Differences in orientation tuning between pinwheel and domain neurons in primary visual cortex depend on contrast and size.

Intrinsic signal optical imaging reveals a highly modular map of orientation preference in the primary visual cortex (V1) of several species. This orientation map is characterized by domains and pinwheels where local circuitry is either more or less orientation selective, respectively. It has now been repeatedly demonstrated that neurons in pinwheels tend to be more broadly tuned to orientation, likely due to the broad range of orientation preference of the neighboring neurons forming pinwheels. However, certain stimulus conditions, such as a decrease in contrast or an increase in size, significantly sharpen tuning widths of V1 neurons. Here, we find that pinwheel neuron tuning widths are broader than domain neurons only for high contrast, optimally sized stimuli, conditions that maximize excitation through feedforward, and local cortical processing. When contrast was lowered or size increased, orientation tuning width sharpened and became equal. These latter conditions are conducive to less local excitation either through lower feedforward drive or by surround suppression arising from long-range cortical circuits. Tuning width differences between pinwheel and domain neurons likely arise through more local circuitry and are overcome through recruitment of longer-range cortical circuits.

Contrast invariance of orientation tuning in cat primary visual cortex neurons depends on stimulus size.

KEY POINTS: The process of orientation tuning is an important and well-characterized feature of neurons in primary visual cortex. The combination of ascending and descending circuits involved is not only relevant to understanding visual processing but the function of neocortex in general. The classic feed-forward model of orientation tuning predicts a broadening effect due to increasing contrast; yet, experimental results consistently report contrast invariance. We show here that contrast invariance actually depends on stimulus size such that large stimuli extending beyond the neuron's receptive field engage circuits that promote invariance, whereas optimally sized, smaller stimuli result in contrast variance that is more in line with the classical orientation tuning model. These results illustrate the importance of optimizing stimulus parameters to best reflect the sensory pathways under study and provide new clues about different circuits that may be involved in variant and invariant response properties. ABSTRACT: Selective response to stimulus orientation is a key feature of neurons in primary visual cortex, yet the underlying mechanisms generating orientation tuning are not fully understood. The combination of feed-forward and cortical mechanisms involved is not only relevant to understanding visual processing but the function of neocortex in general. The classic feed-forward model predicts that orientation tuning should broaden considerably with increasing contrast; however, experimental results consistently report contrast invariance. We show here, in primary visual cortex of anaesthetized cats under neuromuscular blockade, that contrast invariance occurs when visual stimuli are large enough to include the extraclassical surround (ECS), which is likely to involve circuits of suppression that may not be entirely feed-forward in origin. On the other hand, when stimulus size is optimized to the classical receptive field of each neuron, the population average shows a statistically significant 40% increase in tuning width at high contrast, demonstrating that contrast variance of orientation tuning can occur. Conversely, our results also suggest that the phenomenon of contrast invariance relies in part on the presence of the ECS. Moreover, these results illustrate the importance of optimizing stimulus parameters to best reflect the neural pathways under study.

Parallel feedback pathways in visual cortex of cats revealed through a modified rabies virus.

The visual cortex of cats is highly evolved. Analogously to the brains of primates, large numbers of visual areas are arranged hierarchically and can be parsed into separate dorsal and ventral streams for object recognition and visuospatial representation. Within early primate visual areas, V1 and V2, and to a lesser extent V3, the two streams are relatively segregated and relayed in parallel to higher order cortex, although there is some evidence suggesting an alignment of V2 and V3 to one stream over the other. For cats, there is no evidence of anatomical segregation in areas 18 and 19, the analogs to V2 and V3. However, previous work was only qualitative in nature. Here we re-examined the feedback connectivity patterns of areas 18/19 in quantitative detail. To accomplish this, we used a genetically modified rabies virus that acts as a retrograde tracer and fills neurons with fluorescent protein. After injections into area 19, many more neurons were labeled in putative ventral stream area 21a than in putative dorsal stream region posterolateral suprasylvian complex of areas (PLS), and the dendrites of neurons in 21a were significantly more complex. Conversely, area 18 injections labeled more neurons in PLS, and these were more complex than neurons in 21a. We infer from our results that area 19 in cat is more aligned to the ventral stream and area 18 to the dorsal stream. Based on the success of our approach, we suggest that this method could be applied to resolve similar issues related to primate V3.

Orientation tuning of the suppressive extraclassical surround depends on intrinsic organization of V1.

The intrinsic functional architecture of early cortical areas in highly visual mammals is characterized by the presence of domains and pinwheels, with orientation preference of the inputs to these regions being more and less selective, respectively. We exploited this organizational feature to investigate mechanisms supporting extraclassical surround suppression, a process thought to be critical for figure ground segregation and form vision. Combining intrinsic signal optical imaging and single-unit recording in V1 of anesthetized cats, we show for the first time that the orientation tuning of the suppressive surround is sharper for domain than for pinwheel neurons. This difference depends on high center gain and is more pronounced in superficial cortex. In addition, when we remove the near component of the surround stimulus, the strength of suppression induced by the iso-oriented surround is significantly reduced for domain neurons but is unchanged for orthogonal oriented surrounds. This leads to broader orientation tuning of suppression that renders domain cells indistinguishable from pinwheel cells. Because the limited receptive field of the near surround can be accounted for by the lateral spread of long-range connections in V1, our findings suggest that intrinsic V1 circuits play a key role in the orientation tuning of extraclassical surround suppression.

Dynamics of extraclassical surround modulation in three types of V1 neurons.

Visual stimuli outside of the classical receptive field (CRF) can influence the response of neurons in primary visual cortex (V1). While recording single units in cat, we presented drifting sinusoidal gratings in circular apertures of different sizes to investigate this extraclassical surround modulation over time. For the full 2-s stimulus time course, three types of neurons were found: 1) 68% of the cells were "suppressive," 2) 25% were "plateau" cells that showed response saturation with no suppression, and 3) the remaining 6% of cells were "facilitative." Analysis of the response dynamics revealed that at response onset, activity of one-half of facilitative cells, 70% of plateau cells, and all suppressive cells is suppressed by the surround. However, over the next 20-30 ms, surround modulation changes to stronger suppression for suppressive cells, substantial facilitation for facilitative cells, and weak facilitation for plateau cells. For all three cell types, these modulatory effects then stabilize between 100 and 200 ms from stimulus onset. Thus our findings illustrate two stages of surround modulation. Early modulation is mainly suppressive regardless of cell type and, because of rapid onset, may rely on feedforward mechanisms. Surround modulation that evolves later in time is not always suppressive, depending on cell type, and may be generated through different combinations of cortical circuits. Additional analysis of modulation throughout the cortical column suggests the possibility that the larger excitatory fields of facilitative cells, primarily found in infragranular layers, may contribute to the second stage of suppression through intracolumnar circuitry.

Receptive field asymmetries produce color-dependent direction selectivity in primate lateral geniculate nucleus.

Blue-on receptive fields recorded in primate retina and lateral geniculate nucleus are customarily described as showing overlapping blue-on and yellow-off receptive field components. However, the retinal pathways feeding the blue-on and yellow-off subfields arise from spatially discrete receptor populations, and recent studies have given contradictory accounts of receptive field structure of blue-on cells. Here we analyzed responses of blue-on cells to drifting gratings, in single-cell extracellular recordings from the dorsal lateral geniculate nucleus in marmosets. We show that most blue-on cells exhibit selectivity for the drift direction of achromatic gratings. The standard concentric difference-of-Gaussians (DOG) model thus cannot account for responses of these cells. We apply a simple, anatomically plausible, extension of the DOG model. The model incorporates temporally offset elliptical two-dimensional Gaussian subfields. The model can predict color-contingent direction and spatial tuning. Because direction tuning in blue-on cells depends on stimulus chromaticity, spatial frequency, and temporal frequency, this property is of little value as a general mechanism for image movement detection. It is possible that anatomical wiring for color selectivity has constrained the capacity of blue-on cells to contribute to spatial and motion vision.

Segregation of short-wavelength sensitive ("blue") cone signals among neurons in the lateral geniculate nucleus and striate cortex of marmosets.

We measured functional input from short-wavelength selective (S) cones to neurons in the dorsal lateral geniculate nucleus (LGN) and striate cortex (area V1) in anaesthetized marmosets. We found that most magnocellular (MC) and parvocellular (PC) cells receive very little (<5%) functional input from S cones, whereas blue-on cells of the koniocellular (KC) pathway receive dominant input from S cones. Cells dominated by S cone input were not encountered in V1, but V1 cells received more S cone input than PC or MC cells. This suggests that S cone inputs are distributed broadly among neurons in V1. No differences in strength of S cone inputs were seen on comparing dichromatic and trichromatic marmosets, suggesting that the addition of a medium-long wavelength selective cone-opponent ("red-green") channel to a dichromatic visual system does not detectably affect the chromatic properties of the S cone pathways.

Color signals in the primary visual cortex of marmosets.

This study concerns the input from short-wavelength sensitive (S) cone photoreceptors to the primary visual cortex (striate cortex, Brodmann area 17, area V1) in marmosets. Signals from S-cones are thought to reach V1 by way of the koniocellular layers of the dorsal lateral geniculate nucleus. However, it is not known whether the S-cone afferent signals cause selective activation of cytochrome oxidase-rich cortical "blob" domains. To address this question, intrinsic optical signals and extracellular responses of V1 neurons were recorded. Stimuli consisted of drifting achromatic gratings and gratings that stimulated selectively either the S-cones or the medium-long wavelength sensitive (ML) cones. All stimuli produced contrast-dependent activation throughout the imaged regions of V1. The S- and ML-cone-selective stimuli produced activation levels of respectively 30% and 80% of that to achromatic gratings. No spatial variation in the strength of S-cone activation was apparent, and the ratio of S to ML activation was constant across all imaged regions. Consistently, in all of the single neurons recorded from V1, the functional input from S-cones was weaker than the input from ML-cones. We conclude that in the primary visual cortex of marmosets, S-cone signals are uniformly distributed.

Spatial coding and response redundancy in parallel visual pathways of the marmoset Callithrix jacchus.

Many neurons in the primary visual cortex (area V1) show pronounced selectivity for the orientation and spatial frequency of visual stimuli, whereas most neurons in subcortical afferent streams show little selectivity for these stimulus attributes. It has been suggested that this transformation is a functional sign of increased coding efficiency, whereby the redundancy (or overlap in response properties) is reduced at consecutive levels of visual processing. Here we compared experimentally the response redundancy in area V1 with that in the three main dorsal thalamic afferent streams, the parvocellular (PC), koniocellular (KC), and magnocellular (MC) divisions of the dorsal lateral geniculate nucleus (LGN) in marmosets. The spatial frequency and orientation tuning of single cells in the LGN and area V1 were measured, using luminance contrast sine-wave gratings. A joint spatial frequency-orientation response selectivity profile was calculated for each cell. Response redundancy for each population was estimated by cross-multiplication of the joint selectivity profiles for pairs of cells. We show that when estimated in this way, redundancy in LGN neurons is approximately double that of neurons in cortical area V1. However, there are differences between LGN subdivisions, such that the KC pathway has a spatial representation that lies between the redundant code of the PC and MC pathways and the more efficient sparse spatial code of area V1.

Chromatic and spatial properties of parvocellular cells in the lateral geniculate nucleus of the marmoset (Callithrix jacchus).

The parvocellular (PC) division of the afferent visual pathway is considered to carry neuronal signals which underlie the red-green dimension of colour vision as well as high-resolution spatial vision. In order to understand the origin of these signals, and the way in which they are combined, the responses of PC cells in dichromatic ('red-green colour-blind') and trichromatic marmosets were compared. Visual stimuli included coloured and achromatic gratings, and spatially uniform red and green lights presented at varying temporal phases and frequencies.The sensitivity of PC cells to red-green chromatic modulation was found to depend primarily on the spectral separation between the medium- and long-wavelength-sensitive cone pigments (20 or 7 nm) in the two trichromatic marmoset phenotypes studied. The temporal frequency dependence of chromatic sensitivity was consistent with centre-surround interactions. Some evidence for chromatic selectivity was seen in peripheral PC cells. The receptive field dimensions of parvocellular cells were similar in dichromatic and trichromatic animals, but the achromatic contrast sensitivity of cells was slightly higher (by about 30%) in dichromats than in trichromats. These data support the hypothesis that the primary role of the PC is to transmit high-acuity spatial signals, with red-green opponent signals appearing as an additional response dimension in trichromatic animals.