Slow and fast pathways in the human rod visual system - CVRL main

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1662 J. Opt. Soc. Am. A/Vol. 8, No. 10/October 1991ACHROMAT 'aIZ x+ Slow Fast X:5Hz 5Hz c NORMALW8~~~~~5 pV~~~~~~~~~~~~~~N,,- m \ ,.ACHROMAT (ERG)(ERG)0 NORMAL (psycho-,270- physics)17 ~~170i, 0 5 10 15 20so i 1550 200 0 so 100150 200 0 FTime (ms) Time (ms)Frequency (Hz)Fig. 5. Left-hand panel: ERG recordings for the achromat KNmade at a retinal illuminance below his perceptual null (leftrecordings) and at a retinal illuminance above the null (rightrecordings) at frequencies ranging from 5 to 17 Hz. The verticalline in each trace is an estimate of the peak in the ERG recordcorresponding to the flash that occurred at time zero. For theslow pathway there is a delay of 90-115 ms between the flash andthe ERG response; for the fast pathway the delay is 70-80 ms.Right-hand panel: Squares are the phase differences in degreesbetween the slow and fast rod signals for the achromat KN estimatedfrom the ERG records shown in the left-hand panel. Thefilled circles are similar data for the normal subject, also estimatedfrom ERG recordings (not shown). The open circles arephase differences between the slow and fast rod signals for thenormal subject estimated psychophysically. These were obtainedby subtracting the rod-cone phase differences measured justbelow the null (at a time-averaged retinal illuminance of -0.43logio scot. Td) from those measured just above the null (at 0.45logio scot. Td). (See Fig. 6 of Ref. 1.)panel of Fig. 5, in which the phase difference between theslow and fast rod signals in degrees is plotted as a functionof frequency. These data were obtained by a flicker cancellationtechnique, in which the observer is presentedwith rod and cone stimuli flickering at the same frequencyand is asked to adjust their relative phase and retinal illuminanceto cancel the perception of flicker (for more details,see Ref. 1). If rods and cones were equally fast (i.e.,if there were no delay between their signals), flicker cancellationwould be best when the rod and cone stimuliwere physically out of phase. Since the rods are actuallyslower than cones, the rod stimulus must be advanced relativeto the out-of-phase cone stimulus to achieve the null.As predicted by our self-cancellation model, the phasedifference measured psychophysically grows monotonicallywith frequency and reaches approximately 1800 betweenthe slow and fast signals at 15 Hz.If, as we believe, the slow and fast rod signals are differentiatedin the ERG recordings, an electrophysiological estimateof the phase differences between the slow and thefast rod signals should be similar to the psychophysicalestimate. Such estimates can be obtained for both theachromat and the normal observer from the relative delaybetween the slow and fast rod ERG responses. The lefthandpanel of Fig. 5 shows ERG recordings for achromatKN made below the null (left-hand records) and above thenull (right-hand records). In each recording the verticalline is an estimate of the time taken (the delay) for theresponse to the flicker pulse at time zero to appear in theERG. Since the delay of either the slow or the fast rodresponses is roughly constant with temporal frequency,the position of the peak corresponding to the pulse at timezero is roughly the same for all temporal frequencies.The difference in the delay between the slow response(left-hand side) and the fast response (right-hand side) isplotted as a phase difference in degrees by the squares inthe right-hand panel of Fig. 5. The filled circles representsimilar data for the normal subject, also estimatedfrom ERG recordings (not shown). For the normal observerthe phase differences between the slow and the fastrod signals obtained electrophysiologically agree well withthe phase differences determined psychophysically.Further, the estimate obtained electrophysiologically forthe achromat is comparable with the psychophysical andelectrophysiological estimates for the normal observer.4. DISCUSSIONStockman et al.In summary, the flicker detectability data and the ERGrecordings for both the normal observer and the achromatprovide strong support for a duality in the rod visual system,in which rod signals are transmitted through eithera slow, sensitive pathway predominating in dim light or afast, less sensitive one predominating in brighter light.Near 15 Hz, both observers exhibit a region of flicker selfcancellationwell above conventional threshold. This nullseems to be the result of destructive interference betweenslow and fast rod signals that are out of phase with eachother close to 15 Hz. The cancellation is found not onlypsychophysically but also in the ERG. Accompanying thenull is a rapid change of phase. This phase reversal suggeststhat cancellation is indeed the cause of the null:When the two signals are exactly equal in strength and inopposite phase there will be complete cancellation, but,if there is any imbalance in the strengths of the two signals,the result will have the phase of whichever is thestronger signal. In short, there will be a rapid phasetransition of 180° as the 15-Hz fast rod signal equals andthen exceeds the strength of the slow signal, and the transitionwill be accompanied by a flicker null.A. Comparison of Normal and AchromatOne interesting difference between the results for theachromat and those for the normal observer, but one thatseems not to be central to our model, is that the achromat'snull occurs at a higher intensity (compare Figs. 2 and 4).This difference is unlikely to be the result of the normalobserver's cones detecting the target and producing tiny,subthreshold flicker signals because the cone signalswould actually be in phase with the slow rod signals at15 Hz", 3 and out of phase with the fast rod signals. Thustheir effect would be to add to the slow rod signals andcancel the fast ones, so that both the upper and the lowerlimits of the null in the normal observer would be raisedquitethe reverse of what we found..The displacement of the null might instead be caused bya change in the relative strengths of the slow and fast rodsignals between the normal observer and the achromat.If the quickness of the fast rod signals occurs becausethey, but not the slow signals, are transmitted partlythrough a pathway that is ostensibly a cone pathway (oneof the possibilities suggested in Ref. 1), then a deficiencyof cone pathways in the achromat might weaken the fastrod signals and so elevate the null. Histological studies ofthe retinas of totally color-blind observers 2 2 - 2 5 (not all ofwhom may have been typical, complete achromats) differ
Stockman et al.greatly in their results (for a discussion, see Sharpe andNordby,"1 p. 273). Each study divulged the presence ofmorphologically intact cones or conelike structures in theenucleated retinas, even though little or no evidence wasfound for cone function in previous clinical and psychophysicalinvestigations of the subject's vision. In the firsthistological investigation 22 cones were found to be scarceand malformed in the fovea but to be normally distributedand normally shaped in the periphery. However, in thethree subsequent studies 2 3 - 2 5 the cone numbers in thetotally color-blind eye were found to be vastly fewer thanthose found in the normal retina. It is conceivable, therefore,that there are some cones in the eye of our achromatobserver that are structurally malformed or functionallyimpaired or too few in number to provide an independentvisual signal but that suffice to leave intact a vestigialcone system. Although it is unable to contribute to visionper se, this system might provide a weakened pathway forthe fast rod signals.Another difference between the data for the normal observerand for the achromat is that the phase differencebetween the slow and the fast rod signals grows a littlemore quickly for the achromat than for the normal observer(Fig. 5, left-hand panel). One consequence of thiseffect is that the slow and fast rod signals are out of phaseat a lower frequency than those for the normal observer, aresult that is consistent with the need to use 14 Hz ratherthan 15 Hz to improve the null for the achromat. Thesedifferences in phase delay between the achromat andthe normal observer may also be related to the need touse higher-illumination levels to produce flicker selfcancellationin the achromat. The phase delay betweenthe achromat's slow and fast rod signals measured in theregion of his null would be expected to be larger if, forexample, light adaptation differentially speeds up the fastrod signals.B. Other ConsiderationsWhen we describe the rod visual system as being duallyorganized into slow and fast pathways, we are referring inthe first instance to the delay of the two rod responses(see Fig. 5, above), rather than to the shapes of thetemporal-frequency response of the rods. Conner 9 andSharpe et al.' measured the shapes of the rod temporalfrequencyresponses of the slow and the fast rod pathways.At luminances well below the 15-Hz null region, for whichwe assume that the slow pathway predominates, the frequencyresponse is low pass. Similarly, the frequencyresponses measured just below and just above the nullregion are also low pass in shape, but presumably in thisregion neither reflects the exclusive activity of a singlepathway. At higher-luminance levels, for which weassume that the fast pathway predominates, the frequencyresponse becomes bandpass and slightly more extended tohigher frequencies. Thus, in addition to the large differencein response delay between the rod pathways, there isevidence for a change in the shape of the temporalfrequencyresponse.One other aspect of the results shown in Fig. 5 shouldbe mentioned. It is that the phase difference between theslow and fast rod signals falls toward O as the frequencyis reduced. This result argues against a model for thenull in which the cancellation is between a signal and aVol. 8, No. 10/October 1991/J. Opt. Soc. Am. A 1663phase-reversed version of the same signal because such amodel predicts a phase difference of 1800 at all frequencies,not just at 15 Hz as we find.C. Rod-Cone Interactions in FlickerThere is a considerable body of literature on rod-cone interactionsaffecting both cone and rod flicker detection(see, for example, Refs. 26-29). However, there seems tobe no need to invoke any of the reported effects to explainour data, which to a first approximation can be explainedas a simple cancellation between two rod signals. In anearlier paper,' we discussed some evidence for small nonlinearinteractions between the two rod signals.A comparable perceptual null or loss of flicker perceptionhas been demonstrated for suprathreshold mesopicflicker at 7-8 Hz. 4 6 However, we can explain that nullby assuming a cancellation between what we refer to asslow rod signals and cone signals, which are close to outof phase near such frequencies.3-6 As discussed above,the perceptual null near 15 Hz, however, cannot be soexplained.D. Mammalian Rod PathwaysIn the cat-the mammalian species for which we have themost detailed information-there are at least two majorpathways by which rod signals can travel through theretina from the rods to the ganglion cells (see, for example,Refs. 30-32 and Ref. 33 for a recent review). The mainpathway is from rods to rod bipolars, to AII amacrinecells, and then to either ON cone bipolars and ON ganglioncells or to OFF ganglion cells. The secondary pathwayrelies on direct gap junctions between rods and conesthrough which rod signals have access to cone bipolarsand thence to ON and OFF ganglion cells. 34 In the tigersalamander it has been shown that the electrical couplingbetween rods and cones can be strengthened by light. 35Much less is known about the cellular pathways of theprimate retina, but recent evidence suggests that, for theprimate as for the cat, there is always a direct feed betweenthe cone bipolars and ganglion cells, whereas thereis much more amacrine influence and (or) intervention betweenthe rod bipolars and ganglion cells.' 637 And, of the25 amacrine-cell types described so far in the primate,33" 9the A6 can be identified with the All amacrine of thecat.' 9 42 Nevertheless, there may be important differencesbetween the microcircuitry of the cat and the primateretina. For one thing, gap junctions between rodand cone photoreceptors may not be so well developedin primates as they are in lower vertebrates. 4 ' For another,the situation is complicated by the synaptic wiringassociated with the primate's highly developed sense ofcolor vision.E. Site of the Flicker NullThe low-luminance scotopic ERG records shown here arelikely to be predominantly b-wave responses (see, for example,Refs. 44-47). The origin of the b wave has beenknown for some time to be after the receptors 4 " but beforethe ganglion cells. 49 Much evidence suggests that itssource is the glial (Muller) cells 5 0 ' 5 ' and that it is determinedpredominantly by activity in the depolarizing (ON)bipolar cells. 52 ' 5 ' If so, in order for the slow and the fast
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