Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. J Physiol

Department of Neurobiology, Max Planck Institute for Biophysical Chemistry, Göttingen, West Germany.
The Journal of Physiology (Impact Factor: 5.04). 01/1993; 458(1):191-221. DOI: 10.1113/jphysiol.1992.sp019413
Source: PubMed


1. We measured the response of macaque ganglion cells to sinusoidally modulated red and green lights as the relative phase, theta, of the lights was varied. 2. At low frequencies, red-green ganglion cells of the parvocellular (PC-) pathway with opponent inputs from middle-wavelength sensitive (M-) and long-wavelength sensitive (L-) cones were minimally sensitive to luminance modulation (theta = 0 deg) and maximally sensitive to chromatic modulation (theta = 180 deg). With increasing frequency, the phase, theta, of minimal amplitude gradually changed, in opposite directions for cells with M- and L-cone centres. 3. At high frequencies (at and above 20 Hz), phasic cells of the magnocellular (MC-) pathway were maximally responsive when theta approximately 0 deg and minimally responsive when theta approximately 180 deg, as expected from an achromatic mechanism. At lower frequencies, the phase of minimal response shifted, for both on- and off-centre cells, to values of theta intermediate between 0 and 180 deg. This phase asymmetry was absent if the centre alone was stimulated with a small field. 4. For PC-pathway cells, it was possible to provide an account of response phase as a function of theta, using a model involving three parameters; phases of the L- and M-cone mechanisms and a L/M cone weighting term. For red-green cells, the phase parameters were monotonically related to temporal frequency and revealed a centre-surround phase difference. The phase difference was linear with a slope of 1-3 deg Hz-1. If this represents a latency difference, it would be 3-8 ms. Otherwise, temporal properties of the M- and L-cones appeared similar if not identical. By addition of a scaling term, the model could be extended to give an adequate account of the amplitude of responses. 5. We were able to activate selectively the surrounds of cells with short-wavelength (S-) cone input to their centres, and so were able to assess L/M cone weighting to the surround. M- and L-cone inputs added linearly for most cells. On average, the weighting corresponded to the Judd modification of the luminosity function although there was considerable inter-cell variability. 6. To account for results from MC-pathway cells, it was necessary to postulate a cone-opponent, chromatic input to their surrounds. We developed a receptive field model with linear summation of M- and L-cones to centre and surround, and with an additional M,L-cone opponent input to the surround.(ABSTRACT TRUNCATED AT 400 WORDS)

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Available from: Arne Valberg, Oct 09, 2015
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    • "Recent studies of color vision (see Shapley and Hawken, 2011 for a review) have mainly dealt with the properties of the neural channels that lead from the retina via the lateral geniculate nucleus to the higher visual centers of the brain. Anatomical and morphological studies have been complemented with neurophysiological recordings, the latter often using system-theoretical methods like mathematical Fourier analysis of sensitivity and response (Lee et al., 1990; Smith et al., 1992). Within this mechanistic framework the nerve cells are treated as filters of optical information. "
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    ABSTRACT: The tree-receptor theory of human color vision accounts for color matching. A bottom-up, non-linear model combining cone signals in six types of cone-opponent cells in the lateral geniculate nucleus (LGN) of primates describes the phenomenological dimensions hue, color strength, and lightness/brightness. Hue shifts with light intensity (the Bezold-Brücke phenomenon), and saturation (the Abney effect) are also accounted for by the opponent model. At the threshold level, sensitivities of the more sensitive primate cells correspond well with human psychophysical thresholds. Conventional Fourier analysis serves well in dealing with the discrimination data, but here we want to take a look at non-linearity, i.e., the neural correlates to perception of color phenomena for small and large fields that span several decades of relative light intensity. We are particularly interested in the mathematical description of spectral opponency, receptive fields, the balance of excitation and inhibition when stimulus size changes, and retina-to-LGN thresholds.
    Psychology and Neuroscience 12/2013; 6(2):213-218. DOI:10.3922/j.psns.2013.2.09
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    • "Thus, there is imbalance in spectral inputs to centre and surround, allowing opponent colour signals to be transmitted to the brain without evolution of new colour-selective pathways. Consistent with this hypothesis, there is broad agreement that the majority of PC pathway cells show centre–surround organization, and that red–green opponency can arise from centre–surround interaction (Dreher et al. 1976; Derrington et al. 1984; Kaplan & Shapley, 1986; Smith et al. 1992; Lankheet et al. 1998; Kilavik et al. 2003; Blessing et al. 2004; Diller et al. 2004; Solomon et al. 2005; Buzás et al. 2006; Crook et al. 2011). By contrast, according to the original 'two channel' model for chromatic signal transmission, chromatic signals are carried by specific populations of cells showing ('type II') opposing spectral inputs to large and overlapping receptive field regions (Wiesel & Hubel, 1966; Dreher et al. 1976; Rodieck, 1991; Calkins & Sterling, 1999; Conway et al. 2010). "
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    ABSTRACT: Non-technical summary Colour gets a free ride, according to our study of visual nerve cell responses in marmoset monkeys. All male marmosets are red–green colour-blind (dichromatic), but most female marmosets have normal trichromatic colour vision. It is known that signals for high-acuity daytime vision are carried in the parvocellular (P) pathway, and the P pathway also carries signals for red–green colour vision in trichromats. Here we compared P cell responses with patterned stimuli in dichromatic and trichromatic marmosets, and found no detectable difference in resolving power for fine patterns. These results indicate that red–green colour vision does not come at a cost for spatial vision. The ‘piggyback ride’ for colour signals in the P pathway may have encouraged the evolution of full colour vision in primates, including great apes, monkeys and humans. Abstract The red–green axis of colour vision evolved recently in primate evolutionary history. Signals serving red–green colour vision travel together with signals serving spatial vision, in the parvocellular (PC) division of the subcortical visual pathway. However, the question of whether receptive fields of PC pathway cells are specialized to transmit red–green colour signals remains unresolved. We addressed this question in single-cell recordings from the lateral geniculate nucleus of anaesthetized marmosets. Marmosets show a high proportion of dichromatic (red–green colour-blind) individuals, allowing spatial and colour tuning properties of PC cells to be directly compared in dichromatic and trichromatic visual systems. We measured spatial frequency tuning for sine gratings that provided selective stimulation of individual photoreceptor types. We found that in trichromatic marmosets, the foveal visual field representation is dominated by red–green colour-selective PC cells. Colour selectivity of PC cells is reduced at greater eccentricities, but cone inputs to centre and surround are biased to create more selectivity than predicted by a purely ‘random wiring’ model. Thus, one-to-one connections in the fovea are sufficient, but not necessary, to create colour-selective responses. The distribution of spatial tuning properties for achromatic stimuli shows almost complete overlap between PC cells recorded in dichromatic and trichromatic marmosets. These data indicate that transmission of red–green colour signals has been enabled by centre–surround receptive fields of PC cells, and has not altered the capacity of PC cells to serve high-acuity vision at high stimulus contrast.
    The Journal of Physiology 06/2011; 589(Pt 11):2795-812. DOI:10.1113/jphysiol.2010.194076 · 5.04 Impact Factor
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    • "Additional tests, e.g. measuring responses to heterochromatically modulated lights (Smith et al. 1992), were employed in cases when identification was difficult. PC cells can generally be identified by their tonic responses and spectral opponency, and MC cells by their phasic responses and lack of spectral opponency. "
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    ABSTRACT: Segregation of chromatic and luminance signals in afferent pathways are investigated with a grating stimulus containing luminance and chromatic components of different spatial frequencies. Ganglion cell recordings were obtained from the retinae of macaques (Macaca fascicularis). Cell responses to the 'compound' gratings were compared to responses to standard chromatic and luminance gratings. Parvocellular (PC) pathway cell responses to compound and chromatic gratings were very similar, as were magnocellular (MC) cell responses to compound and luminance gratings. This was the case over a broad range of spatial and temporal frequencies and contrasts. In psychophysical experiments with human observers, discrimination between grating types was possible close to detection threshold. These results are consistent with chromatic and luminance structure in complex patterns being strictly localized in different afferent pathways. This novel stimulus may prove useful in identifying afferent inputs to cortical neurons.
    The Journal of Physiology 10/2010; 589(Pt 1):59-73. DOI:10.1113/jphysiol.2010.188862 · 5.04 Impact Factor
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