SUMMARY1. This paper introduces a new technique for the analysis of the chromatic properties of neurones, and applies it to cells in the lateral geniculate nucleus (l.g.n.) of macaque. The method exploits the fact that for any cell that combines linearly the signals from cones there is a restricted set of lights to which it is equally sensitive, and whose members can be exchanged for one another without evoking a response.2. Stimuli are represented in a three-dimensional space defined by (a) an axis along which only luminance varies, without change in chromaticity, (b) a 'constant B' axis along which chromaticity varies without changing the excitation of blue-sensitive (B) cones, (c) a 'constant R & G' axis along which chromaticity varies without change in the excitation of red-sensitive (R) or green-sensitive (G) cones. The orthogonal axes intersect at a white point. The isoluminant plane defined by the intersection of the ' constant B' and 'constant R & G' axes contains lights that vary only in chromatic As j In polar coordinates the constant B axis is assigned the azimuth 0-180 deg, and the constant R & G axis the azimuth 90-270 deg. Luminance is expressed as elevation above or below the isoluminant plane (-90 to + 90 deg).3. For any cell that combines cone signals linearly, there is one plane in this space, passing through the white point, that contains all lights that can be exchanged silently. The position of this 'null plane' provides the 'signature' of the cell, and is specified by its azimuth (the direction in which it intersects the isoluminant plane of the stimulus space) and its elevation (its angle of inclination to the isoluminant plane).4. A colour television receiver was used to produce sinusoidal gratings whose chromaticity and luminance could be modulated along any vector passing through the white point in the space described. The spatial and temporal frequencies of modulation could be varied over a large range. A. M. DERRINGTON, J. KRA USKOPF AND P. LENNIE from only R and G cones. These we call R-G cells. The null planes ofthe smaller group were narrowly distributed about an azimuth of 178-4 deg and an elevation of deg, which suggests that these cells receive inputs from B cones almost equally opposed by some combined input from R and G cones. We call these B-(R & G) cells. No cells were found that lacked chromatic opponency.6. By assuming that the spectral sensitivities of the macaque's cones are like those of man's, the azimuths and elevations of the null planes can be transformed by the use of Smith & Pokorny's (1975) fundamental spectral sensitivities to yield the weights attached by each cell to signals from the three classes of cone. This representation shows that cells that receive inputs from B cones have these inputs opposed by varying combinations of inputs from R and G cones.7. Raising the spatial frequency of a grating systematically reduced the elevations but did not systematically alter the azimuths of the null planes of parvocellular units. This change, which was more pronounc...
SUMMARY1. The discharges of single neurones in the parvocellular and magnocellular laminae of the macaque's lateral geniculate nucleus (l.g.n.) were recorded with glass-insulated tungsten micro-electrodes.2. Linearity of spatial summation was examined using the test devised by Hochstein & Shapley (1976). 2 of 272 parvocellular units and 6 of 105 magnocellular units showed clearly non-linear spatial summation. A quantitative index of nonlinearity did not suggest the existence of a distinct 'non-linear' class of magnocellular unit.3. Spatial contrast sensitivity to moving gratings was measured by a tracking procedure in which contrast was adjusted to elicit a reliable modulation of discharge. With the exception of cells that were driven by blue-sensitive cones, measurements of contrast sensitivity did not reveal distinct subgroups of parvocellular units. All had low sensitivity, and those with receptive fields in the fovea could resolve spatial frequencies of up to 40 cycles deg-'. Magnocellular units had substantially higher sensitivity, but poorer spatial resolution.4. The higher sensitivities of magnocellular units led to their giving saturated responses to stimuli of high contrast. Responses of parvocellular units were rarely saturated by any stimulus.5. At any one eccentricity the receptive fields of parvocellular units had smaller centres than did those of magnocellular units. Receptive fields of magnocellular units driven by the ipsilateral eye had larger receptive fields than did those driven by the contralateral eye.6. Parvocellular units were most sensitive to stimuli modulated at temporal frequencies close to 10 Hz; magnocellular units to stimuli modulated at frequencies nearer 20 Hz. The loss of sensitivity as temporal frequency fell below optimum was more marked in magnocellular than parvocellular units.7. Changes in temporal frequency altered the shapes of the spatial contrast sensitivity curves of both parvocellular and magnocellular units. These changes could be explained by supposing that centre and surround have different temporal properties, and that the surround is relatively less sensitive to higher temporal frequencies.
Electrophysiological recordings show that individual neurons in cortex are strongly activated when engaged in appropriate tasks, but they tell us little about how many neurons might be engaged by a task, which is important to know if we are to understand how cortex encodes information. For human cortex, I estimate the cost of individual spikes, then, from the known energy consumption of cortex, I establish how many neurons can be active concurrently. The cost of a single spike is high, and this severely limits, possibly to fewer than 1%, the number of neurons that can be substantially active concurrently. The high cost of spikes requires the brain not only to use representational codes that rely on very few active neurons, but also to allocate its energy resources flexibly among cortical regions according to task demand. The latter constraint explains the investment in local control of hemodynamics, exploited by functional magnetic resonance imaging, and the need for mechanisms of selective attention.
We measured the responses of 305 neurons in striate cortex to moving sinusoidal gratings modulated in chromaticity and luminance about a fixed white point. Stimuli were represented in a 3-dimensional color space defined by 2 chromatic axes and a third along which luminance varied. With rare exceptions the chromatic properties of cortical neurons were well described by a linear model in which the response of a cell is proportional to the sum (for complex cells, the rectified sum) of the signals from the 3 classes of cones. For each cell there is a vector passing through the white point along which modulation gives rise to a maximal response. The elevation (theta m) and azimuth (phi m) of this vector fully describe the chromatic properties of the cell. The linear model also describes neurons in l.g.n. (Derrington et al., 1984), so most neurons in striate cortex have the same chromatic selectivity as do neurons in l.g.n. However, the distributions of preferred vectors differed in cortex and l.g.n.: Most cortical neurons preferred modulation along vectors lying close to the achromatic axis and those showing overt chromatic opponency did not fall into the clearly defined chromatic groups seen in l.g.n. The neurons most responsive to chromatic modulation (found mainly in layers IVA, IVC beta, and VI) had poor orientation selectivity, and responded to chromatic modulation of a spatially uniform field at least as well as they did to any grating. We encountered neurons with band-pass spatial selectivity for chromatically modulated stimuli in layers II/III and VI. Most had complex receptive fields. Neurons in layer II/III did not fall into distinct groups according to their chromatic sensitivities, and the chromatic properties of neurons known to lie within regions rich in cytochrome oxidase appeared no different from those of neurons in the interstices. Six neurons, all of which resembled simple cells, showed unusually sharp chromatic selectivity.
The response of a neuron in striate cortex to an optimally configured visual stimulus is generally reduced when the stimulus is enlarged to encroach on a suppressive region that surrounds its classical receptive field (CRF). To characterize the mechanism that gives rise to this suppression, we measured its spatiotemporal tuning, its susceptibility to contrast adaptation, and its capacity for interocular transfer. Responses to an optimally configured grating confined to the CRF were strongly suppressed by annular surrounding gratings drifting at a wide range of temporal and spatial frequencies (including spatially uniform fields) that extended from well below to well above the range that drives most cortical neurons. Suppression from gratings capable of driving cortical CRFs was profoundly reduced by contrast adaptation and showed substantial interocular transfer. Suppression from stimuli that lay outside the spatiotemporal passband of most cortical CRFs was relatively stronger when the stimulus on the CRF was of low contrast, was generally insusceptible to contrast adaptation, and showed little interocular transfer. Our findings point to the existence of two mechanisms of surround suppression: one that is prominent when high-contrast stimuli drive the CRF, is orientation selective, has relatively sharp spatiotemporal tuning, is binocularly driven, and can be substantially desensitized by adaptation; the other is relatively more prominent when low-contrast stimuli drive the CRF, has very broad spatiotemporal tuning, is monocularly driven, and is insusceptible to adaptation. Its character suggests an origin in the input layers of primary visual cortex, or earlier.
Complex cells in striate cortex of macaque showed a rapid pattern-specific adaptation. Adaptation made cells more sensitive to orientation change near the adapting orientation. It reduced correlations among the responses of populations of cells, thereby increasing the information transmitted by each action potential. These changes were brought about by brief exposures to stationary patterns, on the time scale of a single fixation. Thus, if successive fixations expose neurons' receptive fields to images with similar but not identical structure, adaptation will remove correlations and improve discriminability.
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