Rank Order Coding: a Retinal Information Decoding Strategy Revealed by Large-Scale Multielectrode Array Retinal Recordings.
How a population of retinal ganglion cells (RGCs) encodes the visual scene remains an open question. Going beyond individual RGC coding strategies, results in salamander suggest that the relative latencies of a RGC pair encode spatial information. Thus, a population code based on this concerted spiking could be a powerful mechanism to transmit visual information rapidly and efficiently. Here, we tested this hypothesis in mouse by recording simultaneous light-evoked responses from hundreds of RGCs, at pan-retinal level, using a new generation of large-scale, high-density multielectrode array consisting of 4096 electrodes. Interestingly, we did not find any RGCs exhibiting a clear latency tuning to the stimuli, suggesting that in mouse, individual RGC pairs may not provide sufficient information. We show that a significant amount of information is encoded synergistically in the concerted spiking of large RGC populations. Thus, the RGC population response described with relative activities, or ranks, provides more relevant information than classical independent spike count- or latency- based codes. In particular, we report for the first time that when considering the relative activities across the whole population, the wave of first stimulus-evoked spikes is an accurate indicator of stimulus content. We show that this coding strategy coexists with classical neural codes, and that it is more efficient and faster. Overall, these novel observations suggest that already at the level of the retina, concerted spiking provides a reliable and fast strategy to rapidly transmit new visual scenes.
Biovision Team, Inria Sophia Antipolis Méditerranée , F R-06902, Sophia Antipolis, France.
Geoffrey
G
Portelli
Faculty of Medical Sciences, Institute of Neuroscience, Newcastle University , Newcastle-upon-Tyne NE2 4HH, United Kingdom.
John M
0000-0002-7524-6035
JM
Barrett
Faculty of Medical Sciences, Institute of Neuroscience, Newcastle University , Newcastle-upon-Tyne NE2 4HH, United Kingdom.
Gerrit
0000-0001-5008-5493
G
Hilgen
INSERM, U968, Paris, F-75012, France; Sorbonne Universités, UPMC Univ Paris 06, UMR S 968, Institut de la Vision, Paris, F-75012, France; CNRS, UMR 7210, Paris, F-75012, France; Present address: CERCO UMR 5549, CNRS - Université de Toulouse, F-31300, France.
Timothée
0000-0001-8629-9506
T
Masquelier
NetS3 Laboratory, Neuroscience and Brain Technologies Dpt., Istituto Italiano di Tecnologia , Genova, Italy.
Alessandro
A
Maccione
NetS3 Laboratory, Neuroscience and Brain Technologies Dpt., Istituto Italiano di Tecnologia , Genova, Italy.
Stefano
S
Di Marco
NetS3 Laboratory, Neuroscience and Brain Technologies Dpt., Istituto Italiano di Tecnologia , Genova, Italy.
Luca
0000-0001-9521-2812
L
Berdondini
Biovision Team, Inria Sophia Antipolis Méditerranée , F R-06902, Sophia Antipolis, France.
Pierre
P
Kornprobst
Faculty of Medical Sciences, Institute of Neuroscience, Newcastle University , Newcastle-upon-Tyne NE2 4HH, United Kingdom.
Evelyne
0000-0003-3803-257X
E
Sernagor
D000200:Action Potentials; D000818:Animals; D066264:Datasets as Topic; D008810:Mice, Inbred C57BL; D008839:Microelectrodes; D010775:Photic Stimulation; D012165:Retinal Ganglion Cells / Q000145:classification / Q000502:physiology*; D012815:Signal Processing, Computer-Assisted; D013997:Time Factors; D014785:Vision, Ocular / Q000502:physiology*
ganglion cells; multielectrode array; population coding; rank order coding; retina