015.CrossRef
Bolbecker, A.R., Lim, C.C.M., Li, J., Traverso, V., Orchard, A. & Christadoss, C., et al. (2005). Are photoreceptors in the attention spotlight? Efferent neuromodulators accelerate and/or retard the time course of photoreceptor responses evoked by light flashes. Vision Sciences Society Fifth Annual Meeting.
Brecha, N., Hendrickson, A., Florén, I. & Karten, H.J. (1982). Localization of substance P-like immunoreactivity within the monkey retina. Investigative Ophthalmology and Visual Science 23, 147–153.Google Scholar
Brodie, S.E. (1979). Temperature dependence of the dynamic response of the Limulus retina. Vision Research 19, 91–94.CrossRefGoogle Scholar
Calman, B.G. & Battelle, B.-A. (1991). Central origin of the efferent neurons projecting to the eyes of Limulus polyphemus. Visual Neuroscience 6, 481–495.CrossRefGoogle Scholar
Cervetto, L., Marchiafava, P.L. & Pasino, E. (1976). Influence of efferent retinal fibers on responsiveness of ganglion cells to light. Nature 260, 56–57.CrossRefGoogle Scholar
Chamberlain, S.C. & Engbretson, G.A. (1982). Neuropeptide immunoreactivity in Limulus. I. substance P-like immunoreactivity in the lateral eye and protocerebrum. Journal of Comparative Neurology 208, 304–315.Google Scholar
Cheng, Z. & Wasserman, G.S. (1996). Receiver operating characteristic (ROC) analysis of neural code efficacies. I. Graded photoreceptor potentials and data quality. Biological Cybernetics 75, 93–103.Google Scholar
Cuenca, N., de Juan, J. & Kolb, H. (1995). Substance P-immunoreactive neurons in the human retina. Journal of Comparative Neurology 356, 491–504.CrossRefGoogle Scholar
Dick, E. & Miller, R.F. (1981). Peptides influence retinal ganglion cells. Neuroscience Letters 26, 131–135.CrossRefGoogle Scholar
Duke-Elder, S. (1968). System of Ophthalmology: The Physiology of the Eye and of Vision. Mosby.
Easland, G.S. & Wasserman, G.S. (1979). Multiple intracellular contributions to light adaptation in Limulus ommatidia. Vision Research 19, 1–8.CrossRefGoogle Scholar
Evans, J.A., Chamberlain, S.C. & Battelle, B.-A. (1983). Autoradiographic localization of newly synthesized octopamine to retinal efferents in the Limulus visual system. Journal of Comparative Neurology 219, 369–383.CrossRefGoogle Scholar
Fahrenbach, W.H. (1981). The morphology of the horseshoe crab (Limulus polyphemus) visual system. VII. Innervation of photoreceptor neurons by neurosecretory efferents. Cell Tissue Research 216, 655–659.CrossRefGoogle Scholar
Fuortes, M.G.F. & Hodgkin, A.L. (1964). Changes in time scale and sensitivity in the ommatidia of Limulus. Journal of Physiology 172, 239–263.CrossRefGoogle Scholar
Glickman, R.D. & Adolph, A.R. (1982). Acetylcholine and substance P: Action via distinct receptors on carp retinal ganglion cells. Investigative Ophthalmology and Visual Science 22, 804–808.Google Scholar
Glickman, R.D., Adolph, A.R. & Dowling, J.E. (1982). Inner plexiform circuits in the carp retina: Effects of cholinergic agonists, GABA, and substance P on the ganglion cells. Brain Research 234, 81–99.Google Scholar
Hartline, H.K. & Graham, C.H. (1932). Nerve impulses from single receptors in the eye. Journal of Cellular and Comparative Physiology 1, 227–295.Google Scholar
Holden, A.L. (1990). Centrifugal pathways to the retina: Which way does the “searchlight” point? Visual Neuroscience 4, 493–495.Google Scholar
Kaplan, E. & Barlow, R.B., Jr. (1980). Circadian clock in Limulus brain increases response and decreases noise of retinal photoreceptors. Nature 286, 393–395.Google Scholar
Kaplan, E., Barlow, R.G., Renninger, G. & Purpura, K. (1990). Circadian rhythms in Limulus photoreceptors. II. Quantum bumps. Journal of General Physiology 96, 665–685.Google Scholar
Kass, L. & Barlow, R.B., Jr. (1984). Efferent neurotransmission of circadian rhythms in Limulus lateral eye. I. Octopamine-induced increases in retinal sensitivity. Journal of Neuroscience 4, 908–917.Google Scholar
Lee, H.M. & Wyse, G.A. (1991). Immunocytochemical localization of octopamine in the central nervous system of Limulus polyphemus: A light and electron microscopic study. Journal of Comparative Neurology 307, 683–694.Google Scholar
Lewandowski, T.J., Lehman, H.K. & Chamberlain, S.C. (1989). Immunoreactivity in Limulus: III. Morphological and biochemical studies of FARFamide-like immunoreactivity and colocalized substance P-like immunoreactivity in the brain and lateral eye. Journal of Comparative Neurology 288, 136–153.Google Scholar
Lim, C.C.M. & Wasserman, G.S. (2001). Categorical and prolonged potentials are evoked when brief, intermediate-intensity flashes stimulate horseshoe crab lateral eye photoreceptors during octopamine neuromodulation. Biological Signals and Receptors 10, 399–415.Google Scholar
Lim-Kessler, C.C.M, Bolbecker, A.R., Li, J. & Wasserman, G.S. (2007). Osmotic properties of Limulus seawaters and organ cultures: An unrecognized issue. Visual Neuroscience 25, 103–105.Google Scholar
Mancillas, J.R. & Brown, M.R. (1984). Neuropeptide modulation of photosensitivity: I. Presence, distribution, and characterization of a substance P-like peptide in the lateral eye of Limulus. Journal of Neuroscience 4, 832–846.Google Scholar
Mancillas, J.R. & Selverston, A.I. (1984). Neuropeptide modulation of photosensitivity: II. Physiological and anatomical effects of substance P on the lateral eye of Limulus. Journal of Neuroscience 4, 847–859.Google Scholar
Mancillas, J.R. & Selverston, A.I. (1985). Substance P-like immunoreactivity is present in the central nervous system of Limulus polyphemus. Journal of Comparative Neurology 238, 38–52.Google Scholar
Nisly-Nagele, S.J. & Wasserman, G.S. (2001). Dissociating sensory and cognitive contributions to visual persistence: I. Photoreceptor response duration as a function of flash intensity, adaptation state, and candidate code. Biological Cybernetics 85, 167–183.Google Scholar
Nordström, P. & Warrant, E.J. (2000). Temperature-induced pupil movements in insect superposition eyes. Journal of Experimental Biology 203, 685–692.Google Scholar
O'Day, P.M. & Lisman, J.E. (1985). Octopamine enhances dark adaptation in Limulus ventral photoreceptors. Journal of Neuroscience 5, 1490–1496.Google Scholar
Poloschek, C.M. & Sutter, E.E. (2002). The fine structure of multifocal ERG topographies. Journal of Vision 2, 577–587.Google Scholar
Renninger, G.H., Kass, L., Pelletier, J.L. & Schimmel, R. (1988). The eccentric cell of the Limulus lateral eye: Encoder of circadian changes in visual responses. Journal of Comparative Physiology A 163, 259–270.Google Scholar
Renninger, G.H., Schimmel, R. & Farrell, C.A. (1989). Octopamine modulates photoreceptor function in the Limulus lateral eye. Visual Neuroscience 3, 83–94.Google Scholar
Tatler, B., O'Carroll, D.C. & Laughlin, S.B. (2000). Temperature and the temporal resolving power of fly photoreceptors. Journal of Comparative Physiology A 186, 399–407.Google Scholar
Tyler, W.D. & Mercier, A.J. (2003). Synaptic modulation by a neuropeptide depends on temperature and extracellular calcium. Journal of Neurophysiology 89, 1807–1814.Google Scholar
Van den Burg, E.H., Metz, J.R., Ross, H.A., Darras, V.M., Wendelaar Bonga, S.E. & Flik, G. (2003). Temperature-induced changes in thyrotropin-releasing hormone sensitivity in carp melanotropes. Journal of Neuroendocrinology 77, 15–23.Google Scholar
Viana di Prisco, G., Pearlstein, E., Le Ray, D., Robitaille, R. & Dubuc, R. (2000). A cellular mechanism for the transformation of a sensory input into a motor command. Journal of Neuroscience 20, 8169–8176.Google Scholar
Viana di Prisco, G., Pearlstein, E., Robitaillie, R. & Dubuc, R. (1997). Role of sensory-evoked NMDA plateau potentials in the initiation of locomotion. Science 278, 1122–1125.Google Scholar
Wasserman, G.S. (1967). Density spectrum of Limulus screening pigment. Journal of General Physiology 50, 1075–1077.Google Scholar
Wasserman, G.S., Felsten, G. & Easland, G.S. (1979). The psychophysical function: Harmonizing Fechner and Stevens. Science 204, 85–87.Google Scholar
Wong, F., Knight, B.W. & Dodge, F.A. (1982). Adapting bump model for ventral photoreceptors of Limulus. Journal of General Physiology 79, 1089–1113.Google Scholar