A role for compromise: Synaptic inhibition and electrical coupling interact to control phasing in the leech heartbeat CPG

Frontiers in Behavioral Neuroscience

Volumn 4, Issue JUL, 2010, Pages

  Weaver, Adam L ^a,b   Roffman, Rebecca C ^a   Norris, Brian J ^a   Calabrese, Ronald L ^a  

^a EMORY UNIVERSITY   (United States)

^b SAINT MICHAEL'S COLLEGE   (United States)

Author keywords

Entrainment; Neuronal networks; Neuronal oscillators

Indexed keywords

EID: 80051564603     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2010.00038     Document Type: Article

References (50)

1. Bose, A., Manor, Y., and Nadim, F. (2004). The activity phase of postsynaptic neurons in a simplified rhythmic network. J. Comput. Neurosci. 17, 245-261.
2. Bower, J. M., and Beeman, D. (1998). The Book of GENESIS: Exploring Realistic Neural Models with the GEneral NEural SImulation System, 2nd Edn. New York: Springer-Verlag.
3. Bucher, D., Prinz, A. A., and Marder, E. (2005). Animal-to-animal variability in motor pattern production in adults and during growth. J. Neurosci. 25, 1611-1619.
4. Calabrese, R. L. (1977). The neural control of alternate heartbeat coordination states in the leech, Hirudo medicinalis. J. Comp. Physiol. 122, 11-143.
5. Cropper, E. C., Evans, C. G., Hurwitz, I., Jing, J., Proekt, A., Romero, A., and Rosen, S. C. (2004). Feeding neural networks in the mollusc Aplysia. Neurosignals 13, 70-86.
6. Cymbalyuk, G. S., Gaudry, Q., Masino, M. A., and Calabrese, R. L. (2002). Bursting in leech heart interneurons: cell-autonomous and network-based mechanisms. J. Neurosci. 22, 10580-10592.
7. De Schutter, E., Ekeberg, O., Kotaleski, J. H., Achard, P., and Lansner, A. (2005). Biophysically detailed modelling of microcircuits and beyond. Trends Neurosci. 28, 562-569.
8. Garcia, P. S., Wright, T. M., Cunningham, I. R., and Calabrese, R. L. (2008). Using a model to assess the role of the spatiotemporal pattern of inhibitory input and intrasegmental electrical coupling in the intersegmental and side-to-side coordination of motor neurons by the leech heartbeat central pattern generator. J. Neurophysiol. 100, 1354-1371.
9. Goaillard, J. M., Taylor, A. L., Schulz, D. J., and Marder, E. (2009). Functional consequences of animal-to-animal variation in circuit parameters. Nat. Neurosci. 12, 1424-1430.
10. Gramoll, S., Schmidt, J., and Calabrese, R. L. (1994). Switching in the activity state of an interneuron that controls coordination of the hearts in the medicinal leech (Hirudo medicinalis). J. Exp. Biol. 186, 157-171.
11. Grillner, S., Kozlov, A., Dario, P., Stefanini, C., Menciassi, A., Lansner, A., and Hellgren Kotaleski, J. (2007). Modeling a vertebrate motor system: pattern generation, steering and control of body orientation. Prog. Brain Res. 165, 221-234.
12. Hill, A. A., Lu, J., Masino, M. A., Olsen, O. H., and Calabrese, R. L. (2001). A model of a segmental oscillator in the leech heartbeat neuronal network. J. Comput. Neurosci. 10, 281-302.
13. Hill, A. A., Masino, M. A., and Calabrese, R. L. (2002). Model of intersegmental coordination in the leech heartbeat neuronal network. J. Neurophysiol. 87, 1586-1602.
14. Hooper, S. L., Buchman, E., Weaver, A. L., Thuma, J. B., and Hobbs, K. H. (2009). Slow conductances could underlie intrinsic phase-maintaining properties of isolated lobster (Panulirus interruptus) pyloric neurons. J. Neurosci. 29, 1834-1845.
15. Hooper, S. L., and DiCaprio, R. A. (2004). Crustacean motor pattern generator networks. Neurosignals 13, 50-69.
16. Houck, C. R., Joines, J. A., Kay, M. G., and Wilson, J. R. (1997). Empirical investigation of the benefits of partial Lamarckianism. Evol. Comput. 5, 31-60.
17. Ivanov, A. I., and Calabrese, R. L. (2000). Intracellular Ca2+ dynamics during spontaneous and evoked activity of leech heart interneurons: low-threshold Ca currents and graded synaptic transmission. J. Neurosci. 20, 4930-4943.
18. Ivanov, A. I., and Calabrese, R. L. (2003). Modulation of spike-mediated synaptic transmission by presynaptic background Ca2ttin leech heart interneurons. J. Neurosci. 23, 1206-1218.
19. Ivanov, A. I., and Calabrese, R. L. (2006a). Graded inhibitory synaptic transmission between leech interneurons: assessing the roles of two kinetically distinct low-threshold Ca currents. J. Neurophysiol. 96, 218-234.
20. Ivanov, A. I., and Calabrese, R. L. (2006b). Spike-mediated and graded inhibitory synaptic transmission between leech interneurons: evidence for shared release sites. J. Neurophysiol. 96, 235-251.
21. Jezzini, S. H., Hill, A. A., Kuzyk, P., and Calabrese, R. L. (2004). Detailed model of intersegmental coordination in the timing network of the leech heartbeat central pattern generator. J. Neurophysiol. 91, 958-977.
22. Jones, S. R., Mulloney, B., Kaper, T. J., and Kopell, N. (2003). Coordination of cellular pattern-generating circuits that control limb movements: the sources of stable differences in intersegmental phases. J. Neurosci. 23, 3457-3468.
23. Krahl, B., and Zerbst-Boroffka, I. (1983). Blood pressure in the leech Hirudo medicinalis. J. Exp. Biol. 107, 163-168.
24. Kristan, W. B. Jr., Calabrese, R. L., and Friesen, W. O. (2005). Neuronal control of leech behavior. Prog. Neurobiol. 76, 279-327.
25. Lu, J., Gramoll, S., Schmidt, J., and Calabrese, R. L. (1999). Motor pattern switching in the heartbeat pattern generator of the medicinal leech: membrane properties and lack of synaptic interaction in switch interneurons. J. Comp. Physiol. A 184, 311-324.
26. Mamiya, A., and Nadim, F. (2004). Dynamic interaction of oscillatory neurons coupled with reciprocally inhibitory synapses acts to stabilize the rhythm period. J. Neurosci. 24, 5140-5150.
27. Marder, E., and Bucher, D. (2007). Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu. Rev. Physiol. 69, 291-316.
28. Marder, E., Bucher, D., Schulz, D. J., and Taylor, A. L. (2005). Invertebrate central pattern generation moves along. Curr. Biol. 15, R685-699.
29. Marder, E., and Calabrese, R. L. (1996). Principles of rhythmic motor pattern generation. Physiol. Rev. 76, 687-717.
30. Marder, E., Tobin, A. E., and Grashow, R. (2007). How tightly tuned are network parameters? Insight from computational and experimental studies in small rhythmic motor networks. Prog. Brain Res. 165, 193-200.
31. Masino, M. A., and Calabrese, R. L. (2002a). Period differences between segmental oscillators produce intersegmental phase differences in the leech heartbeat timing network. J. Neurophysiol. 87, 1603-1615.
32. Masino, M. A., and Calabrese, R. L. (2002b). Phase relationships between segmentally organized oscillators in the leech heartbeat pattern generating network. J. Neurophysiol. 87, 1572-1585.
33. Mouser, C., Nadim, F., and Bose, A. (2008). Maintaining phase of the crustacean tri-phasic pyloric rhythm. J. Math. Biol. 57, 161-181.
34. Norris, B. J., Weaver, A. L., Morris, L. G., Wenning, A., Garcia, P. A., and Calabrese, R. L. (2006). A central pattern generator producing alternative outputs: temporal pattern of premotor activity. J. Neurophysiol. 96, 309-326.
35. Norris, B. J., Weaver, A. L., Wenning, A., Garcia, P. A., and Calabrese, R. L. (2007a). A central pattern generator producing alternative outputs: pattern, strength and dynamics of premotor synaptic input to leech heart motor neurons. J. Neurophysiol. 98, 2983-2991.
36. Norris, B. J., Weaver, A. L., Wenning, A., Garcia, P. A., and Calabrese, R. L. (2007b). A central pattern generator producing alternative outputs: phase relations of leech heart motor neurons with respect to premotor synaptic input. J. Neurophysiol. 98, 2992-3005.
37. Olsen, O. H., and Calabrese, R. L. (1996). Activation of intrinsic and synaptic currents in leech heart interneurons by realistic waveforms. J. Neurosci. 16, 4958-4970.
38. Olypher, A. V., Cymbalyuk, G., and Calabrese, R. L. (2006). Hybrid systems analysis of the control of burst duration by low-voltage-activated calcium current in leech heart interneurons. J. Neurophysiol. 96, 2857-2867.
39. Peterson, E. L. (1983a). Generation and coordination of heartbeat timing oscillation in the medicinal leech. I. Oscillation in isolated ganglia. J. Neurophysiol. 49, 611-626.
40. Peterson, E. L. (1983b). Generation and coordination of heartbeat timing oscillation in the medicinal leech. II. Intersegmental coordination. J. Neurophysiol. 49, 627-638.
41. Prinz, A. A., Bucher, D., and Marder, E. (2004). Similar network activity from disparate circuit parameters. Nat. Neurosci. 7, 1345-1352.
42. Seaman, R. C., and Calabrese, R. L. (2008). Synaptic variability and stereotypy in the leech heartbeat CPG. Abstr.-Soc. Neurosci. 371.7/MM7.
43. Siddall, M. E., Trontelj, P., Utevsky, S. Y., Nkamany, M., and Macdonald, K. S. (2007). Diverse molecular data demonstrate that commercially available medicinal leeches are not Hirudo medicinalis. Proc. Biol. Sci. 274, 1481-1487.
44. Smarandache, C., Hall, W. M., and Mulloney, B. (2009). Coordination of rhythmic motor activity by gradients of synaptic strength in a neural circuit that couples modular neural oscillators. J. Neurosci. 29, 9351-9360.
45. Stein, P. S. (2005). Neuronal control of turtle hindlimb motor rhythms. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 191, 213-229.
46. Thompson, W. J., and Stent, G. S. (1976). Neuronal control of heartbeat in the medicinal leech. I. Generation of the vascular constriction rhythm by heart motor neurons. J. Comp. Physiol. 111, 261-279.
47. Tobin, A. E., and Calabrese, R. L. (2006). Endogenous and half-center bursting in morphologically inspired models of leech heart interneurons. J. Neurophysiol. 96, 2089-2106.
48. Wenning, A., Cymbalyuk, G. S., and Calabrese, R. L. (2004a). Heartbeat control in leeches. I. Constriction pattern and neural modulation of blood pressure in intact animals. J. Neurophysiol. 91, 382-396.
49. Wenning, A., Hill, A. A., and Calabrese, R. L. (2004b). Heartbeat control in leeches. II. Fictive motor pattern. J. Neurophysiol. 91, 397-409.
50. Wenning, A., Norris, B. J., Seaman, R. C., and Calabrese, R. L. (2008). Two additional pairs of premotor heart interneurons in the leech heartbeat CPG: the more the merrier. Abstr.-Soc. Neurosci. 371.6/MM6.