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.

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.

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.

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.

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.