development of tools such as capsazepine as probes for the physiological function of the receptor; this in turn raises the question as to what the endogenous ligands for the site are. The anatomical tracing of the terminals of unmyelinated C-fibres innervating tissues throughout the body should be considerably aided by the description of the capsaicin gap tech-

nique. The importance of capsaicin as a research tool and as a model for the development of novel therapeutic agents will no doubt continue.

Selected references 1 Fitzgerald, M. (1983) Pain 15,109-130 2 Lynn, B. (1990) Pa/n 41, 61-69 3 8evan, S. eta/. (1991) Br. J. Pharmaco/. (in press)

Colorand the integrationof motionsignals Thomas D.

Albright Salk Institute for Biological Studtes, La Jolla, San Diego, CA 92138, USA.

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everal lines of evidence indicate that there are at least two stages of motion processing in the primate visual cortex. The first stage involves 'local' measurements of image motion. Motiondetecting neurons at this stage are characterized by marked orientation selectivity and a limited spatial field. Orientation selectivity restricts the contribution of individual detectors to one-dimensional motion signals, i.e. motion is detected only along the axis perpendicular to the preferred orientation. All motion-sensitive neurons in primary visual cortex (area V1) and a substantial fraction of cells in the middle temporal visual area (area MT) of the macaque have properties characteristic of this first stage of motion processing 1. At the second stage these local motion signals are integrated to construct a representation of the 'global' two-dimensional velocity field - a representation consistent with the integrity of our perceptual experience of motion. This second stage is embodied by a small subset (about 25%) of MT neuronsl'2. The nature of this motion signal integration process has been the subject of intense research in the past decade and a fairly coherent story has begun to emerge. Much of the story centers on the use of 'plaid' stimuli (Fig. 1) developed by Adelson and Movshon 3, which afford a conceptually straightforward means to probe the integration process both physiologically and psychophysically. These stimuli are produced by the superimposition of two drifting gratings. Individually the gratings stimulate detectors at the first stage of motion processing. These early signals are then integrated by the

S

second stage to yield the percept of a coherently moving plaid pattern. In the real world it is commonly the case that multiple motion signals arise from approximately the same region of the visual field. Sometimes these signals are produced by different parts of a single moving object. In other instances they may arise from different objects drifting past one another. Successful motion processing is, of course, critically dependent upon integrating only those signals common to each object. By using moving plaid patterns as visual stimuli, a central objective has been to explore the 'rules' that govern motion signal integration. Typically, similarity of the two component gratings is manipulated along some dimension and subjects are asked to indicate whether their dominant percept is that of a coherently moving plaid pattern or of two gratings sliding past one another. In seminal experiments Adelson and Movshon 3 showed that the coherent motion percept was less likely if the two gratings differed sufficiently in either spatial frequency or contrast. More recently it has been found that coherence is markedly reduced if the gratings are in different stereoscopic depth planes 4 or if one grating is perceived to be transparent and overlying the other 5. These results seem to suggest that any of a variety of cues for image segmentation have the capacity to 'gate' the motion integration process. To put it another way, it seems that motion signals that are likely to have originated from the same object - j u d g i n g from image segmentation cues are most likely to be integrated. New results addressing the

© 1991, ElsevierSciencePubhshersLtd, (UK) 0166- 2236191/$0200

4 Jancs6, G. and Lawson, S. N. (1990) Neuroscience 39, 501-511 5 Jancs6, G., Kiraly, E. and Jancs6-G,~,bor, A. (1977) Nature 270, 741-743 6 0 t t e n , U., Lorez, H. P. and Businger, F. (1983) Nature 301,515-517 7 Johnson, E. M., Rich, K. M. and Yip, H. K. (1986) Trends Neurosci. 9, 33-37 8 Besse, D., Lombard, M. C. and Besson, J-M. (1990) Pain (Suppl.) 5, $122 9 Dickenson, A., Ashwood, N., Sullivan, A. F., James, I. and Dray. A. (1990) Eur. J. Pharmacol. 187. 225-233

rules and mechanisms underlying motion signal integration have been obtained from an elegant and strikingly simple psychophysical experiment reported by Krauskopf and Farell in a recent issue of Nature 6. Their findings are of particular interest as they also bear on the contribution of color to motion processing - a subject that has of late given rise to considerable debate. Before describing the result it is worthwhile briefly reviewing some salient features of the way color is encoded at early stages in the primate visual system. The primate retina contains three types of cone photoreceptors, which are maximally sensitive to long (L), middle (M) or short (S) wavelengths of light. Signals arising from L, M, and S cones are combined at subsequent stages to render three channels that define a 'color space' with three principal axes (Fig. 2) 7-9. Activity in the first of these post-receptoral channels is proportional to the difference between the activation of L and M cones (Fig. 3). This channel is one of two purely chromatic channels and it encodes, roughly speaking, the relative intensities of long and mid-spectral light, but is insensitive to absolute levels of illuminatio1:. Activity in the second channel is proportional to the difference between the activation of S cones and the combined activation of L and M cones, i.e. S - ( L + M ) . This second channel is also purely chromatic since it encodes, roughly speaking, the relative intensities of short and non-short (i.e. long and mid-spectral) wavelengths of light. Activity in the third channel is proportional to the summed activity of L and M cones. This channel thus encodes overall luminance within the broad range of spectral frequencies that excite L and M cones. However, this TINS, 9'oi. 14, No. 7, 1991

luminance channel lacks color selectivity as there are many colors of light for which the combined activity of L and M cones does not vary. These are termed 'isoluminant' colors. Psychophysical experiments on humans have shown that sensitivity to contrast modulation within any one of the three post-receptoral channels is reduced by prior activity modulation within the s a m e channel only8. This channel-specific desensitization is of some significance as it implies linear independence: by appropriate changes of illumination it is possible to modulate activity within any single channel while not affecting either of the others. As a consequence, perceivable colors can be uniquely defined by their relative activation of the three channels. They can thus be described by single points in a three-dimensional color space (Fig. 2) in which the three channels form the principal or 'cardinal' axes. Conveniently, the azimuth and elevation of any point measured relative to the origin of this space identify the familiar attributes of hue and brightness. Radius from the origin provides a measure of saturation or purity of color. Neurophysiological evidence for the cardinal nature of the two purely chromatic channels includes the fact that the chromatic sensitivities of neurons in the primate lateral geniculate nucleus are limited to two distinct types 7. 'Red-green' opponent neurons receive inputs of opposing sign from L and M cones and their activity is

*The color names used to identify these color-opponent channels are historically entrenched, but imprecise. Over 100.years ago Edwald Hering1° proposed a theory of color vision based upon three independent mechanisms - two chromaticallyopponent channels and one acttromatic luminance sensor - that are similar to the three channels now knownto exist. Heringpostulated that the axes of the two chromatic channels were aligned with the colors we perceive as 'unique' (i.e. non-reducible, perceptually, to a combination of hues): red, green, blue and yellow. It now appears, however, that while the poles of the L-M channelare not far fromuniquecolors (red and green), the poles of the S-(L+M) channelare. Ratherthan appearinguniquely blue and yellow, they are closer to violet and chartreuse. The color names used throughout the remainder of this text are meant to conveyto the reader the approximate colorappearanceof visualpatterns and are not intended to implyunique colors.

TINS, Vol. 14, No. 7, 1991

A

B

t

kk '- tt/t i

I.

I COMPONENTS

I

I I

PATTERN

Fig. 1. Moving 'plaid patterns' developed by Adelson and Movshon ~ are produced by the superimposition of two drifting sine wave gratings. Motions of the component gratings (A) are encoded at the first cortical motion processing stage 1. These motion signals are integrated by the second motion processing 1'2 stage such that perceived direction and speed of the resultant plaid pattern (B) differs from that of either grating alone, This integration process has been shown previously to be 'gated' by reliable image segmentation cues such as spatial frequency3, contrast3, depth 4 and perceptual transparency5.

modulated in proportion to the difference between L and M cone excitations. In a similar fashion, 'blue-yellow'* opponent neurons receive contrasting inputs from S and (L+M) cones and their activity parallels the S - ( L + M ) cone difference. In the laboratory, activity within the L - M channel can be modulated selectively [i.e. without concurrent modulation of either S - ( L + M ) or L + M channels] by visual patterns composed of redgreen chromatic contrast, such as alternating red and green stripes in a sine wave grating. Likewise, activity within the S - ( L + M) channel can be modulated selectively by patterns composed of violetchartreuse chromatic contrast. Finally, activity within the L + M (luminance) channel can be modulated selectively by black-white patterns that do not vary in their spectral content. Krauskopf and Farell hypothesized, quite simply, that motion signals arising from the same channel would be more likely to yield a coherent motion percept than those arising from different channels (Fig. 3, top) 6. As a first test of this hypothesis, plaid patterns were constructed from pairs of sine wave gratings modulated along either the same or along different axes in color space. As expected, plaids composed of two identical isoluminant gratings designed to stimulate only the L - M channel (e.g. red-green) were

found far more likely to cohere than were plaids composed of gratings designed to stimulate the L - M and S - ( L + M ) channels independently (e.g. red-green and violet-chartreuse). Similar results were obtained from all of the other possible combinations of same and different channel activations. Chromatic stimuli that do not fall along one of the three cardinal axes in color space will elicit activity from more than one channel. For example, a pattern of isoluminant orange-turquoise stripes falls along a 45-225 ° diagonal in color space (Fig. 2) and thus activates both the L - M and S - ( L + M ) channels to a similar degree. A pattern of isoluminant limemagenta stripes falls along an opposing (135-315 °) diagonal in color space (Fig. 2) and also activates both L - M and S - ( L + M ) channels although, of course, it looks quite different from the orangeturquoise pattern. A second straightforward prediction tested by Krauskopf and Farell is that motion signals will cohere if they arise from patterns that activate the same channel(s), regardless of how different they appear. Indeed, plaid patterns formed by combining gratings modulated along any pair of diagonals in color space (e.g. orange-turquoise and lime-magenta) were seen to cohere nearly all the time. Thus it seems that motion signals arising from visual stimuli that are processed through separate 267

LUMINANCE (L+M) AXIS S-(L+M) AXIS

~ant

L-M AXIS

Fig. 2. Three-dimensional color space defined by three orthogonal ('cardinal') channels in the primate visual system. Two color-opponent channels [ L - M axis and S-(L +A4) axis] and one broad-band luminance channel (L + M axis) are formed by algebraic sums of excitation among cone photoreceptors sensitive to long (L), middle (Iv1) or short (S) wavelengths of light (see Fig. 3). Colors are uniquely represented by relative activation of these three channels. Hue is proportional to azimuth (such that 45 ° is roughly orange, for example) and apparent brightness is proportional to elevation. Color saturation along any axis within an isoluminant plane (e.g. the ratio of red to green light in a mixture of constant luminance) is proportional to deviation from the center of the plane. The colored sectors shown in this figure are only a rough approximation to actual hue, brightness and saturation.

chromatic and luminance channels are not likely to be integrated by the second cortical stage of motion processing. In contrast, moving stimuli giving rise to activity within the same channel(s) are very likely to be integrated. These results are important for several reasons. First and foremost, they add to mounting evidence that visual stimulus attributes unrelated to motion per se can profoundly affect the way we see things move. Stimulus 'similarity' as assessed by patterns of modulation in color space directly influences the integration of local motion signals. Not 0nly do these results tell us much about the stimulus attributes that 'gate' the integration process but they imply a simple channel-based mechanism for doing so and they reinforce the significance of the three cardinal axes in color space. 268

These results are also significant in the light of recent controversy regarding the parallel processing of color and motion. Considerable neuroanatomical, neurophysiological and psychophysical evidence has led to the belief that there are limited avenues for interaction between color and motion processing pathways in the primate cerebral cortex (see Refs 11 and 12 for reviews). Although few would dispute the rarity of traditional color selectivity among motion selective neurons, there are increasing indications that the chromatic properties of visual stimuli have important effects on the detection of motion. Observations such as those presented by Krauskopf and Farell betray the existence of significant crosstalk between color and motion pathways. Revealing though they might be,

there are also a number of puzzling issues raised by these new results, one of the most nagging of which concerns their functional significance. As mentioned earlier, many of the stimulus attributes known to affect motion signal integration (e.g. contrast, depth, transparency) are reliable indicators of object boundaries, and their influence over integration has clear functional significance for visual perception. The case is far less clear for gating by chromatic channels. It is easy to imagine how image segmentation might occur from chromatic stimuli that cause activation of common channels (such as turquoise and magenta) and yet motion signals arising from such stimuli readily cohere. One intriguing idea is suggested by the fact that under normal daylight conditions chromatic variation within the visible spectrum is dominated by modulation along the S - ( L + M ) axis 13. It could thus be the case that image segmentation has evolved to be optimal (and coherence poorest) when objects differ maximally from this dominant background by modulation along the non-dominant (L-M) axis. However, the possibility exists that the reported effects of color on motion coherence are merely an epiphenomenon resulting from channel-based processing of color and are of no 'value' in any functional sense. A second question arises upon consideration of the possible routes by which color input reaches the motion integration stage, which is presumed to be in area MT. Current thinking dictates that the local motion signals characteristic of the first cortical stage of motion processing are encoded by directionally selective V1 neurons, which provide a massive input to area MT. The findings reported by Krauskopf and Farell indicate that motion signals at this first cortical stage are carried within three independent channels. However, a recent report TM claims that the chromatic and luminance sensitivities of V1 neurons do not fall strictly along the cardinal axes in color space as would be expected from the results of Krauskopf and Farell. Furthermore, a recent psychophysical experiment 15 has revealed marked adaptation-induced changes in color appearance that cannot be explained by TINS, Vol. 14, No. 7, 1991

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simple desensitization of one or more of the three post-receptoral channels. This result indicates that, at some level of color processing, either (1) the favored axes number greater than three a possibility that might also explain the aforementioned chromatic sensitivities of V1 neurons - or (2) the cardinal axes are more mutable than previously suspected. Specifically, the orientations of these axes might adaptively realign, altering color sensitivity in a fashion that is dependent upon chromatic properties of the ambient light. An exciting possibility is that optimal conditions for motion coherence might, in turn, be influenced by adaptive restructuring of color space. Thus, although we now have a better understanding of the phenomenon of chromatic effects on motion processing, precisely how and why color influences motion coherence in the way that it does remains something of a mystery. Selected references 1 hAovshon, J. A., Adelson, E. H., Gizzi, hA. and Newsome, W. T. (1985) in

Study Group on Pattern Recognition Mechanisms (Chagas, C., Gattass, R. 2 3 4 5 6 7 8 9 Fig. 3. Schematic illustration of color and luminance channels in the primate

visual system and their contributions to motion signal integration. Light within the visible spectrum is detected in the retina by three types of cone photoreceptors (bottom). These cones are maximally sensitive to long (L), middle (M) or short (S) wavelenooths of light. Cone signals are combined at a subsequent stage (center) to render two types of color-opponent channels. One chromatic channel encodes the relative intensities of long and midspectral light (L-M). The second chromatic channel encodes the relative intensities of short and non-short (i.e. long and mid-spectral) wavelengths of light [S-(L +M)]. There is also a third channel sensitive to broad-spectrum luminance (L + M). The two purely chromatic channels are represented by the signals from two types of color-opponent neurons in the parvocellular laminae of the lateral geniculate nucleus< The color gradients shown at the center are approximately those that have been shown to modulate selectively the activity of each of the channels. Krauskopf and Farell6 now report that moving colored gratings that activate common channels (e.g. red-green + red-green; top left, small arrows) readily cohere (bold arrow). In contrast, gratings that cause no common channel activation (e.g, red-green + violet-chartreuse; top right, small arrows) are perceived to slide across one another (bold arrows). TINS, Vol. 14, No. 7, 1991

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and Gross, C. G., eds), Pontifica Academia Scientiarium Rodman, H. R. and Albright, T. D. (1989) Exp. Brain Res. 75, 53-64 Aclelson, E. H. and hAovshon, J. A. (1982) Nature 300, 523-525 Adelson, E. H. and hAovshon, J. A. (1984) J. Opt. Soc. Am. 1, 1266 Stoner, G. R., Albright, T. D. and Ramachandran, V. S. (1990) Nature 344, 153-155 Krauskopf, J. and Farell, B. (1990) Nature 348, 328-331 Derrington, A. M., Krauskopf, J. and Lennie, P. (1984)J. Physiol. 357, 241-265 Krauskopf, J., Williams, D. R. and Heeley, D. W. (1982) Vision Res. 22, 1123-1131 hAacLeod, D. I. A. and Boynton, R. hA. (1978) J. Opt. Soc. Am. 69, 1'183-1186 Hering, E. (1878) Zur Lehre vom

Lichtsinne (Principles of a New Theory of the Color Sense), translated by K. Butler and partially reprinted in:

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Teevan, R. C. and Birney, R. C., eds (1961) Color Vision, Selected Readings, Van Nostrand Reinhold Livingstone, hA. S. and Hubel, D. H. (1988) Science 240, 740-749 Van Essen, D. C. (1985) in Cerebral Cortex (Vol. 3) (Peters, A. and Jones, E. G., eds), pp. 259--327, Plenum Judcl, D. B., hAacAdam, D. L. and Wyszecki, G. (1964) J. Opt. Soc. Am. 54, 1031-1040 Lennie, P., Krauskopf, J. and Sclar, G. (1990) J. Neurosci. 10, 649-669 Webster, hA. A. and hAollon, J. D. (1991) Nature 349, 235-238

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