Widespread Inhibition Proportional to Excitation Controls the Gain of a Leech Behavioral Circuit

Neuron

Volumn 57, Issue 2, 2008, Pages 276-289

  Baca, Serapio M ^a   Marin Burgin, Antonia ^a   Wagenaar, Daniel A ^a   Kristan Jr , William B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

SYSBIO; SYSNEURO

Indexed keywords

DYE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BEHAVIORAL SCIENCE; CONTROLLED STUDY; IMAGING; INTERNEURON; INTRACELLULAR RECORDING; INVERTEBRATE; NERVE CELL NETWORK; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; STIMULUS; VERTEBRATE;

ANIMALS; BEHAVIOR, ANIMAL; BICUCULLINE; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; GABA ANTAGONISTS; GANGLIA, INVERTEBRATE; LEECHES; MODELS, NEUROLOGICAL; MOTOR ACTIVITY; MULTIVARIATE ANALYSIS; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; VIDEO RECORDING;

EID: 38149085369     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.11.028     Document Type: Article

References (69)

1. Abbott L.F., and Chance F.S. Drivers and modulators from push-pull and balanced synaptic input. Prog. Brain Res. 149 (2005) 147-155
2. Baca S.M., Thomson E.E., and Kristan W.B. Location and intensity discrimination in the leech local bending response quantified using optic flow and principal components analysis. J. Neurophysiol. 93 (2005) 3560-3572
3. Berg R.W., Alaburda A., and Hounsgaard J. Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315 (2007) 390-393
4. Blitz D.M., and Regehr W.G. Timing and specificity of feed-forward inhibition within the LGN. Neuron 45 (2005) 917-928
5. Briggman K.L., Abarbanel H.D.I., and Kristan Jr. W.B. Optical imaging of neuronal populations during decision-making. Science 307 (2005) 896-901
6. Buneo C.A., and Andersen R.A. The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44 (2006) 2594-2606
7. Cacciatore T.W., Brodfuehrer P.D., Gonzalez J.E., Jiang T., Adams S.R., Tsien R.Y., Kristan W.B., and Kleinfeld D. Identification of neural circuits by imaging coherent electrical activity with FRET-based dyes. Neuron 23 (1999) 449-459
8. Carandini M., and Heeger D.J. Summation and division by neurons in primate visual cortex. Science 264 (1994) 1333-1336
9. Chance F.S., Abbott L.F., and Reyes A.D. Gain modulation from background synaptic input. Neuron 35 (2002) 773-782
10. Cline H. Evidence for GABA as a neurotransmitter in the leech. J. Neurosci. 6 (1986) 2848-2856
11. Cline H.T., Nusbaum M.P., and Kristan Jr. W.B. Identified GABAergic inhibitory motor neurons in the leech central nervous system take up GABA. Brain Res. 348 (1985) 359-362
12. Connor C.E., Preddie D.C., Gallant J.L., and Van Essen D.C. Spatial attention effects in macaque area V4. J. Neurosci. 17 (1997) 3201-3214
13. Doiron B., Longtin A., Berman N., and Maler L. Subtractive and divisive inhibition: effect of voltage-dependent inhibitory conductances and noise. Neural Comput. 13 (2001) 227-248
14. Dunn F.A., and Rieke F. The impact of photoreceptor noise on retinal gain controls. Curr. Opin. Neurobiol. 16 (2006) 363-370
15. Eccles J.C. The Inhibitory Pathways of the Central Nervous System (1969), Thomas, Springfield, IL
16. Gabernet L., Jadhav S.P., Feldman D.E., Carandini M., and Scanziani M. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48 (2005) 315-327
17. Garcia-Perez E., Zoccolan D., Pinato G., and Torre V. Dynamics and reproducibility of a moderately complex sensory-motor response in the medicinal leech. J. Neurophysiol. 92 (2004) 1783-1795
18. Granzow B., and Kristan Jr. W.B. Inhibitory connections between motor neurons modify a centrally generated motor pattern in the leech hirudo-medicinalis nervous system. Brain Res. 369 (1986) 321-325
19. Granzow B., Friesen W., and Kristan Jr. W. Physiological and morphological analysis of synaptic transmission between leech motor neurons. J. Neurosci. 5 (1985) 2035-2050
20. Haider B., Duque A., Hasenstaub A.R., and McCormick D.A. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J. Neurosci. 26 (2006) 4535-4545
21. Hatton G.I. Synaptic modulation of neuronal coupling. Cell Biol. Int. 22 (1998) 765-780
22. Heckman C.J., Lee R.H., and Brownstone R.M. Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci. 26 (2003) 688-695
23. Heckman C.J., Gorassini M.A., and Bennett D.J. Persistent inward currents in motoneuron dendrites: Implications for motor output. Muscle Nerve 31 (2005) 135-156
24. Heinzel H., Weimann J., and Marder E. The behavioral repertoire of the gastric mill in the crab, Cancer pagurus: an in situ endoscopic and electrophysiological examination. J. Neurosci. 13 (1993) 1793-1803
25. Higley M.J., and Contreras D. Balanced excitation and inhibition determine spike timing during frequency adaptation. J. Neurosci. 26 (2006) 448-457
26. Holt G.R., and Koch C. Shunting inhibition does not have a divisive effect on firing rates. Neural Comput. 9 (1997) 1001-1013
27. Kristan Jr. W.B. Sensory and motor neurons responsible for the local bending response in leeches. J. Exp. Biol. 96 (1982) 161-180
28. Kristan Jr. W.B., McGirr S.J., and Simpson G.V. Behavioral and mechanosensory neurone responses to skin stimulation in leeches. J. Exp. Biol. 96 (1982) 143-160
29. Kristan Jr. W.B., Lockery S.R., and Lewis J.E. Using reflexive behaviors of the medicinal leech to study information processing. J. Neurobiol. 27 (1995) 380-389
30. Kuffler S.W. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16 (1953) 37-68
31. Lewis J.E., and Kristan Jr. W.B. A neuronal network for computing population vectors in the leech. Nature 391 (1998) 76-79
32. Lewis J.E., and Kristan Jr. W.B. Quantitative analysis of a directed behavior in the medicinal leech: implications for organizing motor output. J. Neurosci. 18 (1998) 1571-1582
33. Lockery S., and Kristan Jr. W. Distributed processing of sensory information in the leech. I. Input- output relations of the local bending reflex. J. Neurosci. 10 (1990) 1811-1815
34. Lockery S.R., and Kristan Jr. W.B. Distributed processing of sensory information in the leech II.Identification of interneurons contributing to the local bending reflex. J. Neurosci. 10 (1990) 1816-1829
35. Lockery S.R., and Kristan Jr. W.B. Two forms of sensitization of the local bending reflex of the medicinal leech. J. Comp. Physiol. [A] 168 (1991) 165-177
36. Lucas, B.D., and Kanade, T. (1981). An iterative image registration technique with an application to stereo vision (DARPA). Paper presented at: Proceedings of the 1981 Image Understanding Workshop.
37. Magloczky Z., and Freund T.F. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci. 28 (2005) 334-340
38. Mamiya A., Manor Y., and Nadim F. Short-term dynamics of a mixed chemical and electrical synapse in a rhythmic network. J. Neurosci. 23 (2003) 9557-9564
39. Marin-Burgin A., Eisenhart F.J., Baca M.S., Kristan Jr. W.B., and French K.A. Sequential development of electrical and chemical synaptic connections generates a specific behavioral circuit in the leech. J. Neurosci. 25 (2005) 2478-2489
40. Mason A., and Kristan Jr. W.B. Neuronal excitation, inhibition, and modulation of leech longitudinal muscle. J. Comp. Physiol. [A] 146 (1982) 527-536
41. McAdams C.J., and Maunsell J.H.R. Effects of attention on the reliability of individual neurons in monkey visual cortex. Neuron 23 (1999) 765-773
42. Misell L.M., Shaw B.K., and Kristan Jr. W.B. Behavioral hierarchy in the medicinal leech, Hirudo medicinalis: Feeding as a dominant behavior. Behav. Brain Res. 90 (1998) 13-21
43. Mittmann W., Koch U., and Hausser M. Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J. Physiol. 563 (2005) 369-378
44. Moss B.L., Fuller A.D., Sahley C.L., and Burrell B.D. Serotonin modulates axo-axonal coupling between neurons critical for learning in the leech. J. Neurophysiol. 94 (2005) 2575-2589
45. Muller K.J., Nicholls J.G., and Stent G.S. Neurobiology of the Leech (1981), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
46. Murphy G.J., Darcy D.P., and Isaacson J.S. Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit. Nat. Neurosci. 8 (2005) 354-364
47. Nicholls J.G., and Baylor D.A. Specific modalities and receptive fields of sensory neurons in CNS of the leech. J. Neurophysiol. 31 (1968) 740-756
48. Nicholls J.G., and Purves D. Monosynaptic chemical and electrical connections between sensory and motor cells in the central nervous system of the leech. J. Physiol. 209 (1970) 647-667
49. Ort C.A., Kristan Jr. W.B., and Stent G.S. Neuronal control of swimming in the medicinal leech part 2 identification and connections of motor neurons. J. Comp. Physiol. 94 (1974) 121-154
50. Pouille F., and Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293 (2001) 1159-1163
51. Priebe N.J., and Ferster D. Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45 (2005) 133-145
52. Ribak C.E., Harris A.B., Vaughn J.E., and Roberts E. Inhibitory, GABAergic nerve terminals decrease at sites of focal epilepsy. Science 205 (1979) 211-214
53. Salinas E., and Abbott L.F. Invariant visual responses from attentional gain fields. J. Neurophysiol. 77 (1997) 3267-3272
54. Salinas E., and Thier P. Gain modulation: a major computational principle of the central nervous system. Neuron 27 (2000) 15-21
55. Seutin V., and Johnson S.W. Recent advances in the pharmacology of quaternary salts of bicuculline. Trends Pharmacol. Sci. 20 (1999) 268-270
56. Shadlen M.N., and Newsome W.T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4 (1994) 569-579
57. Stent G.S., Kristan Jr. W.B., Friesen W.O., Ort C.A., Poon M., and Calabrese R.L. Neuronal generation of the leech swimming movement an oscillatory network of neurons driving a loco motory rhythm has been identified. Science 200 (1978) 1348-1357
58. Stevens C.F., and Zador A.M. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1 (1998) 210-217
59. Stuart A.E. Excitatory and inhibitory motoneurons in the central nervous system of the leech. Science 165 (1969) 817-819
60. Stuart A.E. Physiological and morphological properties of motoneurones in the central nervous system of the leech. J. Physiol. 209 (1970) 627-646
61. Taylor A.L., Cottrell G.W., Kleinfeld D., and Kristan Jr. W.B. Imaging reveals synaptic targets of a swim-terminating neuron in the leech CNS. J. Neurosci. 23 (2003) 11402-11410
62. Thomson E.E., and Kristan W.B. Encoding and decoding touch location in the leech CNS. J. Neurosci. 26 (2006) 8009-8016
63. Vogels T.P., and Abbott L.F. Signal propagation and logic gating in networks of integrate-and-fire neurons. J. Neurosci. 25 (2005) 10786-10795
64. Wehr M., and Zador A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426 (2003) 442-446
65. Wilent W.B., and Contreras D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat. Neurosci. 8 (2005) 1364-1370
66. Wolfart J., Debay D., Le Masson G., Destexhe A., and Bal T. Synaptic background activity controls spike transfer from thalamus to cortex. Nat. Neurosci. 8 (2005) 1760-1767
67. Ye M., and Haralick R.M. Image flow estimation using facet model and covariance propagation. In: Yang Y.H., and Cheriet M. (Eds). Vision Interface: Real World Applications of Computer Vision (2000), World Scientific Pub Co, Hackensack, NJ 209-241
68. Yokoi M., Mori K., and Nakanishi S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. USA 92 (1995) 3371-3375
69. Zoccolan D., and Torre V. Using optical flow to characterize sensory-motor interactions in a segment of the medicinal leech. J. Neurosci. 22 (2002) 2283-2298