Contextual modulation revealed by optical imaging exhibits figural asymmetry in macaque V1 and V2

Abstract

Neurons in early visual cortical areas are influenced by stimuli presented well beyond the confines of their classical receptive fields, endowing them with the ability to encode fine-scale features while also having access to the global context of the visual scene. This property can potentially define a role for the early visual cortex to contribute to a number of important visual functions, such as surface segmentation and figure-ground segregation. It is unknown how extraclassical response properties conform to the functional architecture of the visual cortex, given the high degree of functional specialization in areas V1 and V2. We examined the spatial relationships of contextual activations in macaque V1 and V2 with intrinsic signal optical imaging. Using figure-ground stimulus configurations defined by orientation or motion, we found that extraclassical modulation is restricted to the cortical representations of the figural component of the stimulus. These modulations were positive in sign, suggesting a relative enhancement in neuronal activity that may reflect an excitatory influence. Orientation and motion cues produced similar patterns of activation that traversed the functional subdivisions of V2. The asymmetrical nature of the enhancement demonstrated the capacity for visual cortical areas as early as V1 to contribute to figure-ground segregation, and the results suggest that this information can be extracted from the population activity constrained only by retinotopy, and not the underlying functional organization.

Keywords: extrastriate; figure-ground; functional organization; segmentation; striate.

Figure 1

Contextual modulation in V1. Notes: (A) A representative spot-activation map from area V1 of monkey 1,047 was taken from the region shown in the inset. The stimulus-spot size was 2°. The value of each pixel represents the area under the receiver-operating characteristic curve (AUC) computed from six blocks of four trials each. Figural (Fig) and background (Bkg) regions of interest are indicated. Scale bar 1 mm. (B) The time courses of the average AUC values within the Fig and Bkg regions of interest in A, normalized by the first prestimulus frame, show the divergence of the responses to the two stimuli. The stimulus appeared at t=0 and persisted throughout the remainder of the time course. Gray shading represents 1 standard deviation. Time values are rounded for clarity.

Figure 2

Optical imaging reveals figural enhancement. Notes: Activation maps were obtained from ten blocks of four trials each in monkey 1,045. These images indicate that response enhancement specific to the spot (A), orientation (Ori)-contrast (B), and motion (Mot)-contrast (C) conditions resides in the medial portion of the imaged field, and is present in both V1 (bottom) and V2 (top). Scale bar 1 mm. Abbreviation: AUC, area under the curve.

Figure 3

Enhancement is confined to the figural (Fig) region. Notes: Area under the curve (AUC) values were obtained from spot (A), orientation (Ori)-contrast (B), and motion (Mot)-contrast (C) conditions from Fig and background (Bkg) regions of interest of all five monkeys, showing the consistent effect across animals. Each point corresponds to the mean AUC value measured in a single animal in the 1- to 2-second period following stimulus onset.

Figure 4

Localization of the figural region using an orientation map. Notes: (A) A difference image was obtained from the average of six blocks of four trials each from monkey 1,032. This image was constructed by subtracting the mean image obtained with homogeneous vertical gratings from that obtained with homogeneous horizontal gratings. Dark patches indicate areas more strongly activated by horizontal gratings; light patches correspond to stronger vertical activation. Pale and thick stripes contain orientation maps; one such stripe is referenced by the arrow. (B) We multiplied the homogeneous condition-orientation map shown in A with the contrast-orientation map (not pictured). Prior to the multiplication, both maps were high-pass filtered using a Gaussian filter with σ=38.5 pixels. Yellow pixels correspond to mutual activation between maps, while blue pixels correspond to opposite activation. The dashed line is used as a landmark to show the approximate border, defined by the spot-activation map shown in the inset. (C) The orientation contrast-activation map is shown for the imaging session depicted in A and B. The dashed line was defined by the spot-activation map. Scale bar 1 mm. Abbreviations: Corr, correlation; ROC, receiver-operating characteristic; AUC, area under the curve.

Figure 5

Figural enhancement extends across a large expanse of V2. Notes: V2-activation maps are shown for all four monkeys in which V2 was imaged. The first case (monkey 1,032) corresponds to the images shown in Figure 4. The second case (monkey 1,045) was previously presented in Figure 2. The outlines correspond to the computed figural regions of interest, as described in the Materials and methods section, which depict the extent of enhancement by spot, orientation (Ori)-contrast, or motion (Mot)-contrast stimulation in comparison to homogeneous stimulation. Asterisks in the first and third cases denote masking of the signal by flare artifacts produced by large surface vasculature. Below each illustration is an estimate of the horizontal extent of these activation regions, taken as the length of the axis parallel to the V1–V2 border of a best-fit ellipse. For each case, the three estimates were generally similar to one another and typically exceeded ~2.5 mm, indicating that figure–ground enhancement usually activated multiple adjacent-stripe compartments.