High speed coding for velocity by archerfish retinal ganglion cells

BMC Neuroscience

Josef Ammermüller²  Malte T Ahlers²  Friedrich Kretschmer¹  Viola Kretschmer² 

[1] Department of Biology and Environmental Sciences, Computational Neuroscience, University of Oldenburg, 26111, Oldenburg, Germany;Department of Biology and Environmental Sciences, Neurobiology, University of Oldenburg, 26111, Oldenburg, Germany

关键词: Latency coding;    Rate coding;    Ganglion cells;    Retina;   

Others  :  1170665
DOI  :  10.1186/1471-2202-13-69

 received in 2012-02-06, accepted in 2012-05-24,  发布年份 2012

【 摘 要 】

Background

Archerfish show very short behavioural latencies in response to falling prey. This raises the question, which response parameters of retinal ganglion cells to moving stimuli are best suited for fast coding of stimulus speed and direction.

Results

We compared stimulus reconstruction quality based on the ganglion cell response parameters latency, first interspike interval, and rate. For stimulus reconstruction of moving stimuli using latency was superior to using the other stimulus parameters. This was true for absolute latency, with respect to stimulus onset, as well as for relative latency, with respect to population response onset. Iteratively increasing the number of cells used for reconstruction decreased the calculated error close to zero.

Conclusions

Latency is the fastest response parameter available to the brain. Therefore, latency coding is best suited for high speed coding of moving objects. The quantitative data of this study are in good accordance with previously published behavioural response latencies.

【 授权许可】

   
2012 Kretschmer et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Timmermans PJ, Vossen JM: Prey catching in the archer fish: does the fish use a learned correction for refraction? Behav Processes 2000, 52(1):21-34.
• [2]Schlegel T, Schuster S: Small circuits for large tasks: high-speed decision-making in archerfish. Science 2008, 319(5859):104-106.
• [3]Wöhl S, Schuster S: Hunting archer fish match their take-off speed to distance from the future point of catch. J Exp Biol 2006, 209(Pt 1):141-151.
• [4]Canfield JG: Temporal constraints on visually directed c-start responses: behavioral and physiological correlates. Brain Behav Evol 2003, 61(3):148-158.
• [5]Canfield JG: Functional evidence for visuospatial coding in the mauthner neuron. Brain Behav Evol 2006, 67(4):188-202.
• [6]Cleland BG, Harding TH, Tulunay-Keesey U: Response to the length of moving visual stimuli of the brisk classes of ganglion cells in the cat retina. J Physiol 1983, 345:27-45.
• [7]Lee BB, Willshaw DJ: Responses of the various types of cat retinal ganglion cells to moving contours. Vision Res 1978, 18(7):757-765.
• [8]Barlow HB, Hill RM, Levick WR: Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J Physiol 1964, 173:377-407.
• [9]Clifford CWG, Ibbotson MR: Fundamental mechanisms of visual motion detection: models, cells and functions. Prog Neurobiol 2002, 68(6):409-437.
• [10]Taylor WR, Vaney DI: New directions in retinal research. Trends Neurosci 2003, 26(7):379-385.
• [11]Oyster CW, Takahashi E, Collewijn H: Direction-selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit. Vision Res 1972, 12(2):183-193. Feb 1972
• [12]Thiel A, Greschner M, Eurich CW, Ammermüller J, Kretzberg J: Contribution of individual retinal ganglion cell responses to velocity and acceleration encoding. J Neurophysiol 2007, 98(4):2285-2296.
• [13]Shadlen MN, Newsome WT: Noise, neural codes and cortical organization. Curr Opin Neurobiol 1994, 4(4):569-579.
• [14]Thiel A, Greschner M, Ammermüller J: The temporal structure of transient on/off ganglion cell responses and its relation to intra-retinal processing. J Comput Neurosci 2006, 21(2):131-151.
• [15]Theunissen F, Miller JP: Temporal encoding in nervous systems: a rigorous definition. J Comput Neurosci 1995, 2(2):149-162.
• [16]Oram MW, Xiao D, Dritschel B, Payne KR: The temporal resolution of neural codes: does response latency have a unique role? Philos Trans R Soc Lond B Biol Sci 2002, 357(1424):987-1001.
• [17]Gollisch T, Meister M: Rapid neural coding in the retina with relative spike latencies. Science 2008, 319(5866):1108-1111.
• [18]Johansson RS, Birznieks I: First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 2004, 7(2):170-177.
• [19]Averbeck BB, Latham PE, Pouget A: Neural correlations, population coding and computation. Nat Rev Neurosci 2006, 7(5):358-366.
• [20]Meister M, Berry MJ 2nd: The neural code of the retina. Neuron 1999, 22(3):435-450.
• [21]Greschner M, Bongard M, Rujan P, Ammermüller J: Retinal ganglion cell synchronization by fixational eye movements improves feature estimation. Nat Neurosci 2002, 5(4):341-347.
• [22]Berry MJ 2nd, Brivanlou IH, Jordan TA, Meister M: Anticipation of moving stimuli by the retina. Nature 1999, 398(6725):334-338.
• [23]Fetcho JR: Excitation of motoneurons by the mauthner axon in goldfish: complexities in a "simple" reticulospinal pathway. J Neurophysiol 1992, 67(6):1574-1586.
• [24]Preuss T, Osei-Bonsu PE, Weiss SA, Wang C, Faber DS: Neural representation of object approach in a decision-making motor circuit. J Neurosci 2006, 26(13):3454-3464.
• [25]Canfield JG, Rose GJ: Activation of mauthner neurons during prey capture. J Comp Physiol A 1993, 172:611-618.
• [26]Ullmann JFP, Moore BA, Temple SE, Fernandez-Juricic E, Collin SP: The retinal wholemount technique: A window to understanding the brain and behaviour. Brain Behav Evol 2012, 79:26-44.
• [27]Tsvilling V, Donchin O, Shamir M, Segev R: Archer fish fast hunting maneuver may be guided by directionally selective retinal ganglion cells. E J Neurosci 2012, 35:436-444.
• [28]Zottoli SJ, Hordes AR, Faber DS: Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell. Brain Res 1987, 401:113-121.
• [29]Segev R, Schneidman E, Goodhouse J, Berry MJ 2nd: Role of eye movements in the retinal code for a size discrimination task. J Neurophysiol 2007, 98(3):1380-1391.
• [30]Greschner M, Thiel A, Kretzberg J, Ammermüller J: Complex spike-event pattern of transient on-off retinal ganglion cells. J Neurophysiol 2006, 96(6):2845-2856.