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Progress in Retinal and Eye Research 26 (2007) 636–
The ON–OFF dichotomy in visual processing:
From receptors to perception
Gerald Westheimer
Division of Neurobiology, University of California, Berkeley, CA 94720-3200, USA
Abstract
Vision scientists long ago pointed to black and white as separate sensations and saw confirmation in the fact that in the absence of light, one perceives the visual field as gray against which the negative after-image of a bright light appeared blacker. The first recordings from optic nerve fibers in vertebrates revealed ON and OFF signals, later associated with separate streams, arising already at the synapse between receptors and bipolar cells. These can be identified anatomically and physiologically and remain distinct all the way to the lateral geniculate nucleus, whose fibers form the input to the primary visual cortex. The dichotomy has been probed by electroretinography and analyzed by means of pharmacological agents and dysfunction due to genetic causes. The bi- rather than a unidirectional nature of the retinal output has advantages in allowing small signals to remain prominent over a greater dynamic range. The two streams innervate cortical neurons in a push–pull manner, generating receptive fields with spatial sensitivity profiles featuring ON and OFF subregions. Manifestations of the dichotomy appear in a variety of simple visual discriminations where there are often profound threshold differences in patterns with same polarity as compared with mixed contrast-polarity components. But even at levels in which the spatial, contrast and color attributes have already been securely established and black and white elements participate equally, a categorical difference between blackness and whiteness of a percept persists. It is an opponency, akin to the ones in the color domain, derived from the original ON and OFF signals and subsequently bound with the other attributes to yield a feature’s unitary percept. r 2007 Elsevier Ltd. All rights reserved.
Keywords: Retina; Visual cortex; Contrast polarity; Center–surround antagonism; Black/white opponency; Visual discrimination thresholds; Perceptual grouping
Contents
- Introduction............................................................................... 637
- Retina................................................................................... 637 2.1. Source of ON/OFF divide—internal retinal circuitry.............................................. 637 2.2. Antagonistic pairing in the domain of brightness................................................. 638 2.3. Spatial antagonism...................................................................... 638 2.4. Abnormalities of genetic origin............................................................. 638 2.5. Other pathways........................................................................ 639
- Primary visual cortex......................................................................... 640 3.1. Input to the cortex...................................................................... 640 3.2. Receptive fields......................................................................... 640
- ON/OFF dichotomy in visual perception........................................................... 641 4.1. Criterion I............................................................................ 641 4.2. Criterion II............................................................................ 641 4.3. Criterion III........................................................................... 643
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proper, has been the first venue for detailed analyzes of neural circuitry and so it was in connection with the ON–OFF dichotomy originally discovered in optic nerve fibers. The photochemical and cellular light transduction stages in the retina in vertebrate photoreceptors, the rods and cones, were shown to fit in with the physicalist view of light exchange of electromagnetic energy—photon absorp- tion is absent in complete darkness and increases with increasing light levels. That is to say, photon capture and the entrained photoreceptor activation increase from none in darkness to the maximum in the brightest light. Curiously, however, vertebrate photoreceptors respond by increasing hyperpolarization with increasing light capture, in contradistinction to the typical sense cell where the stimulus acts to depolarize the cell membrane. Because the release of transmitter substance increases with cell depolarization, photoreceptor cells have the strange property of releasing less transmitter substance the more light activation they experience. Regardless of this detail, the conclusion is that activity within and communication from the primary light sensory cell undergo a gradual change in a single direction as the range from dark to bright is traversed. There are no separate ON and OFF photoreceptors; all photoreceptors release glutamate, and in decreasing doses as their light activation increases. The dichotomy under consideration here appears at the very next stage of processing. The photoreceptor signals represented by the release of the glutamate neurotransmitter (in decreasing quantity with increasing light level) are directed principally to the next tier of cells, the bipolar cells which exist in two flavors: ‘‘about half of the units hyperpolarize to central illumination, while the other half depolarize’’ (Werblin and Dowling, 1969). Those showing an increase in excitation with increase in glutamate concentration, i.e., that are activated by a decrease in light, are called OFF bipolar cells, and are now known to express the ionotropic glutamate receptor molecules at their synaptic ending, which respond to glutamate by opening cation channels, thus depolarizing the cell. On the other hand, those with a response in the opposite direction, i.e., increasingly activated by decreases in glutamate release consequent to onset of light, are called ON bipolars. The receptor molecule on their surface at the synapse with the rods or cones is the mGluR6 metabotropic receptor (Duvoisin et al., 2005) which is coupled to a pathway causing cation channels to close and thus, through this inhibitory influence, producing an inverted signal. Although retinal circuitry is quite complicated, the basic organizational principle, entrained by this bifurcation of the originally unipolar stream onto reciprocally activated ON and OFF paths, is maintained and conveyed out of the retina by the final output, viz., the ganglion cell axons which become the optic nerve fibers.
2.2. Antagonistic pairing in the domain of brightness
When the retina is exposed to a uniform field, ganglion cells discharge impulses at a rate of a score or so per second
but they fall into two classes as regards their light response. Those fed by ON bipolar cells and manifesting a burst of additional impulses for a brightening light pulse are the ON ganglion cells and are responsible for the ON burst discovered in the frog by Hartline in the 1930s. The members of the other class respond with a burst when a small spot is suddenly dimmed and are called OFF ganglion cells. Ignoring the complications associated with the temporal transients for which there is yet another overlaid internal retinal circuitry, and of the non-statio- narity due to prominent adaptational effects, changes in light level are signaled by two reciprocally activated paths, one for increases and the other for decreases in light. In each case, this is superimposed on a steady low-level ‘‘spontaneous’’ firing in the absence of specific stimuli, which can thus experience increases on delivery of the relevant stimulus (light for an ON cell or darkening for an OFF cell), as well as inhibition on delivery of the opposite stimulus (e.g., darkening for an ON cell, light for an OFF cell); see Fig. 1.
2.3. Spatial antagonism
Each of the two classes of ganglion cell also exhibits a spatial antagonism, in that a ganglion cell, whether ON or OFF, has its activation reduced when its relevant stimulus is extended from the center of its receptive field into a concentric spatially surrounding zone. Thus, an ON ganglion cell will fire briskly when the center of its receptive field is brightened but less so when the stimula- tion also extends into its surround. This spatial antagonism has the important property of dropping out in dim illumination (Barlow et al., 1957). According to the current teaching of physiology, all the properties of an ON-center retinal ganglion cells in photopic vision are generated, at least in the mammal, entirely through intraretinal circuitry involving bipolar cells of only the ON variety, and the equivalent statements holds for OFF ganglion and bipolars cells (Fig. 2). The strong support for this view comes from experiments with the pseudo-neurotransmittor, APB (Schiller, 1992), which competitively binds to and hence inactivates the synapse between receptor and ON bipolar cells while leaving the OFF stream unaffected.
2.4. Abnormalities of genetic origin
Relevant also are two abnormalities now identified as having a genetic origin, the congenital stationary night- blindnesses types 1 and 2 (CSNB1 and CSNB2). In the first there is a mutation of a gene, NYX, whose protein product nyctalopin is involved in the pathway through which glutamate acting on the mGluR6 metabotropic receptor at the ON bipolar cell synapse controls Ca 2+^ channels (Morgans et al., 2006). Because in the first instance the rods communicate only through ON bipolar cells (Waessle, 2004), affected patients have no rod vision, but because the
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cone ON bipolar cells also do not function, there are deficits in photopic vision as well. Electroretinography has revealed a similarity between the effect of APB, which is a
competitive inhibitor of glutamate at these mGlu5R receptors, and the CSNB1 syndrome (Khan et al., 2005). In CSBN2, a different protein is malfunctioning, the CANA1F Ca2+^ channel (Morgans, 2001) which seems to be involved in glutamate release at the rod/rod-bipolar synapse. Some patients with this condition have fully functional cone vision (Allen et al., 2003) but it is possible that cone pathways may not always be spared (Bech-Hansen et al., 1998; Strom et al., 1998). The situation is complicated by the existence of several subtypes of both ON and OFF bipolar cells.
2.5. Other pathways
One cannot leave a survey of retinal processing, however brief and schematic, without mention of its immense intricacy and subtlety that have been ignored here. The overlaid temporal properties—transient vs. sustained fir- ing, adaptation—have already been referred to. In some species, there is even movement selectivity. The structural and functional divisions subserving color discrimination fill many additional chapters (Masland, 2001; Waessle, 2004). So does the magnocellular/parvocellular dissociation. Finally, there is one recent development that is pertinent to this study: the existence, even in the mammal, of a separate pathway utilizing a small number of simple light- level detectors in the retina containing the photopigment melanopsin. The output is purveyed directly to non-cortical structures in the central nervous system, and has been implicated in pupil responses and in the setting of diurnal rhythms and the photoentrainment to the day/ night, light/dark cycle (Berson, 2003; Freedman et al., 1999; Van Gelder, 2003).
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ON Unit
OFF Unit
White
Black
Light Stimulus
Fig. 1. Schematic illustration of ON and OFF retinal ganglion cell discharges when white and dark stimuli are delivered to the centers of their receptive fields (redrawn from Schiller, 1992). Bursts occur in ON cells for white and in OFF cells for black, and there is brief cessation of firing in the reverse situation. Surround stimulation yields an inverse pattern, but the center/surround antagonism is engendered by excitatory and inhibitory interaction separately within each stream and not by superposition of ON and OFF signals.
Fig. 2. Schema of channeling of ON and OFF signals in retina from receptors via bipolar cells, creating center/surround structure of ganglion cell receptive fields separately for the ON (open symbols and light lines) and OFF (closed symbols and heavy lines) systems. Adjacent region cause surround antagonism by inhibitory interaction, but in each case this takes place within its stream. The more complex interconnection within the retina involving horizontal and amacrine cells has been ignored in this sketch.
G. Westheimer / Progress in Retinal and Eye Research 26 (2007) 636–648 639
Though a great deal can be known about the kinds of optimal object light patterns that will activate cells in the primary visual cortex of even an alert, behaving primate, what remains vague is the nature of the contribution of that neuron’s firing to the final percept. If a particular cell’s receptive field is optimally covered by, say, a bright bar of given location, orientation, width and length, would a firing burst of that cell lead to the perception of such a bar, or perhaps, with a more modest expectation, provide a substantial contribution within an ensemble of kindred cells to the emergence of such a percept? Experiments in which minimal localized stimulation was applied to a cortex have so far been inconclusive and contradictory. Nor have modern non-invasive techniques of visualizing cortical activity as yet achieved the needed resolution to help with an answer. In such a situation, it is best to concentrate analysis on the other end of the arc that leads from object presentation to a subject’s experience, namely on carefully conducted psychophysical experiments designed, in this particular instance, to elucidate the role of the blackness and whiteness attribute of pattern components and their interaction in the performance of relevant visual tasks. This is not only appropriate if the overall research program is the understanding of the full perceptual process, but it is also a powerful aid in mapping the channeling of visual streams within the neural pathways.
- ON/OFF dichotomy in visual perception
Evidence for the separation into ON and OFF compo- nents in the afferent stream in visual function and perception can be examined according to several criteria.
4.1. Criterion I
Performance asymmetries between stimulus brightening and darkening, due to differences in processing of the two pathways during their initial stretch of segregation between the outer retina and the visual cortex: The elimination of ON signals at the retina by APB produces some impair- ment of contrast detection and resolution in the primate, and this is consonant with reduced, but not absent, input to cortical neurons whose full response capabilities depend on both streams. Data in more sophisticated visual tasks is lacking so far. The congenital night blindness syndrome, whose putative cause is genetic impairment of signals to the ON bipolar cells, has yielded contradictory results when it comes to visual performance, though its effect in abolishing signals from rods seems firm. The seemingly clear segregation of processing within the retinal ON and OFF streams in the center/surround antagonism would preclude major interaction effects between them, for example where activity in one might impede or potentiate that in the other. However, the two may not operate in exactly the same way. For example, it has been documented that thresholds for light increments are consistently different from those for light decrements (Chichilnisky and Wandell, 1996; Walraven, 1977). This asymmetry has been ascribed to a difference in the rules for adaptation in the ON and OFF pathways, a consequence of the fact that at any adaptation level the range of possible increments is always bigger than the range of decrements.
4.2. Criterion II
Performance difference, assignable to confluence of ON and OFF pathways in primary visual cortex: There is abundant evidence of the influence of differences in contrast-polarity of patterns, or pattern components, in a variety of visual tasks. In several of these tasks, further- more, the interaction, or lack of it, between bright and dark stimulus elements is distance dependent and hence most easily explained by the specific patterning of ON and OFF subregions in the receptive field of neurons in the primary visual cortex (Fig. 5). Vernier discrimination suffers if one of the abutting lines is white and the other black (O’Shea and Mitchell, 1990), as well as when the alignment task involves black/white edges with oppositely directed gradients (Levi and Waugh, 1996; Westheimer, 2007). The same applies for separation discrim- ination (Levi and Waugh, 1996; Levi and Westheimer, 1987) where the deficit decreases with separation, being essentially abolished for a 10 arcmin separation at the fovea (Fig. 6). In a two-dot alignment task when one dot is white and the other
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Fig. 4. Convergence of ON and OFF streams onto V1 neurons. The receptive field of this neuron has two subregions. The lighter is an ON zone, receiving excitatory contributions from the ON incoming stream (shown as a white +) and inhibitory contributions from the OFF stream (shown as a black ). The reverse applies to the flanking OFF subregion, shown in a darker shade.
G. Westheimer / Progress in Retinal and Eye Research 26 (2007) 636–648 641
black on a gray background, the opposite-polarity deficit exhibits a similar fall-off with separation (Levi and Waugh, 1996). Three-line bisection behaves in the same fashion (Westheimer et al., 2001). The discrimination of the orientation of a line is seriously impaired when it is made up of alternating dark and bright segments (Fig. 7), but the orientation signal of two jointly exposed lines can be summed when they are about 10 arcmin apart or more in the fovea—although there seems to be the need for strict collinearity (Brincat and Westheimer, 2000; Westheimer and Ley, 1997). For the detection of contrast differences, data from several studies were summarized by Dresp who concluded that in interactions between neighboring stimuli—for example, potentiation or sensitization—there are contrast polarity influences, depending on the separation (Dresp, 1999). In a field in which dot pairs with short separation are arrayed in a distinct fashion, e.g., all with radial or circular displacements (Glass patterns), the overall pattern is clearly
evident when both members of the pair have the same contrast polarity, both black or white, but the percept is severely impaired when the members of the pairs have opposite contrast polarity (Badcock et al., 2005; Glass and Switkes, 1976; Fig. 9). There are indications that the effect is asymmetrical. Neither the putative processing apparatus nor the interaction distances provide certainty at this juncture whether the task fits into the present category or whether it should really be included among those discussed below, i.e., where interaction takes place between pattern elements that have already been fully articulated. In experiments using random-dot cinematograms to study global motion processing, Edwards and Badcock concluded that ON and OFF signals remained separate at a beginning stage of motion detection because no motion is seen when a dot changed contrast-polarity during a stroboscopic displacement. But at higher levels of the motion processing there was sub-threshold summation of white and black dots, implying that at that stage integration of information from the two streams had taken place (Edwards and Badcock, 1994). The interaction between components of a stroboscopic stimulus pair is, however, somewhat more nuanced. A line changing contrast polarity when it is suddenly displaced can indeed generate a stroboscopic movement, but for some temporal and spatial intervals this movement is in the reverse direction, the so-called inverse phi phenomenon (Anstis, 1970). A modern viewpoint of the cortical mechanism of movement detection (Adelson and Bergen,
- as validated by intracellular recording in mammalian cortical neurons (Priebe and Ferster, 2005) makes this readily understood: the temporal sequence of two stimuli with the same contrast polarity will excite the central lobe of the temporal–spatial receptive field, but excitation can also ensue if the later member of the stimulus pair is of the opposite contrast polarity and has a temporal–spatial location that places it in the (opponent) flanking zone of the receptive field. For this to occur, its displacement needs to be in the opposite direction. This phenomenon thus belongs to the category where there are spatial (here spatio- temporal) subregions of a unit’s receptive field fed by ON and OFF fibers, each contributing according to their own sign to the cell’s response. Size-specific adaptation experiments also suggest segrega- tion of ON and OFF streams as demonstrated in the change of apparent duty cycle of square-wave gratings and bar widths after an observer had been viewing patterns of related but spatially wider configurations (De Valois, 1977). A single explanation can cover the extensive list of visual tasks in which the responses differ when two or more pattern elements are of like or unlike contrast polarity: their neural locus is at the site where the separate ON and OFF retinal streams converge, most prominently on the primary visual cortex. Such stimuli are, therefore, of particular interest in the elucidation of the mechanism through which the respective discriminations are achieved. They allow the delineation of the distances over which
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Fig. 5. Patterns in which psychophysical discrimination thresholds depend on contrast polarity of elements: (A) line vernier, (B) alignment of edges with opposite contrast polarity and (C) separation discrimination of two lines.
2 5
0
5
10
15
20
25
30 Both lines black One line black, other white
Separation Discrimination Threshold (arc secs) Line Separation (arcmins)
3 4 6 7 8
Fig. 6. Thresholds for discrimination of the separation of two parallel lines as a function of their base separation (condition (C) in Fig. 5). Performance is poorer for mixed contrast-polarity patterns only at short separations. (redrawn from Levi and Westheimer (1987)).
642 G. Westheimer / Progress in Retinal and Eye Research 26 (2007) 636–
to mixing of contrast polarity. These illusions are unfortu- nately not a uniform group, but in at least some of them the magnitude of the perceptual error depends on whether the configurations in made up entirely with lines of the same contrast polarity or not (Fig. 11). By the same token, situations in which contrast polarity does not matter can occasionally afford insight. The central apparatus of visual acuity still needs full elucidation; hence it is an important pointer that ‘‘crowding’’ of visual acuity letters, where closely adjacent bars impair performance, seems to be largely indifferent to whether the contrast-
polarity of the letter and the masking elements is the same or not (Ehrt and Hess, 2005). The neural basis of stereopsis continues to fascinate and here also, contrast-polarity issues enter, as was emphasized already by Helmholtz in the plates included in his Physiological Optics and has emerged as an analytical probe in more recent studies (Cumming and Parker, 1997).
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Fig. 9. The Glass pattern formed by duplicating each dot with a displacement is easier to discern when the duplicates have the same contrast polarity (top) than the opposite contrast polarity (bottom).
Fig. 10. Contour salience in a field of same and mixed contrast polarity of elements. Physiological evidence from the primate implicates changes in local connectivity among the neurons in the primary visual cortex in the grouping of line elements in the generation of the percept of a contour, in this case vertical line-pairs arrayed vertically in center of panel (Li and Gilbert, 2002). This appears to be largely robust to the contrast polarity of the line elements.
644 G. Westheimer / Progress in Retinal and Eye Research 26 (2007) 636–
- Benefits of ON/OFF bifurcation
The retinal recoding that produces strong and active signals in optic nerve fibers both for increases as well as for decreases in incident light can be interpreted as having benefits at two levels of visual processing, first by making the initial signals for small light changes more conspicuous, and, secondly, by accenting and segmenting contrast polarity of visual elements for purposes of perception.
5.1. Conspicuity of impulse responses over large dynamic range
Setting the discharge frequency of retinal output neurons at a non-zero level during steady light stimulation becomes an option once adaptation (in part even photochemical in origin) decouples the neural state from the magnitude of the invariant incident light intensity, and thus allows both increases and decreases in light to be represented by equivalent changes in impulse rates. Because there is always a greater range of possible light increases than decreases, the maintained steady-state discharge frequency would have to be quite high to allow a good range of signal levels in both the up and the down directions. It is presumably for this reason that a second analogous system with sign-inversion has evolved, assuring that at least one of them provides a well-defined signal. In principle, a single ON channel can convey the needed information and it is telling that the sign inversion needed for spatial surround antagonism in constructing retinal center/surround recep- tive fields is provided not by an opponent-stream signal but by inhibitory interaction arising from the same-polarity stream. The well-known phenomenon of successive contrast, in which a sudden change in light intensity gives a strongly contrasting experience is a manifestation of this organiza-
tion. When a step increase of light is presented to the eye, the ON retinal ganglion cell will respond with an additional burst superimposed on their sputtering spontaneous activity, and the OFF ganglion cell’s spontaneous activity will be briefly silenced. This pattern is maintained in the LGN (Lateral Geniculate Nucleus) cells that become the cortical input. It has been shown that the visual field representing on the retinal surface is seamlessly tiled by overlapping ON and OFF ganglion cells (Waessle et al.,
- and superposition of their inputs ensures that this is the case also for neurons in the primary visual cortex (Martinez et al., 2005). This push–pull effect explains how the retinal ON and OFF dichotomy, associated as it is with overlap at the retina and accurate superposition in the cortex, can act to enhance the magnitude of the cortical signal to a temporal light change. The case for a darkening pulse is equivalent, with a reversal of the roles of the ON and OFF ganglion cells. Most studies in the visual cortex have been devoted to the spatial profile of the receptive fields, showing that there is a convergence and spatially meaningfully ordering of retinal ON and OFF inputs in the interest of building up the spatial profile characteristic to the cell. Though both are needed for optimum results, nevertheless the cell will generate a signal to one alone, illustrating that, just as ON–OFF interaction is not necessary for center/surround antagonism in the retina, so it is quite possible that similar spatial differentiation within receptive fields could be achieved by suitable circuitry involving just one of these streams.
5.2. Contrast polarity as a feature label
As is obvious from inspection of Figs. 8–11, contrast polarity is an immediate and compelling perceptual property of a feature. The difference in character between features with positive and negative contrast is a great advantage in the articulation of forms and objects in the perceptual process. But receptive fields of neurons in the primary visual cortex arise through a confluence of ON and OFF signals onto their subregions, so that each cell can no longer be regarded as belonging to either the ON or the OFF stream, as is the case for the preceding neurons. That is not a problem so long as the units are assumed to represent detectors or templates with particular spatial profiles, such as a Gabor patch. That single isolated features have a well-defined darkness or whiteness label, on the other hand, requires operations in which information on this attribute, which is fully contained in earlier visual stages, be conserved and ultimately bound with output from other processes to yield the unitary percept. Regardless of how it is implemented, there is something categorical in the way, against a gray background, black and a white targets present themselves. The difference is qualitative, not just quantitative as would be the case if merely a photon count per unit of space and time were being performed.
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Fig. 11. The apparent misalignment of the transverses in the Poggendorff illusion depends on the contrast polarity of the line elements of the pattern; the illusion is much weaker when black and white lines are intermingled in the pattern construct.
G. Westheimer / Progress in Retinal and Eye Research 26 (2007) 636–648 645
purposes of elaborating shape and form and contour, with parallel mechanisms not only for movement and perhaps depth, but also for color—all this with the need for binding signals for each of these attributes to allow for the emergence of a unitary percept. If Hering’s usual prescience is eventually confirmed, the continuum which has black and white as its poles will be found to be subserved by a circuit separate from that which generates the spatially diverse receptive fields in the primary visual cortex and more akin to that for chromaticity. And its source surely cannot exist apart from the retinal ON/OFF dichotomy any more than that of color from the retinal signals encoded from the red, green and blue cones.
- Future directions
That black and white are seen as antagonists rather than end-points in a single continuum, preceded visual science as a discipline and, surviving the physicists’ teaching of a monotonic rise in energy absorption and photochemical activity with increasing incident light levels, received underpinning from the discovery of separate ON and OFF signals in the retina. The dichotomy has its origin at the very first synapse in the visual system where receptor signals are transmitted to the next tier of retinal cells; the molecular events here are only beginning to be unraveled and several steps interven- ing between the change in receptor cell membrane and the opening of ion channels in the bipolar cells remain to be elucidated, specifically the operations associated with the ionotropic and metabotropic glutamate receptors where genetic intervention has and should continue to provide clues. In view of the complex and deeply intertwined circuitry of the retina, the apparently sharp dissociation between ON and OFF streams in this structure seems surprising and may need further probing, especially since it is being questioned not only in necturus (Pang et al., 2007) but also in the mouse (Renteria et al., 2006). In the same vein, the full separation of pathways into the cortex, drawn schematically in Fig. 3, may have to be revised, in particular since subtle interaction in the LGN has already been reported. The most intriguing question relates to the provenance of the perceptually distinct attributes of black and white. Their opponent nature is at least of the same kind as that of yellow vs. blue and red vs. green, even though the intermediate stages of gray seem to have more unity than the spectral intermediates. How are the signals threaded through the cortex so as to allow the emergence of such a categorical distinction while they at the same time converge to operate in a push–pull fashion in the generation of receptive fields with spatially antagonistic subregions? And if there is indeed a separate elaboration of blackness and whiteness via subsidiary pathways, what are the similarities and differences to those responsible for the chromatic attributes?
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