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The Journal of Neuroscience, March 11, 2009, 29(10):3045-3058; doi:10.1523/JNEUROSCI.5071-08.2009

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Behavioral/Systems/Cognitive
Loss of Sensitivity in an Analog Neural Circuit

Bart G. Borghuis,¹ Peter Sterling,² and Robert G. Smith²

¹Howard Hughes Medical Institute, Janelia Farm Research Campus, Ashburn, Virginia 20147, and ²Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6085

Correspondence should be addressed to Bart G. Borghuis at the above address. Email: borghuisb{at}janelia.hhmi.org

A low-contrast spot that activates just one ganglion cell in the retina is detected in the spike train of the cell with about the same sensitivity as it is detected behaviorally. This is consistent with Barlow's proposal that the ganglion cell and later stages of spiking neurons transfer information essentially without loss. Yet, when losses of sensitivity by all preneural factors are accounted for, predicted sensitivity near threshold is considerably greater than behavioral sensitivity, implying that somewhere in the brain information is lost. We hypothesized that the losses occur mainly in the retina, where graded signals are processed by analog circuits that transfer information at high rates and low metabolic cost. To test this, we constructed a model that included all preneural losses for an in vitro mammalian retina, and evaluated the model to predict sensitivity at the cone output. Recording graded responses postsynaptic to the cones (from the type A horizontal cell) and comparing to predicted preneural sensitivity, we found substantial loss of sensitivity (4.2-fold) across the first visual synapse. Recording spike responses from brisk-transient ganglion cells stimulated with the same spot, we found a similar loss (3.5-fold) across the second synapse. The total retinal loss approximated the known overall loss, supporting the hypothesis that from stimulus to perception, most loss near threshold is retinal.

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Received Oct. 21, 2008; revised Jan. 19, 2008; accepted Jan. 20, 2009.

Correspondence should be addressed to Bart G. Borghuis at the above address. Email: borghuisb{at}janelia.hhmi.org

This article has been cited by other articles:

				V. Balasubramanian and P. Sterling Receptive fields and functional architecture in the retina J. Physiol., June 15, 2009; 587(12): 2753 - 2767. [Abstract] [Full Text] [PDF]

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