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Clinical Trial
. 2005 Jul 1;566(Pt 1):93-102.
doi: 10.1113/jphysiol.2005.084855. Epub 2005 Apr 21.

Functional evidence for cone-specific connectivity in the human retina

Chara Vakrou  1 , David Whitaker, Paul V McGraw, Declan McKeefry
Affiliations
Clinical Trial

Functional evidence for cone-specific connectivity in the human retina

Chara Vakrou et al. J Physiol. .

Abstract

Physiological studies of colour vision have not yet resolved the controversial issue of how chromatic opponency is constructed at a neuronal level. Two competing theories, the cone-selective hypothesis and the random-wiring hypothesis, are currently equivocal to the architecture of the primate retina. In central vision, both schemes are capable of producing colour opponency due to the fact that receptive field centres receive input from a single bipolar cell - the so called 'private line arrangement'. However, in peripheral vision this single-cone input to the receptive field centre is lost, so that any random cone connectivity would result in a predictable reduction in the quality of colour vision. Behavioural studies thus far have indeed suggested a selective loss of chromatic sensitivity in peripheral vision. We investigated chromatic sensitivity as a function of eccentricity for the cardinal chromatic (L/M and S/(L + M)) and achromatic (L + M) pathways, adopting stimulus size as the critical variable. Results show that performance can be equated across the visual field simply by a change of scale (size). In other words, there exists no qualitative loss of chromatic sensitivity across the visual field. Critically, however, the quantitative nature of size dependency for each of the cardinal chromatic and achromatic mechanisms is very specific, reinforcing their independence in terms of anatomy and genetics. Our data provide clear evidence for a physiological model of primate colour vision that retains chromatic quality in peripheral vision, thus supporting the cone-selective hypothesis.

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Figures

Figure 1
Figure 1. Models proposed for L/M chromatic opponency, based on centre–surround receptive field antagonism
The resulting opponency is determined by the relative weights of the cone input to the centre versus the surround. In the parafovea a ‘private-line’ arrangement exists, where a single cone type (+M here) provides input to the centre of the ganglion cell's receptive field, whilst the surround gets input from another cone type (‘cone-selective’ hypothesis) or from mixed cone types (‘random-wiring’ hypothesis). Chromatic opponency is preserved in both cases. In the peripheral retina midget ganglion cells' receptive fields are much larger and receive convergent input from a number of photoreceptors. The cone-selective hypothesis postulates a selective circuitry where both centre and surround receive input from a single cone type; chromatic opponency is preserved. The ‘random-wiring’ hypothesis postulates mixed input both to the centre and surround of receptive field, resulting in a non-opponent peripheral cell.
Figure 2
Figure 2. Stimuli
Examples of some of the stimuli used for the experiment (A) and their modulation around the MBDKL colour space (B). All stimuli are magnified versions of each other.
Figure 3
Figure 3. Sensitivity as a function of spatial frequency across eccentricity for the three post-receptoral mechanisms
Results show the measured chromatic (L/M (A) and S/(L + M) (B)) and achromatic (L + M (C)) visual sensitivity for two subjects (C.V. and D.W.) at 0, 5, 10 and 20 deg eccentricity. Note that progressively lower spatial frequency stimuli are required for the eccentric positions in order to reach the same level of performance as that at the fovea. ○: 0 deg; □: 5 deg; ⋄: 10 deg; ▵: 20 deg. Average standard error approximated to the size of the data points.
Figure 4
Figure 4. The data of Fig. 3, scaled to account for eccentricity
Scaled data of visual sensitivity for the two observers are shown. For each observer, the graphs from Fig. 3A–C were scaled by an estimated E2 value, and the residual variance was calculated with eqn (3) (for A and B) and eqn (2) (for C). The three parameters of the curve fit were allowed to float in order to minimize the residual sum-of-squares deviation of the combined eccentricity data around the curve fit. With an iterative procedure an E2 value was found to minimize the overall residual variance for each observer: C.V. = 97.41%, D.W. = 94.34% (A); CV = 97.19%, DW = 98.31% (B); CV = 92.81%, DW = 92.75% (C). ○: 0 deg; □□: 5 deg; ⋄: 10 deg; ▵: 20 deg. Very different scaling factors were found for the three post-receptoral mechanisms, each depending upon the axis of colour or contrast.
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