Journial of Physiology (1992), 458, pp. 579-602 WVith 12 figures Printed in (Great Britain

579

RESPONSES OF MACAQUE GANGLION CELLS TO MOVEMENT OF CHROMATIC BORDERS BY A. VALBERG*, B. B. LEEt, P. K. KAISER: AND J. KREMERS From the Department of Neurobiology, Max Planck Institute for Biophysical Chemistry, D-3400 G5ttingen, Germany

(Received 15 April 1991) SUTMMARY

1. We have measured responses of macaque ganglion cells to moving borders under conditions designed to simulate the minimally distinct border (MDB) task. 2. Extending previous results, we show that minimization of responses of phasic ganglion cells of the magnocellular (MC)-pathway obey the photometric laws of transitivity and additivity. 3. To equal luminance borders, a residual response was present in MC-pathway cells analogous to the second harmonic response seen in these neurones with temporal chromatic modulation. It was proportional to the tritanopic purity difference (IAPtl, the rectified middle- to long-wavelength cone opponent signal) between the two colours on either side of the border. For a APt of one, the mean residual response was equivalent to the response evoked by achromatic borders of about 14 % luminance contrast. Both these properties of the MC-pathway closely resemble psychophysical estimates as to the distinctness of equal luminance borders. 4. We show how MC-pathway cell responses could be used centrally to support the MIDB task. It was difficult to generate a model from responses of tonic ganglion cells of the parvocellular (PC)-pathway which would support the task. 5. The MDB task is still possible psychophysically after blurring the retinal image. Although blurring the border spatially smeared the responses of MC-pathway ganglion cells and reduced their amplitude, responses still went through a minimum close to equal luminance. Thus, blurring the image did not affect the ability of MCpathway cells to support the task. Blurring the retinal image decreased the ' sharpness' of the border response of tonic, PC-pathway ganglion cells, but response amplitude was unaffected. Response features indicative of centre-surround organization were attenuated. A central mechanism reliant on centre-surround field structure of PC-pathway cells would thus not be able to support the task after blurring. 6. Taken together, these results strongly suggest that the MC-pathway forms the * Permanent address: Section of Biophysics, Department of Physics, University of Oslo, Norway. t To whom correspondence should be addressed. t Permanent address: Department of Psychology, York University, North York, Ontario, Canada. MIS 9302

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sole physiological substrate of the MDB task, and any contribution of the PCpathway is, indeed, minimal. INTRODUCTION

In the minimally distinct border (MDB) technique, two precisely juxtaposed, differently coloured fields are adjusted in relative radiance until the border between them is least distinct. This is found to occur when the fields are of equal luminance. Some residual distinctness usually remains. The technique shares with heterochromatic flicker photometry all the characteristics of a photometric method, as exemplified by the original demonstration of photometric additivity (Boynton & Kaiser, 1968). The minimally distinct border is thus parent to more recent experiments with isoluminant patterns (e.g. Cavanagh, Tyler & Favreau, 1984). In the case of flicker photometry, it has been possible to show that cells of the magnocellular (MC)-pathway of the primate visual system possess all the properties required of a physiological substrate of the task (Lee, Martin & Valberg, 1988). Other evidence has further supported the hypothesis that the MC-pathway is the sole physiological substrate for flicker photometry. For example, psychophysical results obtained on changing the relative phase of the two flickering lights are directly reproduced in responses of cells of the MC-pathway (Smith, Lee, Pokorny, Martin & Valberg, 1992). Also, the variety in opponent cone weighting and centre-surround phase delay in parvocellular (PC)-pathway cells makes it difficult to build a convincing model from them with the necessary photometric properties. It is parsimonious to assume that both MDB and flicker photometry rest on the same physiological substrate. We have shown that cells of the MC-pathway display properties consistent with their being the substrate of the MDB task (Kaiser, Lee, Martin & Valberg, 1990). On adjusting the luminance contrast across a border between two different colours, activity in the MC-pathway goes through a minimum when the colours are at equal luminance. However, there appears a residual, rectified-opponent response in this pathway, analogous to the frequency-doubled response found with temporal chromatic modulation of a uniform field (Lee, Martin & Valberg, 1989a). With different wavelengths tested against a white field, this residual response changes as a function of wavelength in the same way as residual distinctness reported by human observers. Thus, cells of the MC-pathway not only provide a signal which can support the MDB task, they also provide a signal which can account for the magnitude of residual distinctness at equal luminance. These results do not rule out the possibility that cells of the PC-pathway are also involved in the task. For example, it is possible that PC-pathway signals are combined to form an 'achromatic channel' at some later stage in the visual system. Data from experiments in which differential lesions of PC- and MC-pathways have been attempted (Schiller, Logothetis & Charles, 1990) might support such a hypothesis. We may thus distinguish two alternative hypotheses as to the physiological substrate of the MDB task. Either the MC-pathway is the sole substrate, or some combination of MC- and PC-pathways is involved. Previous results (Kaiser et al. 1990) were consistent with the former alternative. One aim of the experiments reported here was to explore the second alternative. Firstly, we provide a detailed demonstration of photometric additivity and

LK GANG(LION CELL BORDER RESPONSES AMAC(AQU

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transitivitv in MC-pathway cells. Secondly, we show that residual responses of MCpathw\ay cells at equal luminance are proportional to the tritanopic purity difference between the colours on either side of the border, as is the case for psychophysical residual distinctness estimates (Valberg & Tansley, 1977). Tritanopic purity difference is a measure of the IL-Ml cone difference signal and is defined in the Methods section. Thirdly. we consider how more central mechanisms may utilize MCand PC-pathway signals. Fourthly, we consider the effect of defoeusing the border on cell responses, since blurring the retinal image is known to have little effect on MDB (Lindsey & Teller. 1989). The observations, taken together, make it likely that MCpathway cells provide by far the most significant contribution to border distinctness as assessed psychophvsically wAith the minimally distinct border. A short report of these results has been presented (Valberg. Lee & Kaiser, 1990). METHODS

Ganglioni cell activity was recorded from the retinae of juvenile macaques (iiacacafasaicularis). After initial anaesthesia bv intramuscular injection of ketarnine, thereafter anaesthesia was maintained with halothane or- isofluorane in a 70 %-30 % N20-02 mixture (1--2 % during surgery, and 0 2-1 % during recording). Local anaesthetic was applied to points of surgical intervention. EEG and E(-C'(G were continuously monitored as a control for anaesthetic depth. Muscular relaxation was provided by infusion of gallamine triethiodide (5 mg kg-1 h-1) together with ca 5 ml h-1 of dextrose Ringer solution. End-tidal PIto was kept near 4 % by adjusting the rate and depth of ventilation, and body temperature was maintained near 37-5 'C. Further details of the experimental procedulre are giveen in Kaiser et al. (1990) and details of recording technique and cell classification are to be founid in Lee, Martin & Valberg (1989b). WTe recorded from ganglion cells from parafoveal retina. V'isual stimulation Visual stimuli are described in detail elsewhere (Kaiser et al. 1990). Briefly, two projectors (Leitz, Prado) provided orthogonal light beams. A front surface-silvered coating was deposited on half a glass flat to give a mirr or edge. The glass was positioned at 45 deg to the stimulus beams. A lens brought the mirror edge into focuts on a back-projection screen. On the way to the screen, the beam was reflected off a front suirface-silvered mirror mounted on a galvanometer. Rotation of this mirror provided stimultus inovement. The unfiltered projector light could provide white reference fields with CIE (Commission Internationale de lEclairage chromaticity co-ordinates (x and y) = (0404, 0-410), or the spectral composition of each half'-field could be adjusted with interference filters (NAL, 25 nm halfbandwidth at half'-maximum: Schott, AMainz, Germany). Neutral-densitv filter wheels in each stimulus beam allowed the intensities of each half-field to be changed by the computer system which also averaged and stored cell responses. A Photo Research 702A/703A Scanning Spectrophotometer (Burbank, CA, USA) was used to measure the radiance distribution (390-760 nm) and the 2 deg luminance and chromaticity co-ordinates of the stimuli. Since cell receptive fields were parafoveal (4 15 deg eccentricity), we converted these values to the CIE 10 deg luminosity function for our calibrations and calculations (Valberg, Lee & Tryti, 1987). XVith a 2 mm artificial pupil, the retinal illuminance was usually 80 trolands (td). For the additivitv experiments, a third projector was installed and its beam combined with that of the test beam, allowing us to mnix two wavelengths on one side of the border in any given proportion. Cells' receptive fields were cenitred on a 5 deg field across which the edge was moved. UJsuallv a movement of 1 deg was used, but in somne experiments larger excursions were also tested. For each condition, cell responses to a series of relative luminances across the edge were measured, the range being adjusted to straddle the point of equal luminance. Fourteen to twenty responses to each edge movement were averaged and stored as a peristimulus time histogram of 128 bins. For clarity of illustration, a resolution of sixtv-four bins is shown in the figures, with a binwidth of 4 ms. An analogue oultput from a spot photometer (Photo Research) was also stored, to give us a record of the luminaince modulation over a cell's receptive field.

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For phasic cells, response amplitude was measured in a window (80 ins at 4 deg s-1) centred on the response peak. Maintained activity (derived from the mean of twenty bins at the beginning and twenty bins at the end of the histogram) was then subtracted. Negative responses thus reflect a suppression of maintained activity. The responses of tonic cells were so sustained (see Fig. 9) that A

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Dominant wavelength (nm) 1. A. Fig. tritanopic purity (defined as in the text) as a function of dominant wavelength. Points indicate the filters used, and the radiance peak wavelengths (in nm) of the lights generated are shown. The dashed line is the tritanopic purity of the white reference, relative to that of equal energy white. Tritanopic purity difference is the separation between a pair of points on the ordinate, In B this difference is plotted for the different wavelengths relative to the white reference used. a different procedure had to be adopted. Mean firing rates over thirty bins (120 ins) before and after the edge passed over the receptive field centre wNere measured and the difference between these values used as the cell's response. WAe tested using other window widths for phasic cells, and we tried using a peak r-esponse measure for tonic cells. These manipulations changed response amplitudes, but the pattern of curves obtained remained similar to those presented in the figures. We use here tritanopic purity difference as a measure of the IL -Ml cone difference signal across the border at equal luminance (as defined using the CIE 10 deg V&, and calculated as described in Valberg et al. 1987). With two lights having a difference of zero, only the S-cone signals a difference between them. Tritanopic subjects, lacking S-cones, are unable to distinguish such pairs of lights. Valberg & Tansley (1977) defined tritanopic purity, Pt, as proportional to (R - G)/(R + G), where R and G were normalized excitations of the L- and M-cones. Between two fields, the tritanopic purity difference is APt = Pl -Pt2. Figure I A shows tritanopic purity as a function of wavelength relative to an equal-energy white. The lights used in these experiments are indicated by points on the curve. They are situated on the curve according to dominant wavelength, which differed somewhat from peak wavelength measured with the spectrophotometer due to the broad half-bandwidth of the filters (25 nm). The radiance peak wavelengths are indicated on the curve next to each point. These latter values are those cited in the text. The absolute value of tritanopic purity difference, APtl, between two filters is their separation on the ordinate. This is indicated in Fig. 1 B, in which IAPJ for the different filters compared with the white reference has been plotted. The curve has a form resembling that of residual responses in the MC-pathway for different wavelengths relative to the white reference (Kaiser et al. 1990; Fig. 13). RESULTS

We report here on data collected from forty-two phasic and twenty-eight tonic ganglion cells from the macaque retina. Different members of these groups were

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tested with the different stimulus conditions described. We are confident, on the basis of tests summarized elsewhere (Kaiser et al. 1990), that cells classified as phasic belonged to the MC-pathway and those classified as tonic belonged to the PCpathway.

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Fig. 2. Responses of typical phasic MC-pathway cell demonstrating additivity. An edge, bordered by the wavelengths indicated, was moved back and forth across the receptive field. The luminance ratio (LA/Lw,; based on 10 deg lA sensitivity) across the border was systematically varied around unity as indicated on the abscissa. Examples of histograms for the two directions are shown, next to the relevant points. The points represent firing rate in peak response (80 ms) with maintained activity subtracted. The luminance ratio of minimum response for the cell is derived from the intersection of the curves for the two movement directions, and the amplitude of residual response by the distance q. Luminance ratio of minimum response is close to unity under all conditions, indicating transitivity. Four deg s-' movement speed, average of twenty sweeps, 64 bins sweep-', 4 ms bin-'.

A. VrALBERG A-ND OTHERS

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Tra,n.sltivity anadl additirity in phasic, MC-pathway cells WNhen different wavelengths w,ere tested against a white reference, the mean spectral sensitivity of MC-pathway cells closely mnatched the CIE 10 deg VA function and transitivity, a(lditivity and proportionality of cells in this pathway were briefly 414 nm 430 nm 460 nm 508 nm 548 nm 568 nm 590 nm 646 nm 688 nm White

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lFig. 3. Distribution of iluinance ratio of miniimum responses for two phasic cells for a large variety of -wa,velength conmbinations; those used are indicated in the key.

described (Kaiser et al. 1990). W'e now present more detailed demonstrations of' transitivity and additivity, wlhich are essential properties of a photometric measure. Figure 2 shows response histograms and measuremients of response amplitude for a phasic off-centre ganglion cell. The results illustrate the method of analysis and the principle of transitivity. Heterochromatic borders were moved back and forth across the receptive field, and the two directions of movement are distinguished by filled and open symbols and histograms. Two wavelengths were tested against a white reference lioht and then against one another. The luminance ratio across the border was changed in 01 log unit steps. When the luminance ratio is far from unity, a vigorous off-response can be seen to one direction of movement, and no response or a suppression of maintained firing to the reverse direction. As seen from peak firing rate curves. as equal luminance is approaclhed response amplitude becomes less, and close to equal luminance the two curves intersect to form a minimum, although some residual response is present for movements in both directions, as can be seen from the histograms. We drop a perpendicular from the intersection onto the abscissa, to give the lumninance r atio of the response minimum. The amplitude of the residual response is given by the distance q. For the 646-508 nm condition, q was approximately the sumn of when these wavelengths were tested against the white reference, because the tritanopic purity difference adds for these conditions. The amplitude of residual responses as a ftunction of tritanopic purity difference is discussed in a later sectionl. Transitivity (if A = B and B = C then A = C) implies that if the minima for 508 nm and white, and for 646 nm and white are both at equal luminance, then the

585 MACAQlJE GANGLION CELL BORDER RESPONSES comparison of 508 and 646 nm should also display a minimum at equal luminance. The results in Fig. 2 indicate that transitivity holds for this ganglion cell. When two wavelengths were tested against a white reference, a minimal response was evoked close to a luminance ratio of one, and this was also the case when they were tested against one another. In Fig. 3 is shown a more extensive demonstration of transitivity. For two phasic cells, responses to a large number of pairs of lights were measured. White, 646, 568, 508 and 460 nm were used as reference lights and were tested against those shown in the key. The histograms show the distributions of the luminance ratios of response minima, measured as in Fig. 2. Luminance ratios cluster around unity. This demonstrates that transitivity applies. Similar data were acquired for six other neurones. Some variability in the distributions in Fig. 3 may be due to cells' spectral sensitivities not precisely matching the VA curve due to intercell variability in L/Mcone weighting (Kaiser et al. 1990). A small but systematic deviation from VA sensitivity was demonstrable for the cell in the right-hand panel of Fig. 3, consistent with a deviation from the L/M-cone weighting expected of the VA function. We now examine the assumptions involved in extrapolation of physiological results to the psychophysical task of additivity (Boynton & Kaiser, 1968). Two chromaticities (534 and 626 nm) were each tested separately against a white reference field. They were then mixed in different proportions and the mixture tested against the white reference field. The retinal illuminance in trolands for each wavelength at each minimal response was calculated, and the two values plotted against one another, as in an earlier psychophysical analysis (Boynton & Kaiser, 1968). Eight cells were tested, and three are shown in Fig. 4A-C. For each cell, a straight line relationship provides an adequate description of the data. This indicates that additive combinations of these wavelengths give mixtures which 'match' the white reference. The slope of the regression line varied from cell to cell. This is likely to arise from variation in the L/M-cone weighting. An analogous result was obtained when different wavelengths were tested against the white reference (Kaiser et al. 1990). From the cone fundamentals and the spectral distributions of the 534 and 626 nm lights, it was possible to calculate their M- and L-cone excitations (Valberg et al. 1987). We have drawn the slopes expected had the L- or M-cone been the sole input to a cell in each panel. Slopes for the eight cells varied between these extremes, as may be seen in Fig. 4A-C. For the eight cells studied with this protocol, averaged results are shown in Fig. 4D. The mean slope was - 101 (S.D. 0 38, n = 8), as expected from the VA function. Standard deviations of individual points can be seen to be greater toward the ends of the line rather than in the middle, reflecting the variability in slope of the linear relationships for individual cells, causing the regression lines to rotate about the intersection of the dashed M- and L-cone lines. The results presented in Figs 2-4 show that the requirements of photometric linearity are directly met by the MC-pathway.

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Responses to borders at equal luminance After subjects minimize border distinctness, they report that the magnitude of residual distinctness depends on the chromnaticities on either side of the border. Residual distinctness is almost linearly related to the tritanopic purity difference A 100 80

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Fig. 4. Demonstration of additivity on a populationi of phasic cells. A --C examples of three individual neurones. Various proportions of 534 and 626 nm lights were tested against an 80 td white reference. Trolands of 534 nm light at the cell's response minimum are plotted against trolands of' 626 nm. All cells display a straight line relationship (indicating each cell showed additivitv) of variable slope. The interrupted lines indicate the slopes expected if the cell were to receive input solely from the M- or L-cone. Slopes of all cells' regression lines were within these limits. D. with values averaged from eight neurones, the slope of the regression is close to - 1. as expected from VA sensitivity. Standard deviations are minimal around the intersection of the M- and L-cone lines, indicating the regression lines of the individual cells formed a distribution which rotated around this point.

between the two lights. Tritanopic purity difference, as defined in the Methods section, is a measure of the IL-MI-cone difference signal across the border at equal luminance. When two lights of equal luminance are exchanged, either with temporal chromatic modulation of a uniform field or with a, moving border, phasic cells of the MC-pathway give a response at twice the modulation frequency, or to both directions of border movement. Present results strongly resemble our earlier data using chromatic modulation, both in terms of absolute response amplitude and its linear relationship to IAPtl as described below (Lee et al. 1989 a; Fig. 3). When different wavelengths were tested against white. residual border responses of phasic ganglion cells varied across the spectrum in a way strongly resemnbling psychophysical data on

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residual distinctness (Kaiser et al. 1990). This suggested that the residual response of these cells might also be related to tritanopic purity difference. Wre specifically tested this hypothesis on a sample of nineteen phasic cells using different wavelengths against a white reference and against a number of other reference wavelengths. The

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Fig. 5. The amplitude of the residual response at equal luminance is plotted against tritanopic purity difference for four phasic cells. Different test wavelengths selected from those in Fig. 1 were tested against the reference wavelengths indicated in each panel. For each cell, a linear relationship holds, although its slope varies.

amplitude of residual response, q, was derived as in Fig. 2, and plotted against tritanopic purity difference, IAPtl. Figure 5 shows typical results from four phasic cells, two on- and two off-centre. About six wavelengths, selected from those shown in Fig. 1, were tested against a white reference and against other reference wavelengths, as indicated. Residual responses are well described by a linear relationship, after a small lPtl threshold was exceeded. Similar results Nere obtained from the other cells. The results in Fig. 5 resemble the similar analysis of frequency-doubled responses to temporal chromatic modulation (Lee et al. 1989a; Fig. 3). The slope of the relationship varied from cell to cell, but was not significantly different for on- and off-centre cells. The slope averaged 35 imp s-' per unit of tritanopic purity difference at a 4 deg s-' movement speed for a sample of nineteen cells. The linear relationship appeared to obtain after a small purity difference

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threshold had been exceeded (mean threshold IA/PI = 015, S.D. 007, n = 19). Variability in slope was considerable (S.D. = 14 0 imp s-i per unit purity difference). For each cell in the sample, responses to an achromatic border were available (see Kaiser et al. 1990). A 20% achromatic contrast evoked an average response of 52 imp s-' at 4 deg s-5. The residual response with a IA^Il of one would then be equivalent to a response to approximately 140% achromatic contrast. These results may be related to psychophysical data summarized by Valberg & Tansley (1977; Figs 2, 5 and 6). In one study, for three subjects the mean threshold for zero distinctness corresponded to a ANPtl = 0 11. In that study, mean equivalent achromatic contrast with a IAPtl of one was 19%. In two other studies (Valberg & Tansley, 1977, Fig. 5; and Frome, Buck & Boynton, 1981) the latter value was 14 and 15% respectively. All these values comnpare closely to the physiological data. We also analysed the amplitude of residual responses as a function of speed of movement across the retina. This is of interest for two reasons. Firstly, residual responses could partly be due to a differential chromatic adaptation effect to the colours making up the border. If so, then residual responses, when compared to the response to luminance contrast, should be relatively larger with slow stimulus movement, because slower moveinent should offer a longer opportunity for chromatic adaptation. Secondly, the role of naturally occurring eye movements in MDB is of interest. Either slow drift movements or correctional microsaccades could evoke responses from cells during viewing of a border by an observer. For a given eyemovement velocity, direction relative to a border (i.e. whether at right angles or some other orientation) will modify speed of translation of the border across the retina, for a given eye-movement velocity. It is thus desirable to know if residual responses retain a constant ratio to a luminance contrast response as velocity varies. Figure 6 shows the relationship between movement speed and residual response to a 508-626 nm pair of lights for two cells, compared with the response to the same pair of wavelengths but with a substantial luminance contrast (ca 35 %; results for the two contrast directions are shown). Response amplitude increases with movement speed in a parallel manner for all three curves up to 4-8 deg s-', but above this velocity residual response at equal luminance (E) falls off while the response to luminance contrast (O and 0) continues to increase. Sitmilar results were obtained from all six cells tested. The decrease in residual response at high movement speeds is presumably analogous to attenuation of frequency-doubled responses (relative to the fundamental) with temporal chromatic modulation above 20 Hz (Lee et al. 1989a). The combined results from these earlier experiments and those in Fig. 6 suggest that differential chromatic adaptation does not make a major contribution to residual responses. They also suggest that a residual response corresponds to a constant achromatic contrast up to about 8 deg s-'. It should be noted, however, that these data refer to cells of the parafovea; for foveal ganglion cells, with smaller receptive field centres, the data probably translate to slower movement speeds. For three cells, curves such as those in Fig. 5, relating residual response to tritanopic purity difference, were obtained at different movement speeds, with similar linear relationships but different slopes. For three further phasic cells, we investigated residual responses as a function of retinal illuminance over a two log unit range (from 8 to 800 td). The luminance ratio

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of minimum response remained near one, indicating proportionality. Oni average, residual responses increased by (a 35 imp s- for each log unit increase in illuminance. A similar result was observed with the frequency-doubled responses of phasic cells to temporal chromatic modulation (Lee et al. 1989a). 200

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Fig. 6. Amplitude of response to a 508-626 nm border under three conditions as a function of movement speed for two phasic cells. In t-o conditions a luminiance imbalance was presenit (corresponding to the maximal and minimal values in Fig. 2), of ca 35% Michelson contrast in each case. In the third condition, the residual response at equal luminance has been plotted. Up to 8 deg s-', the residual response increased at approximately the same rate as the luminance conitrast response. At the highest speed tested (16 deg s-m) the luminance response increased further but the residual response

decrleased.

Although residual responses in the MC-pathway at equal luminance provide a signal adequate to account for the magnitude of psychophysical residual distinctness, it is possible that tonic ganglion cells of the PC-pathway also contribute to residual distinctness. Since tritanopic purity is related to the IL-Ml cone excitation difference, those ganglion cells with input only from these cones will also give a response related to tritanopic purity difference. For twelve tonic cells, we measured responses to numerous spectral combinations. Amplitude of response is plotted against tritanopic purity difference, APtI, in Fig. 7, for three red-green opponent cells with only M- and L-cone input (A-C) and one blue-on cell with excitatory input from the S-cone (D). Histograms of responses of tonic cells to equal-luminance borders can be seen in Fig.

to. For the cells in Fig. 7A-C, response magnitude first increased linearly as a function of tritanopic purity (with no apparent threshold), and then tended toward an asymptote. Saturation of responses of these cell types is common at high chromatic contrasts (Valberg et al. 1987). Although the tritanopic purity at which this asymptotic behaviour became apparent varied from cell to cell, it generally was visible above a IAPtI of 12.

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For a blue-on cell the response bears no relation to tritanopic purity difference, being dependent on relative S-cone and surround activations (Fig. 7D). Structuire of ganglion cell border responses The method of analysis shown in Fig. 2 implicitly assuimes somne central mechanism which uses the MC-pathway signal to provide a substrate for the MDB task. Were A 100

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combinations indicated. A-C, three cells with only M- anid L-cone input. Response (derived from the firing rate before and after the border passes across the receptive field) increases as a functioni of tritanopic purity, but typically displays some degree of response saturation at, tritanopic purities greater than one. D, response bears no relation to tritanopic purity difference for a blue-on cell with excitatory S-cone input.

responses of PC-pathway cells to contribute to MDB, there are also assumptions as to how their signals might be combined so as to provide an achroma-tic signal which might support psychophysical performance. We test here both of these sets of assumptions using actual cell responses. We would stress that the models described are arbitrarily chosen to exemplify the kinds of central mechanism which must be postulated. Other models are possible, the feasibility of which are taken up in the

discussion. In the case of MC-pathway ganglion cells, response minima were estimated from intersections of curves for the two directions of movement, as in Fig. 2. This analysis thus implies comparison of responses to the two movement directions. During the psychophysical performance, it is more plausible to assume that signals of neighbouring on- and off-centre cells are combined or compared within a single eye movement. Existing models of cortical receptive fields include plausible structures for such combination. For example. an odd-symmetric receptive field, as dem-

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onstrated in simple cells of the cat striate cortex (Movshon, Thompson & Tolhurst, 1977), has suitable properties. A sketch of how such a receptive field might be constructed is shown in Fig. 8A. To test the feasibility of this model, we took on- and off-centre phasic cell responses and added them after introducing a suitable spatial displacement to generate an oddOdd-symmetric field+

A

Moving edge

/ e4 \_s@' \

B

'Achromatic' sum

Green-on

=

+ Red-on

0

Moving edge

Fig. 8. Possible models of receptive field organization of central mechanism which might process phasic and tonic cell signals. A, phasic cell model. An on- and an off-centre cell with neighbouring receptive fields provides input to a cortical mechanism, thus generating a cortical odd-symmetric receptive field profile. B, tonic cell model. Concentric green-on and red-on receptive fields combine to generate at a cortical level a receptive field with an achromatic profile.

symmetric receptive field. A spatial displacement of 10 min of arc was used; this corresponds approximately to receptive field centre diameter at this eccentricity (Crook, Lange-Malecki, Lee & Valberg, 1988). Figure 9 presents a detailed examination of such a model's properties using data from two sequentially recorded MC-pathway cells with nearby receptive fields. Responses at equal luminance and at two other luminance contrasts are shown, for four conditions ordered from top to bottom according to tritanopic purity. For all conditions, the peak firing rate of the combination goes through a minimum for the central set of histograms at equal luminance. With a luminance contrast present (histograms at left and right) the peak firing rate of the combination is larger and resembled the envelope of curves such as those in Fig. 2. The residual response increases from top to bottom with the increase in tritanopic purity difference. Thus an odd-symmetric receptive field model would provide a satisfactory construct to support performance on the psychophysical task. It has also been suggested that outputs of PC-pathway cells may be combined into an achromatic mechanism which might support MDB (e.g. Ingling, 1991). A suitable

A. VALBERG AND OTHERS

592

White - 568

nm,

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Fig. 9. Test of phasic cell model using responses from on- and off-ganglion cells with nearby receptive fields. As examples, responses at three luminance ratios have been additively combined, after introducing a lateral displacement of 10 min of arc. Four different wavelength combinations are shown. For white-568 nm, the combined output goes through a minimum at a luminance ratio of one, with no residual response, since

MACAQUE GANGLION CELL BORDER RESPONSES

593

model is shown in Fig. 8B. A red (L-M) and a green (M-L) on-centre cell combine to provide a receptive field with summed lMi- and L-cones in the centre and in the surround. This should provide a non-opponent signal. To test such a possible combination of PC-pathway cells, we added responses from pairs of red and green on-centre cells. The rationale behind this test was to take a pair of cells with similar response amplitudes, and slide the response histograms so that their combination added under some specific condition (usually a 626-508 nm border at equal luminance) to yield as small a perturbation of firing rate as possible. Then, the same rule of addition was applied under a variety of other conditions. If the model in Fig. 8B were viable, then the combined responses so generated should show a minimum at equal luminance over the conditions tested. A detailed examination of a cell pair with similar retinal eccentricities is shown in Fig. 10, using the same spectral combinations as in Fig. 9. Five different luminance ratios are shown, straddling equal luminance. For the 626-508 nm condition, the histograms were shifted in space and added so as to give a minimum response at equal luminance. The same manipulation was then applied for all the other sets of histograms. Under the 626-508 nm condition, there is little perturbation of firing rate at equal luminance. However, using the same rule of combination of responses for the 508 nm-white and 646 nm-white conditions does not yield a suitable signal for minimization of border distinctness. Even for the 626-508 nm condition, the combined signal is relatively insensitive to introduction of a luminance imbalance, in comparison with the MC-pathway model in Fig. 9. For the 568 nm-white condition, neither cell gives a response at equal luminance, since these stimuli lie close to a tritanopic confusion line, and can be distinguished only by a cell which has S-cone input. We combined four other pairs of red- and green-on cells, with similar results to those in Fig. 10. The analyses in Figs 9 and 10 show that it is readily possible to conceive of a central mechanism for MDB based on MC-pathway activity, but it is more difficult to combine activity of PC-pathway cells to generate a suitable mechanism for MDB, despite the superficial plausibility of such a model as that in Fig. 8B.

Defocusing the retinal image A model such as that in Fig. 8B would no longer function if a border were blurred, since centre and surround would not be resolved by the blurred stimulus. Blurring the retinal image has little effect on psychophysical performance on the MDB task (Lindsey & Teller, 1989). This manipulation is thus of interest with respect to its effect on cell responses. Also, retinal blur induced by a 5 dioptre lens before the eye can reduce psychophysical sensitivity to an achromatic contrast by up to a factor of ten while sensitivity to chromatic contrast is almost unaffected (Valberg, Seim & Lee, 1991). Insofar as detection of achromatic contrast rests on MC-pathway activity, one might expect that defocusing the image should result in attenuation of the response of phasic MC-pathway cells, but the chromatic response of tonic, PCpathway cells should reinain unaffected. these two lights lie close to a tritanopic confusion line. For 508-626 nm, the combined output goes through a minimum at a ratio of one, but a significant residual response is present.

A. VALBERG AND OTHERS

594

White - 568 nm, APt 0 01

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Fig. 10. Detailed test of tonic cell model using responses from red-on and green-on cells at similar retinal eccentricities. Four different wavelength combinations are shown at five different luminance ratios. The cell responses were adjusted along the abscissa so that under the 508-626 nm condition there is no response at equal luminance. For the white-568 nm condition, the model performs satisfactorily, for the cells individually show a minimum response to this pair of tritanopic lights at equal luminance. With the other combinations, no signal which might be useful for minimizing border distinctness emerges. Even for the 508-626 nm condition, the response as luminance ratio is increased above a luminance ratio of unity is small and of irregular polarity. The tonic cell model thus does not appear to work well.

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We studied the effects of defocusing the image on eleven phasic and six tonic ganglion cells. The defocusing used was optical by means of a 5 dioptre lens before the eye, and spread the retinal image so that 90 % of the luminance change occurred over ca 30 min of arc. An equivalent Gaussian blur would have a standard deviation of about 10 min of arc. A

B

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Fig. II. Response of phasic cell to a 626-508 nm border, before and after defocus (5 dioptre before eye). An equivalent Gaussian blur would have had a standard deviation of around 10 min of arc. The edge was moved back and forth across the receptive field (r.f.) of the cell. A, original response histograms for three luminance ratios to the two directions of movement. Under the defocus condition, the response is smaller and less spatially welldefined. However, plots of firing rate against luminance ratio (B) show a minimum close to equal luminance under both conditions.

Results obtained from a phasic ganglion cell are shown in Fig. 11. Responses at equal luminance are shown, as well as those with a luminance contrast. We chose a cell with a particularly vigorous residual response, to demonstrate that this is not totally abolished by defocusing. Individual responses are spatially smeared by the defocusing procedure, and substantially decreased in amplitude. Nevertheless, when peak firing rate is plotted as a function of luminance ratio in Fig. 11 B, it can be seen that the pairs of curves still intersect at the same luminance ratio, close to one. The other ten neurones yielded similar sets of curves. Results for a green-on and a red-on ganglion cell are shown in Fig. 12A and B, for a red-green border. The most obvious response to the border moving across the field is a sustained change in firing. Although, as shown in Fig. 10, peaks which might reflect centre-surround organization are not large, they may be discerned at some luminance contrasts. On blurring the image, the response becomes smeared out in space and any indication of spatial structure in the response has been largely abolished. Response magnitude, measured as the difference in firing in 30 ms windows just before and after the border passes across the field, is plotted as a function of luminance ratio in Fig. 12 C and D. Response magnitude remains almost unaffected by defocus. Since this partly reflects the fact that the measure used was selective for the sustained component of the response, we also tried an analysis using

A. VALBERG AND OTHERS

596

the same peak measure as for phasic ganglion cells, to try and pick out any luminance component in the response. Defocus then decreased response magnitude due to the more gradual change in firing, but the forms of the curves remained similar to those in Fig. 12C and D. Similar results were obtained from four other neurones. Focus

A

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Fig. 12. Response of green-on (A) and red-on (B) tonic cells to 626-508 nm border moved across the receptive field (r.f.) of the cell with and without defocus (5 dioptre before eye). A and B, original response histograms show the very sustained responses typical for tonic cells. Response onset and offsets are less abrupt after defocus. C and D, plot of firing rate as a function of luminance ratio in the two conditions. In order to make a response assessment which should be sensitive to any luminance component buried in the cell's response, a similar peak firing rate measurement was used as for phasic cells. No significant difference between the two conditions can be seen. This confirms the unsuitability of tonic cell responses for supporting the minimal distinct border task.

Defocusing the retinal image thus has the expected effect on both types of ganglion cell. Only the MC-pathway could readily support the psychophysical task after blurring of the image. DISCUSSION

We have argued previously that responses of the phasic ganglion cells of the MCpathway are suitable as a physiological substrate of the minimally distinct border task (Kaiser et al. 1990). To further consolidate this linking hypothesis, we have demonstrated here that the MC-pathway possesses linear photometric properties, so

AIACQUVE GANGLION CELL BORDER RESPONSES7 597 that transitivity and additivity may be derived from the minimla in responses of this cell systemn. Secondly, we show that at equal lumninance the residual, rectifiedopponent response in the MC-pathway are pr oportional to tritanopic purity difference, as for psychophysical residual distinctness, and of appropriate inagnitude to account for the psyehophysical result. Thirdly, we show that MC-pathway activity can be used to support the MDB task, given a simple cortical model for comparison of on- and off-centre cell signals. On the other hand. an 'achromatic' or 'brightness' channel derived from PC-pathway activity is less plausible as a physiological substrate for MDB. Lastly, blurring the retinal image continues to allow the MC-pathway to support mninimal distinct border performance. Any PCpathway model depending on centre-surround organization of recepti-ve fields would fail with a blurred image.

Transitivity, additivity. and residual responses We show in Figs 2 and 3 that transitivity and additivity are demnonstrable in individual cells of the MC-pathway. A complication for the MC-pathway as a whole is the variability in spectral sensitivity between neurones but if the averaged activity in the MC-pathway goes through a minimum at equal luminance (Fig. 4D), transitivity and additivity result. Extensive tests of additivity with photometric tasks have been performed by Ingling and co-workers (Ingling, Tsou, Gast, Burns, Emerick & Riesenberg, 1978). On increasing retinal illumiinance, deviations from additivitv were observed with flicker photometry, but deviations were minor with MDB. Psychophysically. in flicker photometry more long-wavelength light is needed as retinal illumninance increases. This effect is seen in individual cells of the MCpathway (Lee, 1991). It is not clear why MDB should be less susceptible to these effects. The residual responses of individual MC-pathway cells are linearly related to the tritanopic purity difference across a border. A IAPtI of one evoked on average a response equivalent to that to 140% luminance contrast. This value is close to psychophysical estinates of residual distinctness (VTalberg & Tansley, 1977). The physiological basis of these residual responses is not straightforward. They are present not only with borders, but also with temporal chromatic modulation of a uniform field (Lee et al. 1989a) when they are manifest as a response at twice the stimulus frequency. This frequency-doubled response remains a constant fraction of the response to luminance modulation up to 20 Hz, and thus a significant contribution from ehromatic adaptation is unlikely. Although the amplitude of this response is linearly related to JAPti at equal luminance (Lee et al. 1989a; Fig. 3), a mechanism based on straightforward non-linearity of cone summation (e.g. a threshold effect) is unlikely, because frequency-doubled responses can often be seen to a stimulus modulated so as to stimulate only the M- or L-cone. The residual response in the MC-pathway at eq-ual luminance will arise not only from residual responses in individual cells, but also from the variability in M/L-cone weighting between cells. We have shown the former to be linearly related to tritanopic purity. The same will be true for the latter, for the deviation from 1VA sensitivity due to changes in M/L-cone weighting will also be proportional to tritanopic purity difference. However, inspection of responses and curves such as

598

A. VALBERG A-N7D OTHEhRS

those in Fig. 2 suggested that residual responses provide a larger residual signal at equal luminance than that due to variability in spectral sensitivity. Although the residual response in the NC-pathway is adequate to account for residual distinctness, responses in the PC-pathway may also contribute. However, the responses of M - L-cone opponent PC-pathway cells to equal luminance borders as a function of IAPtl do not bear any such obvious relation to their response to achromatic contrast as seen in the psychophysical results. From curves such as those in Fig. 7, the average response evoked in M - L-cone opponent cells by a border with a IAPtI of 10 was 55 imp s-', for eleven cells for which sufficient data were available. A response of this magnitude could not be evoked from most of these cells by any achromatic border, and for those cells in which this impulse frequency was reached, close to 100 % achromatic contrast was required. Our data thus suggest that the MC-pathway signals border distinctness not only when a luminance contrast is present, but also at equal luminance. It is possible that the residual motion percept at equal luminance could be mediated by this signal, for current psychophysical attempts to rule out this possibility have not yet proved convincing (Cavanagh & Anstis, 1991). The MC-pathway residual signal presumably provides input to those cortical areas responsible for processing of not only motion, but also binocular disparity and other aspects of form perception compr omised but not abolished at equal luminance.

Central mechanisms processing afferent signals It is important when linking physiological and psychophysical data that assumptions as to central processing of the afferent physiological signal should be realistic. This involves devising possible cortical mechanisms which then can be tested with actual data. We show in Fig. 9 that an odd-symmetric cortical receptive field would possess the necessary properties for supporting the MDB task. Such receptive fields are well established in the literature (Movshon et al. 1978), and are equivalent to zero-crossing detectors. The output of such detectors constructed from an on- and an off-centre phasic cell goes through a minimum at equal luminance, in terms of a peak firing measure (Fig. 9). Other models could be easily constructed however; any mechanism in which the signals of on- and off-centre neurones are compared would perform in a similar way. Most of these models assume that the distinctness of a border is somehow related to peak firing rate in the cellular signal. This seems a reasonable assumption, but difficult to verify. An alternative hypothesis is the generation of a luminance signal from PCpathway activity (e.g. Ingling & Martinez-UJriegas, 1983; Ingling & MartinezUriegas, 1985; Ingling, 1991). The luminance signal is assumed to be multiplexed with these cells' chromatic response. The type of luminance signal required might be generated from PC-pathway cell signals in the manner suggested in Fig. 8B. An examination of actual cell responses did not support this model. Although some such effects as predicted may be seen when very high luminance differences were present across a border, a signal suitable for the MDB task was not readily discernible. It could be argued, of course, that the cells chosen for Fig. 10 were an inappropriate combination, but other pairs of neurones yielded no better results. Also, it might be argued that more extensive convergence on a central mechanism might occur. It is,

MACAQUE GANGLION CELL BORDER RESPONSES

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however, difficult to see how after such convergence a useful signal for border distinctness might be extracted. Thus, although the model in Fig. 8B for construction of a luminance mechanism from PC-pathway cells is a priori plausible, it appears difficult to implement when tested with real cell responses. Its failure may have several reasons. Firstly, recent evidence suggests that a high proportion of tonic, M - L-cone opponent ganglion cells have a receptive field structure in which the difference in spatial extent of centre and surround mechanisms is quite small (Shapley, Reid & Kaplan, 1991). Secondly, such a model as that in Fig. 8B requires the component cell inputs to be very precisely matched. This is because the model depends on the chromatic components in the added signal exactly cancelling to allow a luminance signal to be extracted. This cancellation requires the component inputs to be exactly matched in location, and in weighting and extent of centre and surround mechanisms of their receptive fields. Also, the intensity-response functions of each input must be identical. It seems implausible that the model of Fig. 8B could meet these requirements. Although PCpathway cells combine cone signals in a linear manner, rectifying non-linearities in their responses are present in that firing rates cannot be negative and saturating nonlinearities are visible at high chromatic contrasts. Lastly, VA sensitivity requires a L/M-cone weighting of 1'6: 1, whereas the average cone weighting for PC-pathway cells is much closer to 1:1. Thus, although the model of Fig. 8B is plausible, it would seem to involve several concealed assumptions which are not justified on examination of actual cell behaviour. We would stress that it is nevertheless plausible to generate from PC-pathway activity a lightness or brightness signal for ordering spectral mixtures in colour space (Valberg, Seim, Lee & Tryti, 1986; Valberg et al. 1987). Psychophysical spectral sensitivity derived from, for example, heterochromatic brightness matching differs from VA sensitivity, much in the way a combination of PC-pathway cell responses might predict. We would also stress that the models of Fig. 8 have been arbitrarily selected; other kinds of model are possible for both MC- and PC-pathway cells. However, all PCpathway models are likely to suffer from the difficulties discussed in the preceding paragraph. Models involving non-linearities might also be considered, for example, some kind of combination of rectified signals from PC-pathway cells. It is difficult, however, to make such models have the required photometric properties. Another issue raised by this analysis is the role of eye movements in performance on MDB. In the lack of available data for this specific task, fixational eye movements can only be assumed to have the usual pattern, with slow drifts and correctional microsaccades, although the latter are reduced in frequency when an object is carefully inspected (see Hallet, 1986 for review). Both might be expected to give rise to a neural signal. Although the stimulus conditions tested here involved moving the border at much higher velocities over parafoveal receptive fields than are present in the drift movements during foveal fixation, after normalization to parafoveal receptive field centre size the discrepancy is small. On the other hand, correctional saccades have a much higher velocity than movement employed here. It would be of some interest to measure psychophysical performance on MIB using controlled movements after image stabilization, but such data are not available. 20

PHY 458 20PY05

600

A. V.ALBERG AXVI) OTHERS

On-i defocusing the retinal image, a model such as that in Fig. SB can no longer be applicable, since the defocused border cannot differentially activate centre and surround. Psychophysically. the MDB task is little affected by blurring the edge (Lindsey & Teller. 1989). This difficulty was recognized by Ingling (1991), who proposed that with retinal blur MC-pathway cells support the task, but with a sharp border a miechanismn such as that in Fig. 8B becomes operative. In view of the other arguments presented here, this duality of meehanisms for MDB is unnecessary. MCpathway cells can support the task both with sha,rp and blurred borders (Fig. 11). For PC-pathwav cells, retinal blur little affects the sustainied component of the response. This mav be related to the fact that defocus little affects psychophysical sensitivity to chromatic contrast with large fields. Sensitivity to achromatic contrast is much mor-e depressed (Valberg, Seim & Lee, 1 99 t), as are responses of MC-pathway cells. In summary, we have presented several lines of evidence favouring the MCpathway as the major physiological substrate of performiance on MDB. This implies that responses in the PC-pathway play little part in determining border distinctness. This physiological evidence supports previous speculation as to the role of the MCpathway in pattern vision (Livingstone & Hubel, 1987). Also. the results presented suggest that extraction of a lumninance signal for utilization in the MDB task from the PC-pathway is inore difficult than has been supposed. This seems inconsistent with experiments in which monikeys were tested for behavioural deficit after lesions in the parvo- or magnocellular layers of the lateral geniculate nucleus (Schiller et al. 1990), where performn-ance on certain spatial tasks impaired with equal luminance patterns was reported to be unaffected by magnocellular lesions. The resolution of this contradiction remains unclear, but perhaps lesions in different laminae of the geniculate nucleus bring about more complex effects than a straightforward inactivation of one cell svstem. The results presented imply that the mechanism with VA sensitivity responsible for spatial vision in the MDB task has as a physiological substrate the MC-pathway. However. one cannot, extrapolate from these results to the physiological basis of a mechanism responisible for fine spatial vision under other circumstances, for example with achromatic patterns. It is presently difficult to assess the relative roles of the MC- and PC-pathways in such a mechanism. Although some evidence, from consideration of the sampling density in these pathways and from lesion experiments (Schiller et al. 1990). suggyest a predomninant role for the PC-pathway, analysis of the signal-to-noise ratio of MC- and PC-pathway signals in different achromatic hyperacuity tasks suggests a predominant role for the MC-pathway (Lee. Wehrhahn, Kremers & Westheimer, 1991). The numerical superiority of the PC-pathway is unable to make up for its poor signal-to-noise ratio in such tasks, which require the highest, degree of spatial precision. We thank Paul Martin for assistance with some of the earlier experiments and for comments on the manuscript. P. K. K. was supported by the Natural Science and Engineering Research Council of Canada and the York Faculty of' Arts. A.1V. was in receipt of a grant from the Norwegian Research Council for Science and the Humanities and the University of Oslo.

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REFERENCES

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VALBERG, A., LEE, B. B. & KAISER, P. K. (1990). The residual response in macaque ganglion cells is related to tritanopic purity difference across equal luminance borders. Investigative Ophthalmology and Visual Science 31, 265. VALBERG, A., LEE, B. B. & TRYTI, J. (1987). Simulation of responses of spectrally opponent neurones in the macaque lateral geniculate nucleus to chromatic and achromatic light stimuli. Vision Research 27, 867-882. VALBERG, A., SEIM, T. & LEE, B. B. (1991). Different effects of retinal blur on achromatic and chromatic contrast sensitivity. Optical Society Technical Digest Series 17, 41-42. VALBERG, A., SEIM, T., LEE, B. B. & TRYTI, J. (1986). Reconstruction of equidistant color space from responses of visual neurons of macaque. Journal of the Optical Society of America A 3, 1726-1734. VALBERG, A. & TANSLEY, B. W. (1977). Tritanopic purity-difference function to describe the properties of minimally distinct borders. Journal of the Optical Society of America 67, 1330-1335.