Cellular and Behavioral Properties of Learning in Leech and Other Annelids

Annelids in Modern Biology

Volumn , Issue , 2009, Pages 133-155

  Crisp, Kevin M ^a   Burrell, Brian D ^b  

^a ST OLAF COLLEGE   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Cellular and behavioral properties of learning in leech and other annelids; Learning in leech whole body shortening reflex and role of s interneuron; Learning in leech swim circuit

Indexed keywords

EID: 84890771496     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470455203.ch8     Document Type: Chapter

References (137)

1. Acosta-Urquidi, J., Sahley, C.L., Kleinhaus, A.L. 1989. Serotonin differentially modulates two K+ currents in the Retzius cell of the leech. J. Exp. Biol. 145, 403-417.
2. Alkatout, B.A., Crisp, K.M. 2007. Serotonin delays habitaution of leech swim response to touch. Behav. Brain Res. 182, 145-149.
3. Amir, R., Devor, M. 2003. Extra spike formation in sensory neurons and the disruption of afferent spike patterning. Biophys. J. 84, 2700-2708.
4. Angstadt, J.D., Friesen, W.O. 1993. Modulation of swimming behavior in the medicinal leech. I. Effects of serotonin on the electrical properties of swim-gating cell 204. J. Comp. Physiol. [A] 172, 223-234.
5. Antic, S., Wuskell, J.P., Loew, L., Zecevic, D. 2000. Functional profile of the giant metacerebral neuron of Helix aspersa: temporal and spatial dynamics of electrical activity in situ. J. Physiol. 527, 55-69.
6. Baccus, S.A. 1998. Synaptic facilitation by reflected action potentials: enhancement of transmission when nerve impulses reverse direction at axon branch points. Proc. Natl. Acad. Sci. U.S.A. 95, 8345-8350.
7. Baccus, S.A., Burrell, B.D., Sahley, C.L., Muller, K.J. 2000. Action potential reflection and failure at axon branch points cause stepwise changes in EPSPs in a neuron essential for learning. J. Neurophysiol. 83, 1693-1700.
8. Bagnoli, P., Brunelli, M., Magni, F. 1972. A fast conducting pathway in the central nervous system of the leech Hirudo medicinalis. Arch. Ital. Biol. 110, 35-51.
9. Bagnoli, P., Brunelli, M., Magni, F., Pellegrino, M. 1975. The neuron of the fast conducting system in hirudo medicinalis: identification and synaptic connections with primary afferent neurons. Arch. Ital. Biol. 113, 21-43.
10. Baker, M.W., Macagno, E.R. 2000. RNAi of the receptor tyrosine phosphatase HmLAR2 in a single cell of an intact leech embryo leads to growth-cone collapse. Curr. Biol. 10, 1071-1074.
11. Barsanti, C., Pellegrini, M., Pellegrino, M. 2006. Regulation of the mechanosensitive cation channels by ATP and cAMP in leech neurons. Biochim. Biophys. Acta 1758, 666-672.
12. Bashinski, H.S., Werner, J.S., Rudy, J.W. 1985. Determinants of infant visual fixation: evidence for a two -process theory. J. Exp. Child. Psychol. 39, 580-598.
13. Baylor, D.A., Nicholls, J.G. 1969. After-effects of nerve impulses on signalling in the central nervous system of the leech. J. Physiol. 203, 571-589.
14. Belardetti, F., Biondi, C., Colombaioni, L., Brunelli, M., Trevisani, A. 1982. Role of serotonin and cyclic AMP on facilitation of the fast conducting system activity in the leech Hirudo medicinalis. Brain Res. 246, 89-103.
15. Bi, G., Poo, M. 2001. Synaptic modification by correlated activity: Hebb ' s postulate revisited. Annu. Rev. Neurosci. 24, 139-166.
16. Bilen, J., Bonini, N.M. 2005. Drosophila as a model for human neurodegenerative disease. Annu. Rev. Genet. 39, 153-171.
17. Briggman, K.L., Kristan, W.B., Jr. 2006. Imaging dedicated and multifunctional neural circuits generating distinct behaviors. J. Neurosci. 26, 10925-10933.
18. Briggman, K.L., Abarbanel, H.D., Kristan, W.B., Jr. 2005. Optical imaging of neuronal populations during decision-making. Science 307, 896-901.
19. Brodfuehrer, P.D., Friesen, W.O. 1986. Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion. I. Output connections of Tr1 and Tr2. J. Comp. Physiol. [A] 159, 489-502.
20. Brunelli, M., Garcia-Gil, M., Mozzachiodi, R., Scuri, R., Zaccardi, M.L. 1997. Neurobiological principles of learning and memory. Arch. Ital. Biol. 135, 15-36.
21. Bullock, T.H., Quarton, G.C. 1966. Simple systems for the study of learning mechanisms. Neurosci. Res. Program Bull. 4, 105-233.
22. Burrell, B.D., Crisp, K.M. 2008. Serotonergic modulation of afterhyperpolarization in a neuron that contributes to learning in the leech. J. Neurophysiol. 99, 605-616.
23. Burrell, B.D., Li, Q. 2008. Co-induction of long-term potentiation and long-term depression at a central synapse in the leech. Neurobiol. Learn. Mem. 90, 275-279.
24. Burrell, B.D., Sahley, C.L. 1998. Generalization of habituation and intrinsic sensitization in the leech. Learn. Mem. 5, 405-419.
25. Burrell, B.D., Sahley, C.L. 1999. Serotonin depletion does not prevent intrinsic sensitization in the leech. Learn. Mem. 6, 509-520.
26. Burrell, B.D., Sahley, C.L. 2001. Learning in simple systems. Curr. Opin. Neurobiol. 11, 757-764.
27. Burrell, B.D., Sahley, C.L. 2004. Multiple forms of long-term potentiation and long-term depression converge on a single interneuron in the leech CNS. J. Neurosci. 24, 4011-4019.
28. Burrell, B.D., Sahley, C.L. 2005. Serotonin mediates learning-induced potentiation of excitability. J. Neurophysiol. 94, 4002-4010.
29. Burrell, B.D., Sahley, C.L., Muller, K.J. 2000. Laser axotomy of a single interneuron disrupts intrinsic sensitization in the leech. Abstr. Soc. Neurosci.
30. Burrell, B.D., Sahley, C.L., Muller, K.J. 2001. Non-associative learning and serotonin induce similar bi -directional changes in excitability of a neuron critical for learning in the medicinal leech. J. Neurosci. 21, 1401-1412.
31. Burrell, B.D., Sahley, C.L., Muller, K.J. 2003. Progressive recovery of learning during regeneration of a single synapse in the medicinal leech. J. Comp. Neurol. 457, 67-74.
32. Carbonetto, S., Muller, K.J. 1977. A regenerating neurone in the leech can form an electrical synapse on its severed axon segment. Nature 267, 450-452.
33. Cataldo, E., Brunelli, M., Byrne, J.H., Av-Ron, E., Cai, Y., Baxter, D.A. 2005. Computational model of touch sensory cells (T Cells) of the leech: role of the afterhyperpolarization (AHP) in activity-dependent conduction failure. J. Comput. Neurosci. 18, 5-24.
34. Catarsi, S., Brunelli, M. 1991. Serotonin depresses the after-hyperpolarization through the inhibition of the Na+/ K+ electrogenic pump in T sensory neurones of the leech. J. Exp. Biol. 155, 261-273.
35. Catarsi, S., Garcia-Gil, M., Traina, G., Brunelli, M. 1990. Seasonal variation of serotonin content and nonassociative learning of swim induction in the leech Hirudo medicinalis. J. Comp. Physiol. [A] 167, 469-474.
36. Catarsi, S., Scuri, R., Brunelli, M. 1993. Cyclic AMP mediates inhibition of the Na(+)-K+ electrogenic pump by serotonin in tactile sensory neurones of the leech. J. Physiol. 462, 229-242.
37. Catarsi, S., Scuri, R., Brunelli, M. 1995. Octopamine and Leydig cell stimulation depress the afterhyperpolarization in touch sensory neurons of the leech. Neuroscience 66, 751-759.
38. Crisp, K.M., Mesce, K.A. 2006. Beyond the central pattern generator: amine modulation of decision-making neural pathways descending from the brain of the medicinal leech. J. Exp. Biol. 209, 1746-1756.
39. Crisp, K.M., Muller, K.J. 2006. A 3-synapse positive feedback loop regulates the excitability of an interneuron critical for sensitization in the leech. J. Neurosci. 26, 3524-3531.
40. Daoudal, G., Debanne, D. 2003. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn. Mem. 10, 456-465.
41. Darwin, C.D. 1966. Darwin on Humus and Earthworms. London: Faber and Faber, p. 58.
42. Davis, M., File, S.E. 1984. Intrinsic and extrinsic mechanisms of habituation and sensitization: implications for the design and analysis of experiments. In Habituation, Sensitization and Behavior, edited by H.V.S. Peeke and L.F. Petrinovich. New York: Academic Press, pp. 287-323.
43. Davis, M., Wagner, M. 1969. Habituation of the startle response under an incremental sequence of stimulus intensities. J. Comp. Physiol. Psychol. 67, 486-492.
44. Debanne, D., Kopysova, I.L., Bras, H., Ferrand, N. 1999. Gating of action potential propagation by an axonal A-like potassium conductance in the hippocampus: a new type of non-synaptic plasticity. J. Physiol. Paris 93, 285-296.
45. Debski, E.A., Friesen, W.O. 1985. Habituation of swimming activity in the medicinal leech. J. Exp. Biol. 116, 169-188.
46. Debski, E.A., Friesen, W.O. 1986. Role of central interneurons in habituation of swimming activity in the medicinal leech. J. Neurophysiol. 55, 977-994.
47. Debski, E.A., Friesen, W.O. 1987. Intracellular stimulation of sensory cells elicits swimming activity in the medicinal leech. J. Comp. Physiol. [A] 160, 447-457.
48. De Miguel, F.F., Trueta, C. 2005. Synaptic and extrasynaptic secretion of serotonin. Cell Mol. Neurobiol. 25, 297-312.
49. Dierkes, P.W., Wende, V., Hochstrate, P., Schlue, W. R. 2004. L-type Ca2+ channel antagonists block voltage -dependent Ca2+ channels in identified leech neurons. Brain Res. 1013, 159-167.
50. Dorsett, D.A. 1980. Design and function of giant fibre systems. Trends Neurosci. 3, 205-208.
51. Duan, Y., Panoff, J., Burrell, B.D., Sahley, C.L., Muller, K.J. 2005. Repair and regeneration of functional synaptic connections: cellular and molecular interactions in the leech. Cell Mol. Neurobiol. 25, 441-450.
52. Ehrlich, J.S., Boulis, N.M., Karrer, T., Sahley, C.L. 1992. Differential effects of serotonin depletion on sensitization and dishabituation in the leech, Hirudo medicinalis. J. Neurobiol. 23, 270-279.
53. Evans, C.G., Jing, J., Rosen, S.C., Cropper, E.C. 2003. Regulation of spike initiation and propagation in an Aplysia sensory neuron: gating-in via central polarization. J. Neurosci. 23, 2920-2931.
54. Frank, E., Jansen, J.K., Rinvik, E. 1975. A multisomatic axon in the central nervous system of the leech. J. Comp. Neurol. 159, 1-13.
55. Frick, A., Johnston, D. 2005. Plasticity of dendritic excitability. J. Neurobiol. 64, 100-115.
56. Glanzman, D.L. 2006. The cellular mechanisms of learning in Aplysia: of blind men and elephants. Biol. Bull. 210, 271-279.
57. Grey, K.B., Burrell, B.D. 2008. Forskolin induces NMDA receptor-dependent potentiation at a central synapse in the leech. J. Neurophysiol. 99, 2719-2724.
58. Groves, P.M., Lee, D., Thompson, R.F. 1970. Effects of stimulus frequency and intensity on habituation and sensitization in acute spinal cat. Physiol. Behav. 4, 383-388.
59. Gu, X.N., Macagno, E.R., Muller, K.J. 1989. Laser microbeam axotomy and conduction block show that electrical transmission at a central synapse is distributed at multiple contacts. J. Neurobiol. 20, 422-434.
60. Gu, X.N., Muller, K.J., Young, S.R. 1991. Synaptic integration at a sensory-motor reflex in the leech. J. Physiol. 441, 733-754.
61. Gunther, J. 1973. A new type of " node " in the myelin sheath of an invertebrate nerve fiber. Experientia 29, 1263-1265.
62. Gunther, J. 1976. Impulse conduction in the myelinated giant fibers of the earthworm. Structure and function of the dorsal nodes in the median giant fiber. J. Comp. Neurol. 168, 505-531.
63. Hawkins, R.D., Kandel, E.R., Bailey, C.H. 2006. Molecular mechanisms of memory storage in Aplysia. Biol. Bull. 210, 174-191.
64. Hinde, R.A. 1970. Behavioral habituation. In S hort-Term Changes in Neural Activity, edited by G. Horn and R.A. Hinde. London: Cambridge University Press, pp. 3-40.
65. Horridge, G.A. 1959. Analysis of the rapid responses of Nereis and Harmothoe (Annelida). Proc. R. Soc. Lond. B Biol. Sci. 150, 245-262.
66. Jansen, J.K., Nicholls, J.G. 1973. Conductance changes, an electrogenic pump and the hyperpolarization of leech neurones following impulses. J. Physiol. 229, 635-655.
67. Keating, H.H., Sahley, C.L. 1996. Localization of the myomodulin-like immunoreactivity in the leech CNS. J. Neurobiol. 30, 374-384.
68. Kerkut, G.A., Walker, R.J. 1967. The action of acetylcholine, dopamine and 5-hydroxytryptamine on the spontaneous activity of the cells of Retzius in the leech Hirudo medicinalis. Br. J. Pharmacol. Chemother. 30, 644-654.
69. Kramer, A.P. 1981. The nervous system of the glossiphoniid leech Haementeria ghilianii. II. Synaptic pathways controlling body wall shortening. J. Comp. Physiol. [A] 144, 449-457.
70. Krasne, F.B. 1965. Escape from recurring tactile stimulation in Branchiomma vesiculosum. J. Exp. Biol. 4 2, 307-322.
71. Kristan, W.B., Jr., Calabrese, R.L. 1976. Rhythmic swimming activity in neurones of the isolated nerve cord of the leech. J. Exp. Biol. 65, 643-668.
72. Kristan, W.B., Jr., Calabrese, R.L., Friesen, W.O. 2005. Neuronal control of leech behavior. Prog. Neurobiol. 76, 279-327.
73. Laverack, M.S. 1969. Mechanoreceptors, photoreceptors and rapid conduction pathways in the leech, Hirudo medicinalis. J. Exp. Biol. 50, 129-140.
74. Li, Q., Burrell, B.D. 2006. CNQX inhibits transmission at rectifying but not non-rectifying electrical synapses. Soc. Neurosci. (Abstr.132.4).
75. Liu, Y., Nicholls, J.G. 1989. Steps in the development of chemical and electrical synapses by pairs of identified leech neurons in culture. Proc. R. Soc. Lond. B Biol. Sci. 236, 253-268.
76. Lockery, S.R., Rawlins, J.N., Gray, J.A. 1985. Habituation of the shortening reflex in the medicinal leech. Behav. Neurosci. 99, 333-341.
77. Lockery, S.R., Kristan, W.B., Jr. 1990. Distributed processing of sensory information in the leech. I. Input -output relations of the local bending reflex. J. Neurosci. 10, 1811-1815.
78. Lockery, S.R., Kristan, W.B., Jr. 1991. Two forms of sensitization of the local bending reflex of the medicinal leech. J. Comp. Physiol. [A] 168, 165-177.
79. Macagno, E.R., Muller, K.J., Pitman, R.M. 1987. Conduction block silences parts of a chemical synapse in the leech central nervous system. J. Physiol. 387, 649-664.
80. Magni, F., Pellegrino, M. 1975. Nerve cord shortening induced by activation of the fast conducting system in the leech. Brain Res. 90, 169-174.
81. Magni, F., Pellegrino, M. 1978a. Neural mechanisms underlying the segmental and genaralized cord shortening reflexes in the leech. J. Comp. Physiol. [A] 124, 339-351.
82. Magni, F., Pellegrino, M. 1978b. Patterns of activity and the effects of activation of the fast conducting system on the behaviour of unrestrained leeches. J. Exp. Biol. 76, 123-135.
83. Malenka, R.C., Bear, M.F. 2004. LTP and LTD: an embarrassment of riches. Neuron 44, 5-21.
84. Mar, A., Drapeau, P. 1996. Modulation of conduction block in leech mechanosensory neurons. J. Neurosci. 16, 4335-4343.
85. Marinesco, S., Wickremasinghe, N., Kolkman, K.E., Carew, T.J. 2004. Serotonergic modulation in aplysia. II. Cellular and behavioral consequences of increased serotonergic tone. J. Neurophysiol. 92, 2487-2496.
86. Mason, A., Muller, K.J. 1996. Accurate synapse regeneration despite ablation of the distal axon segment. Eur. J. Neurosci. 8, 11-20.
87. Modney, B.K., Sahley, C.L., Muller, K.J. 1997. Regeneration of a central synapse restores nonassociative learning. J. Neurosci. 17, 6478-6482.
88. Moss, B.L., Fuller, A.D., Sahley, C.L., Burrell, B.D. 2005. Serotonin modulates axo-axonal coupling between neurons critical for learning in the leech. J. Neurophysiol. 94, 2575-2589.
89. Muller, K.J., Carbonetto, S. 1979. The morphological and physiological properties of a regenerating synapse in the CNS of the leech. J. Comp. Neurol. 185, 485-516.
90. Muller, K.J., Scott, S.A. 1981. Transmission at a " direct " electrical connexion mediated by an interneurone in the leech. J. Physiol. 311, 565-583.
91. Nicholls, J.G., Purves, D. 1970. Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. J. Physiol. 209, 647-667.
92. Nusbaum, M.P., Kristan, W.B., Jr. 1986. Swim initiation in the leech by serotonin-containing interneurones, cells 21 and 61. J. Exp. Biol. 122, 277-302.
93. Prescott, S.A., Chase, R. 1999. Sites of plasticity in the neural circuit mediating tentacle withdrawal in the snail Helix aspersa: implications for behavioral change and learning kinetics. Learn. Mem. 6, 363-380.
94. Rankin, C.H., Carew, T.J. 1988. Dishabituation and sensitization emerge as separate processes during development in Aplysia. J. Neurosci. 8, 197-211.
95. Raymond, C.R. 2007. LTP forms 1, 2 and 3: different mechanisms for the " long " in long-term potentiation. TINS 30, 167-175.
96. Roberts, M.B.V. 1962a. The rapid response of Myxicola infundibulum (Grubed). J. Mar. Biol. Assoc. U.K. 42, 527-539.
97. Roberts, M.B.V. 1962b. The giant fibre reflex of the earthworm, Lumbricus terrestris L. I. The rapid response. J. Exp. Biol. 39, 219-227.
98. Roberts, M.B.V. 1966. Facilitation in the rapid response of the earthworm, Lumbricus terrestris L. J. Exp. Biol. 45, 141-150.
99. Rosenkoetter, J.S., Boyce, R. 1975. Earthworm pheremones and T-maze performance. J. Comp. Physiol. Psychol. 88, 904-910.
100. Sahley, C.L. 1994. Serotonin depletion impairs but does not eliminate classical conditioning in the leech Hirudo medicinalis. Behav. Neurosci. 108, 1043-1052.
101. Sahley, C.L., Boulis, N.M., Schurman, B. 1994a. Associative learning modifies the shortening reflex in the semi -intact leech Hirudo medicinalis: effects of pairing, predictability, and CS pre-exposure. Behav. Neurosci. 108, 340-346.
102. Sahley, C.L., Modney, B.K., Boulis, N.M., Muller, K.J. 1994b. The S cell: an interneuron essential for sensitization and full dishabituation of leech shortening. J. Neurosci. 14, 6715-6721.
103. Schanbacker, A., Koch, M., Pilz, P.K.D., Schnitzler, H.U. 1996. Lesions of the amygdala do not affect the enhancement of the acoustic startle response by background noise. Physiol. Behav. 60, 1341-1346.
104. Scheibenstock, A., Krygier, D., Haque, Z., Syed, N., Lukowiak, K. 2002. The Soma of RPeD1 must be present for long-term memory formation of associative learning in Lymnaea. J. Neurophysiol. 88, 1584-1591.
105. Scott, S.A., Muller, K.J. 1980. Synapse regeneration and signals for directed axonal growth in the central nervous system of the leech. Dev. Biol. 80, 345-363.
106. Scuri, R., Mozzachiodi, R., Brunelli, M. 2002. Activity-dependent increase of the AHP amplitude in T sensory neurons of the leech. J. Neurophysiol. 88, 2490-2500.
107. Scuri, R., Mozzachiodi, R., Brunelli, M. 2005. Role for calcium signaling and arachidonic acid metabolites in the activity-dependent increase of AHP amplitude in leech T sensory neurons. J. Neurophysiol. 94, 1066-1073.
108. Scuri, R., Lombardo, P., Cataldo, E., Ristori, C., Brunelli, M. 2007. Inhibition of Na+/K+ ATPase potentiates synaptic transmission in tactile sensory neurons of the leech. Eur. J. Neurosci. 25, 159-167.
109. Shaw, B.K., Kristan, W.B., Jr. 1995. The whole-body shortening reflex of the medicinal leech: motor pattern, sensory basis, and interneuronal pathways. J. Comp. Physiol. [A] 177, 667-681.
110. Shaw, B.K., Kristan, W.B., Jr. 1999. Relative roles of the S cell network and parallel interneuronal pathways in the whole-body shortening reflex of the medicinal leech. J. Neurophysiol. 82, 1114-1123.
111. Shefi, O., Simonnet, C., Baker, M.W., Glass, J.R., Macagno, E.R., Groisman, A. 2006. Microtargeted gene silencing and ectopic expression in live embryos using biolistic delivery with a pneumatic capillary gun. J. Neurosci. 26, 6119-6123.
112. Skierczynski, B.A., Wilson, R.J., Kristan, W.B., Jr., Skalak, R. 1996. A model of the hydrostatic skeleton of the leech. J. Theor. Biol. 181, 329-342.
113. Stuart, A.E. 1969. Excitatory and inhibitory motoneurons in the central nervous system of the leech. Science 165, 817-819.
114. Stuart, A.E. 1970. Physiological and morphological properties of motoneurones in the central nervous system of the leech. J. Physiol. 209, 627-646.
115. Szczupak, L., Kristan, W.B., Jr. 1995. Widespread mechanosensory activation of the serotonergic system of the medicinal leech. J. Neurophysiol. 74, 2614-2624.
116. Taylor, A.L., Cottrell, G.W., Kleinfeld, D., Kristan, W.B., Jr. 2003. Imaging reveals synaptic targets of a swim-terminating neuron in the leech CNS. J. Neurosci. 23, 11402-11410.
117. Thompson, L.M., Marsh, J.L. 2003. Invertebrate models of neurologic disease: insights into pathogenesis and therapy. Curr. Neurol. Neurosci. Rep. 3, 442-448.
118. Thompson, R.F., Spencer, W.A. 1966. Habituation: a model phenomenon for the study of the neuronal substrates of behavior. Psychol. Rev. 73, 16-43.
119. Tobin, A.E., Calabrese, R.L. 2005. Myomodulin increases Ih and inhibits the NA/K pump to modulate bursting in leech heart interneurons. J. Neurophysiol. 94, 3938-3950.
120. Trueta, C., Mendez, B., De Miguel, F.F. 2003. Somatic exocytosis of serotonin mediated by L-type calcium channels in cultured leech neurones. J. Physiol. 547, 405-416.
121. Trueta, C., Sanchez-Armass, S., Morales, M.A., De Miguel, F.F. 2004. Calcium-induced calcium release contributes to somatic secretion of serotonin in leech Retzius neurons. J. Neurobiol. 61, 309-316.
122. Van Essen, D.C. 1973. The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech. J. Physiol. 230, 509-534.
123. Walker, R.J., Smith, P.A. 1973. The ionic mechanism for 5-hydroxytryptamine inhibition on Retzius cells of the leech Hirudo medicinalis. Comp. Biochem. Physiol. 45A, 979-993.
124. Wang, Y., Strong, J.A., Sahley, C.L. 1999. Modulatory effects of myomodulin on the excitability and membrane currents in Retzius cells of the leech. J. Neurophysiol. 82, 216-225.
125. Weeks, J.C. 1981. Neuronal basis of leech swimming: separation of swim initiation, pattern generation, and intersegmental coordination by selective lesions. J. Neurophysiol. 45, 698-723.
126. Weeks, J.C. 1982. Segmental specialization of a leech swim-initiating interneuron, cell 205. J. Neurosci. 2, 972-985.
127. Willard, A.L. 1981. Effects of serotonin on the generation of the motor program for swimming by the medicinal leech. J. Neurosci. 1, 936-944.
128. Wittenberg, G., Kristan, W.B., Jr. 1992a. Analysis and modeling of the multisegmental coordination of shortening behavior in the medicinal leech. I. Motor output pattern. J. Neurophysiol. 68, 1683-1692.
129. Wittenberg, G., Kristan, W.B., Jr. 1992b. Analysis and modeling of the multisegmental coordination of shortening behavior in the medicinal leech. II. Role of identified interneurons. J. Neurophysiol. 68, 1693-1707.
130. Wolf, F.W., Heberlein, U. 2003. Invertebrate models of drug abuse. J. Neurobiol. 54, 161-178.
131. Yau, K.W. 1976. Physiological properties and receptive fields of mechanosensory neurones in the head ganglion of the leech: comparison with homologous cells in segmental ganglia. J. Physiol. 263, 489-512.
132. Zaccardi, M.L., Traina, G., Cataldo, E., Brunelli, M. 2001. Nonassociative learning in the leech Hirudo medicinalis. Behav. Brain Res. 126, 91-92.
133. Zaccardi, M.L., Traina, G., Cataldo, E., Brunelli, M. 2004. Sensitization and dishabituation of swim induction in the leech Hirudo medicinalis: role of serotonin and cyclic AMP. Behav. Brain Res. 153, 317-326.
134. Zhang, W., Linden, D.J. 2003. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat. Rev. Neurosci. 4, 885-900.
135. Zheng, M., Friesen, W.O., Iwasaki, T. 2007. Systems -level modeling of neuronal circuits for leech swimming. J. Comput. Neurosci. 22, 21-38.
136. Zoccolan, D., Pinato, G., Torre, V. 2002. Highly variable spike trains underlie reproducible sensorimotor responses in the medicinal leech. J. Neurosci. 22, 10790-10800.
137. Zoran, M.J., Drewes, C. 1987. Rapid escape reflexes in aquatic oligochaetes: variations in design and function of evolutionarily conserved giant fiber systems. J. Comp. Physiol. [A] 161, 729-738.