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The Journal of Neuroscience, February 25, 2009, 29(8):2355-2370; doi:10.1523/JNEUROSCI.3869-08.2009

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Behavioral/Systems/Cognitive
The Sparseness of Neuronal Responses in Ferret Primary Visual Cortex

David J. Tolhurst,² Darragh Smyth,¹ and Ian D. Thompson^1,3

¹Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, United Kingdom, and ²Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom, and ³Medical Research Council Centre for Developmental Neurobiology, New Hunt's House, Guy's Campus, Kings College London, London SE1 1UL, United Kingdom

Correspondence should be addressed to David J. Tolhurst, Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK. Email: djt12{at}cam.ac.uk

Various arguments suggest that neuronal coding of natural sensory stimuli should be sparse (i.e., individual neurons should respond rarely but should respond reliably). We examined sparseness of visual cortical neurons in anesthetized ferret to flashed natural scenes. Response behavior differed widely between neurons. The median firing rate of 4.1 impulses per second was slightly higher than predicted from consideration of metabolic load. Thirteen percent of neurons (12 of 89) responded to <5% of the images, but one-half responded to >25% of images. Multivariate analysis of the range of sparseness values showed that 67% of the variance was accounted for by differing response patterns to moving gratings. Repeat presentation of images showed that response variance for natural images exaggerated sparseness measures; variance was scaled with mean response, but with a lower Fano factor than for the responses to moving gratings. This response variability and the "soft" sparse responses (Rehn and Sommer, 2007) raise the question of what constitutes a reliable neuronal response and imply parallel signaling by multiple neurons. We investigated whether the temporal structure of responses might be reliable enough to give additional information about natural scenes. Poststimulus time histogram shape was similar for "strong" and "weak" stimuli, with no systematic change in first-spike latency with stimulus strength. The variance of first-spike latency for repeat presentations of the same image was greater than the latency variance between images. In general, responses to flashed natural scenes do not seem compatible with a sparse encoding in which neurons fire rarely but reliably.

Key words: visual cortex; sparse coding; natural scenes; ferret; V1; temporal coding

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Received Aug. 14, 2008; revised Jan. 4, 2009; accepted Jan. 9, 2009.

Correspondence should be addressed to David J. Tolhurst, Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK. Email: djt12{at}cam.ac.uk

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