Role of Spike-frequency Adaptation in Shaping Neuronal Response to Dynamic Stimuli

Overview

Journal Biol Cybern

Specialties Neurology
Physiology

Date 2009 Apr 22

PMID 19381681

Citations 18

Authors

Simon Peter Peron

Fabrizio Gabbiani

Affiliations

Soon will be listed here.

Abstract

Spike-frequency adaptation is the reduction of a neuron's firing rate to a stimulus of constant intensity. In the locust, the Lobula Giant Movement Detector (LGMD) is a visual interneuron that exhibits rapid adaptation to both current injection and visual stimuli. Here, a reduced compartmental model of the LGMD is employed to explore adaptation's role in selectivity for stimuli whose intensity changes with time. We show that supralinearly increasing current injection stimuli are best at driving a high spike count in the response, while linearly increasing current injection stimuli (i.e., ramps) are best at attaining large firing rate changes in an adapting neuron. This result is extended with in vivo experiments showing that the LGMD's response to translating stimuli having a supralinear velocity profile is larger than the response to constant or linearly increasing velocity translation. Furthermore, we show that the LGMD's preference for approaching versus receding stimuli can partly be accounted for by adaptation. Finally, we show that the LGMD's adaptation mechanism appears well tuned to minimize sensitivity for the level of basal input.

Citing Articles

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References

Bhattacharjee A, Kaczmarek L . For K+ channels, Na+ is the new Ca2+. Trends Neurosci. 2005; 28(8):422-8. DOI: 10.1016/j.tins.2005.06.003. View

Gabbiani F, Mo C, Laurent G . Invariance of angular threshold computation in a wide-field looming-sensitive neuron. J Neurosci. 2001; 21(1):314-29. PMC: 6762430. View

Benda J, Hennig R . Spike-frequency adaptation generates intensity invariance in a primary auditory interneuron. J Comput Neurosci. 2007; 24(2):113-36. DOI: 10.1007/s10827-007-0044-8. View

Gabbiani F, Krapp H, Laurent G . Computation of object approach by a wide-field, motion-sensitive neuron. J Neurosci. 1999; 19(3):1122-41. PMC: 6782150. View

Ellis L, Mehaffey W, Harvey-Girard E, Turner R, Maler L, Dunn R . SK channels provide a novel mechanism for the control of frequency tuning in electrosensory neurons. J Neurosci. 2007; 27(35):9491-502. PMC: 6673139. DOI: 10.1523/JNEUROSCI.1106-07.2007. View

Gabbiani F, Krapp H . Spike-frequency adaptation and intrinsic properties of an identified, looming-sensitive neuron. J Neurophysiol. 2006; 96(6):2951-62. PMC: 1995006. DOI: 10.1152/jn.00075.2006. View

Benda J, Herz A . A universal model for spike-frequency adaptation. Neural Comput. 2003; 15(11):2523-64. DOI: 10.1162/089976603322385063. View

Sah P . Ca(2+)-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci. 1996; 19(4):150-4. DOI: 10.1016/s0166-2236(96)80026-9. View

Madison D, Nicoll R . Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol. 1984; 354:319-31. PMC: 1193414. DOI: 10.1113/jphysiol.1984.sp015378. View

10.

Powers R, Sawczuk A, Musick J, Binder M . Multiple mechanisms of spike-frequency adaptation in motoneurones. J Physiol Paris. 1999; 93(1-2):101-14. DOI: 10.1016/s0928-4257(99)80141-7. View

11.

Salkoff L, Butler A, Ferreira G, Santi C, Wei A . High-conductance potassium channels of the SLO family. Nat Rev Neurosci. 2006; 7(12):921-31. DOI: 10.1038/nrn1992. View

12.

Benda J, Longtin A, Maler L . Spike-frequency adaptation separates transient communication signals from background oscillations. J Neurosci. 2005; 25(9):2312-21. PMC: 6726095. DOI: 10.1523/JNEUROSCI.4795-04.2005. View

13.

Fraser Rowell C, OShea M, Williams J . The neuronal basis of a sensory analyser, the acridid movement detector system. IV. The preference for small field stimuli. J Exp Biol. 1977; 68:157-85. DOI: 10.1242/jeb.68.1.157. View

14.

Wicher D, Walther C, Wicher C . Non-synaptic ion channels in insects--basic properties of currents and their modulation in neurons and skeletal muscles. Prog Neurobiol. 2001; 64(5):431-525. DOI: 10.1016/s0301-0082(00)00066-6. View

15.

Gorman R, McDonagh J, Hornby T, Reinking R, Stuart D . Measurement and nature of firing rate adaptation in turtle spinal neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005; 191(7):583-603. DOI: 10.1007/s00359-005-0612-1. View

16.

Peron S, Gabbiani F . Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat Neurosci. 2009; 12(3):318-26. PMC: 2662764. DOI: 10.1038/nn.2259. View

17.

Fotowat H, Gabbiani F . Relationship between the phases of sensory and motor activity during a looming-evoked multistage escape behavior. J Neurosci. 2007; 27(37):10047-59. PMC: 2081158. DOI: 10.1523/JNEUROSCI.1515-07.2007. View

18.

Gabbiani F, Cohen I, Laurent G . Time-dependent activation of feed-forward inhibition in a looming-sensitive neuron. J Neurophysiol. 2005; 94(3):2150-61. PMC: 1804290. DOI: 10.1152/jn.00411.2005. View

19.

Hoger U, French A . Slow adaptation in spider mechanoreceptor neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005; 191(5):403-11. DOI: 10.1007/s00359-004-0597-1. View

20.

Segundo J . Some thoughts about neural coding and spike trains. Biosystems. 2001; 58(1-3):3-7. DOI: 10.1016/s0303-2647(00)00100-3. View