1243_book.fm Page 109 Thursday, May 22, 2003 10:45 AM Modular Complexity of 5 Area V2 in the Macaque Monkey Anna W. Roe CONTENTS 5.1 Introduction ..................................................................................................109 5.1.1 Optical Imaging of V2 .....................................................................110 5.2 Redefining Relationships with V1 ...............................................................112 5.2.1 Revision of Anatomical Connectivity..............................................112 5.2.2 Functional V1–V2 Interactions Revealed by Cross-Correlation.....116 5.2.3 Blobs-to-Thin Stripes: Three Classes of Color Interactions...........117 5.2.4 Interblobs-to-Thick/Pale Stripes: Two Classes of Oriented Interactions .......................................................................................117 5.3 Modular Complexity within V2 Stripes ......................................................118 5.3.1 Thin Stripes: Modular Representation of Surface Color and Brightness.........................................................................................119 5.3.2 Thick/Pale Stripes: Modular Representation of Complex Contours ...........................................................................................121 5.3.2.1 Diversity of Higher-Order Contour Cells in V2 ..............121 5.3.2.2 Localization: Evidence for Complex Orientation Domains in V2..................................................................123 5.3.2.3 Feedback: Changing Balance between Two Orientation Networks ...........................................................................123 5.3.3 Thick Stripes: Modular Representation of Relative Disparity........126 5.4 Border and Surface Capture: Foundation for Figure Integration................127 5.5 Summary and Proposal ................................................................................130 Acknowledgments..................................................................................................132 References..............................................................................................................132 5.1 INTRODUCTION Area V2 has traditionally been thought of as the second stage of visual cortical processing in the primate. In addition to receiving ascending feedforward inputs 0-8493-1243-4/02/$0.00+$1.50 © 2003 by CRC Press LLC 109 1243_book.fm Page 110 Thursday, May 22, 2003 10:45 AM 110 The Primate Visual System from primary visual cortex (V1), V2 also receives thalamic input from the pulvinar as well as significant feedback from visual areas in both the ventral and dorsal streams. Thus, as a distribution center for ascending magnocellular, parvocellular, and koniocellular derived inputs from the lateral geniculate nucleus (LGN), V2 is strategically positioned as both an integrator and feedback control point of what and where information. In both Old World and New World monkeys, when stained for cytochrome oxidase,1 V2 is characterized by a pattern of alternating dark and light cytochrome oxidase stripes.2,3 In general, these stripes run perpendicular to the V1/V2 border and alternate in a thin/pale/thick/pale manner from the central (lateral cortex) to peripheral (medial cortex) visual field representations in V2. In the macaque monkey there are approximately 14 sets of thin/pale/thick/pale stripes in dorsal V2, with each set spanning on average 4 mm across. This pattern has also been confirmed by other anatomical staining methods such as Cat-301 staining, which reveals the thick stripes,4,5 and staining for NOS/NADPH.6 These stripe organizations are established early in development and, at least from studies thus far, remain in the face of manipulations in visual experience.7,8 Thus, V2 stripes can be viewed as develop- mental,9 evolutionary10 (cf. Reference 11), and/or functional12,13 entities. The long-standing view that the thin, pale, and thick stripes subserve a tripartite division of color, form, and depth information processing in the early visual pathway has been supported by electrophysiological,12–16 2-deoxyglucose,17,18 and optical imaging studies.13,19–21 This functional segregation in V2 has found compelling parallels in psychophysics of orientation, color, and depth perception.22,23 However, these broad descriptions by no means suggest uniformity of any single stripe. In fact, it is clear that each stripe contains a mixture of response types,16,21,24,25 that neuronal responses are multimodal in nature (e.g., Reference 26), and that there is a significant and important degree of form, color, and disparity integration in V2. Unraveling how functional segregation and multimodal integration are incorporated is the key to understanding V2 function. It is also important to note that, in addition to their uneven and blobby appear- ance, V2 cytochrome stripes exhibit variations in patterning. At times, dark cyto- chrome stripes are seen merging with one another or failing to follow the classic thin/thick alternation. Furthermore, given the variability in the widths of dark cyto- chrome stripes, the relationship of “thick” cytochrome stripes with “disparity” and “thin” cytochrome stripes with “color” is a fickle one (for review, see Reference 27). Despite this, the terms “thin” and “thick” have become strongly associated with the functional terms “color” and “disparity.” Following this usage, in this chapter, the terms “thin” and “thick” are based on the conceptual functional view of what thin and thick stripes are (i.e., “color” or “disparity,” respectively) and not the thickness of stripe as seen in cytochrome oxidase staining. 5.1.1 OPTICAL IMAGING OF V2 Perhaps one of the most compelling views of functional division in V2 is visual- ization of stripe compartments by optical imaging methods. Intrinsic signal optical imaging is a functional mapping method that measures changes in cortical 1243_book.fm Page 111 Thursday, May 22, 2003 10:45 AM Modular Complexity of Area V2 in the Macaque Monkey 111 reflectance derived from changes in hemodynamic signals (for review, see Refer- ences 28 and 29). The primary advantage of this method is its high spatial resolution (tens of microns), which permits the visualization of 50 to 200 mm size functional domains. Because of the limitations of optical penetration and light scatter, detec- tion is thus far limited to the superficial cortical layers (although cf. Reference 30). By definition, optical imaging reveals a representation of the local population response; that is, the predominant response summed over many cells. Therefore, (1) imaged response is still consistent with a diversity of single unit responses at a single locale and does not indicate unitary function at any single location, (2) it is useful for revealing local biases in representation that may not be evident from single unit studies, and (3) in combination with single unit studies, it can provide a joint single unit/local population view of the local neuronal response. Despite its limitations (superficial layers only, slow temporal resolution, limited to exposed cortex), intrinsic signal imaging has proved useful for mapping well-established functional organizations, for revealing novel organizations (e.g., References 31 and 32), and promises to be a useful tool for studying cortical activation in the awake- behaving monkey.33–38 In the macaque monkey, most of dorsal V2 is buried within the lunate sulcus, leaving a 0.5- to 2-mm-wide strip just posterior to the lunate available on the surface for imaging (Figure 5.1A). Because cells in V2 are predominantly binocular, the V2 border with V1 is clearly demarcated by the lack of ocular dominance columns (Figure 5.1B, upper panel). Functional maps are obtained by imaging the cortex during visual stimulation with stimuli such as achromatic sinusoidal gratings and isoluminant color gratings presented at different orientations. Stimulus-induced acti- vation (usually seen as darkening or decrease in tissue reflectance) of cortical activity reveals functional organizations such as ocular dominance columns, orientation domains, blobs, and interblobs in V1, and stripe structures in V2. As shown in Figure 5.1, the thick/pale stripe location is clearly revealed by mapping for orientation (Figure 5.1B, lower panel). Dark cytochrome oxidase stripes can also be determined by mapping for general activation (Figure 5.1C, middle panel). Together with cyto- chrome oxidase histology (Figure 5.1C, top panel), which alone often leaves stripe identity uncertain, thick, pale, and thin stripes can be determined with reasonable confidence (Figure 5.1C). Other methods for mapping stripes, such as color or color vs. luminance response (see Figure 5.4 below), monocularity vs. binocularity (see Figure 5.6 below), and disparity response, will be discussed later in this chapter. Recent studies have furthered our understanding of both the internal organization of V2 and its relationship to V1. These new developments, deriving from studies using anatomical tract tracing, optical imaging, and electrophysiological methods, have led to further modifications and refinement of the long-standing views of V1–V2 connectivity. These new views have developed hand-in-hand with new understand- ings of V2 architecture and hypotheses regarding its relationship to visual perception. The goal of this chapter is to review and integrate these recent developments in our understanding of V2, and propose a conceptual framework for the role of V2 in visual processing. The studies described center on