Optical Imaging of FunctionalOrganization of V1 and V2 in

Marmoset Visual CortexANNA WANG ROE,1* KERSTIN FRITSCHES,2 AND JOHN D. PETTIGREW2

1Department of Psychology, Vanderbilt University, Nashville, Tennessee2Vision, Touch, and Hearing Research Center, University of Queensland,

Queensland, Australia

ABSTRACTUsing optical imaging of intrinsic cortical signals, we examined the func-

tional organization of visual cortical areas V1 and V2 of the marmoset (Cal-lithrix jacchus). Previous studies have reported that adult marmosets do nothave ocular dominance columns (ODCs); however, recent studies have calledthis into question. Using optical imaging methods, we examined whetherODCs could be detected in adult marmosets. We found evidence for functionalODCs in some marmosets but not in others. The activation patterns, whenpresent, were relatively weak and appeared as a mosaic of irregular bands orislands. Consistent with studies in other New World monkeys, these datasuggest the presence of ODC variability within the marmoset population.Orientation maps in V1 revealed iso-orientation domains organized in semi-continuous bands oriented orthogonal to the V1/V2 border, a pattern unlikethat in Macaque monkey. The presence of directional preference maps in V1was also suggested. In V2, similar to V2 in Macaque monkeys, stripe-likeregions of orientation selectivity overlay the pale cytochrome oxidase regions ofV2; zones not selective for orientation overlay the cytochrome thin stripes.However, unlike Macaques, we did not observe clear evidence for orientationmaps overlying thick cytochrome oxidase stripes. In sum, our data suggest thatsignificant organizational differences exist between the organization of V1 andV2 in the marmoset and that of Old World primates. Implications for theestablishment of functional ocular dominance columns, the coestablishment ofmultiple featural maps, and cortical magnification factors are discussed.© 2005 Wiley-Liss, Inc.

Key words: ocular dominance columns; orientation; V2 stripes;cortical magnification; New World primate

In the present investigation, we have used optical im-aging methods to study visual cortical organization in themarmoset, Callithrix jacchus, a New World anthropoidwhose lissencephaly is so complete in the occipitoparietalregion that it allows unobstructed viewing of all the visualcortical areas in both dorsal and ventral streams. Themarmoset may have unusual variants of some features ofvisual cortical organization. These variants might providenatural experiments illuminating the functional signifi-cance of these features of functional organization. Forexample, a number of studies report that marmosets lacksegregation of geniculate afferents to layer IV of V1(termed ocular dominance columns, or ODCs) (Spatz,1979; DeBruyn and Casagrande, 1981) and yet have sub-stantive binocular vision and stereopsis, raising puzzling

questions regarding the possible function of ODCs. Closerexamination reveals that marmosets have clear ODC ar-

Grant sponsor: Australian National Health and Medical Re-search Council; Grant sponsor: the National Institutes of Health;Grant sponsor: Whitehall Foundation.

*Correspondence to: Anna Wang Roe, Department of Psychol-ogy, Vanderbilt University, 301 Wilson Hall, 111 Twenty-firstAvenue South, Nashville, TN 37203. Fax: 615-343-8449.E-mail: anna.roe@vanderbilt.edu

Received 14 April 2005; Accepted 15 July 2005DOI 10.1002/ar.a.20248Published online 18 October 2005 in Wiley InterScience(www.interscience.wiley.com).

THE ANATOMICAL RECORD PART A 287A:1213–1225 (2005)

© 2005 WILEY-LISS, INC.

rays at birth, but that these mostly disappear as the youngmarmoset matures and gains visual experience (Spatz,1989). Could this postnatal fusion of ODC arrays in mar-mosets be connected with the fact that marmosets are thedwarfs of New World anthropoids, with small heads andeven smaller pupillary separations and thereby a markedreduction in binocular parallax? Other studies indicatethat ODCs can be found in some adult marmosets (Chap-pert-Piquemal et al., 2001) and that ODCs can be inducedboth in young (Sengpiel et al., 1996) and even in adultanimals (Markstahler et al., 1998), making marmoset vi-sual cortex fertile ground for pursuing issues of corticalfunctional organization and plasticity.

In the mammalian cerebral cortex, each cortical areamust represent multiple sensory parameters. How multi-ple sensory maps are simultaneously represented in asingle two-dimensional sheet has challenged both biolo-gists and modelers (Swindale, 2000). How does the orga-nization of ocular dominance columns or the lack thereofaffect the organization of orientation domains in V1? Iso-orientation domains appear as a regular mosaic and formpinwheels as in Macaque V1 (Blasdel and Salama, 1986;Bonhoeffer and Grinvald, 1993), but in the ferret, whereODCs are more patchy and irregular in appearance, iso-orientation domains are more elongated or stripe-like(Chapman et al., 1996). With respect to direction, thereappears to be no columnar organization for direction in V1or V2 of the Macaque monkey, but in the cat area 18 andferret area 17 directional columns have a consistent rela-tionship to orientation columns (Shmuel and Grinvald,1996; Weliky et al., 1996). It is also unknown how orga-nization of ocular information might affect functional or-ganization in V2, the second visual area, where most cellsare binocularly driven. The three thin, pale, and thickcytochrome oxidase stripes in V2 of Macaque monkey arecharacterized by a predominance of cells that are selectivefor color, contour orientation, and disparity, respectively(Hubel and Livingstone, 1987; Roe and Ts’o, 1995; Ts’o etal., 2001). Whether in area V2 the dark and light cyto-chrome oxidase stripes in marmosets (Rosa et al., 1997;Lyon and Kaas, 2001; Collins et al., 2003) are functionallysimilar to those in the Macaque monkey is also unknown.Using optical imaging methods, we find both similaritiesand differences in functional organization between themarmoset and the Macaque monkey.

MATERIALS AND METHODSSurgical Preparation

Four adult marmosets (Callithrix jacchus) were used forthese experiments. Following an initial anesthetic dose ofketamine hydrochloride (40 mg/kg), animals were trache-otomized and a catheter was implanted in the femoralvein for drug delivery. Anesthesia was maintainedthroughout the experiment by a constant infusion of so-dium thiopental (2 mg/kg/hr) or sufentanil (8 mg/kg/hr).Animals were paralyzed (pancuronium bromide, 100 �g/kg/hr) and respirated; following paralysis, the level ofanesthetic sufficient during surgical procedures wasmaintained. Heart rate was continuously monitored, rec-tal temperature was maintained at 38°, and expired CO2was maintained at 4%. After dilation of the pupils (atro-pine sulfate 1%), eyes were refracted and fitted with ap-propriate contact lens to focus on a tangent screen 28inches in front of the animal. A craniotomy and a du-rotomy, roughly 1 cm in size, were made over a region

overlying visual cortex, exposing a visual cortical areanear the V1/V2 border representing 2–10° eccentricity.

Optical ImagingOptical imaging of intrinsic cortical signals was used to

localize functional compartments within visual cortex.The details of imaging procedures have been describedelsewhere (Grinvald et al., 1986; Ts’o et al., 1990; Roe andTs’o, 1995, 1999) and will only be described briefly here.For increased cortical stabilization during optical record-ing, an optical chamber was cemented over the craniot-omy, filled with lightweight silicone oil, and sealed with acoverglass. The cortical surface was illuminated throughthe chamber window with 630 nm wavelength light pro-vided by optic fiber light guides. Images of reflectancechange (intrinsic hemodynamic signals) corresponding tolocal cortical activity were acquired using an Imager 2001[Optical Imaging, Germantown, NY; for details, see Grin-vald (1988), Bonhoeffer and Grinvald (1995), Ts’o et al.(1990)]. Signal-to-noise ratio was enhanced by trial aver-aging (10–20 trials per stimulus condition), but withoutsynchronization of acquisition to heart rate or respiration.Animals were positioned on a floating bench to minimizemotion artifacts.

Images of the cortical surface were collected duringpresentation of visual stimuli to the eyes. Stimuli weregenerated using STIM (Kaare Christian) controlled by anIBM PC/AT with a Sargent Pepper Number Nine graphicscard and were projected onto a rear projection screen at114 cm using a Panasonic video projector. Sinusoidal lu-minance and chromatic contrast (red/green isoluminant)drifting gratings (2–15°/sec) of different spatial frequen-cies (0.5–2 cycle/°) and orientations (0, 45, 90, 135°) werepresented in a pseudorandom fashion. Blank conditionconsisted of an even-gray screen equal to the averageluminance of the sinusoidal luminance grating condition.A mechanical shutter in front of each eye allowed forindependent stimulation of each eye. For each stimulus,10–20 trials were presented in random order (3-sec dura-tion per stimulus; 10- to 15-sec interstimulus interval).Images were acquired without synchronization to respira-tion and heartbeat.

Images were digitized, collected, and processed. Allframes acquired for each stimulus condition were summedand divided by the sum of blank stimulus trials; thisprocedure maximizes signal-to-noise ratios and minimizeseffects of uneven illumination. Blood vessel artifact was attimes substantial, leading to low signal-to-noise ratios. Tocompare two functional properties (e.g., ocular domi-nance), the sum of images obtained under one stimuluscondition (e.g., left eye) was subtracted from that obtainedunder another (e.g., right eye). For orientation maps, weused a “cocktail blank” reference, constructed by summingthe responses to all four cardinal orientations (Bartfeldand Grinvald, 1992; Bonhoeffer and Grinvald, 1993). Suchcocktail blanks are activated blanks that serve to averageout biological artifacts such as those due to blood vessels(Bartfeld and Grinvald, 1992). Difference images werethen scaled, clipped, smoothed, and displayed on a colormonitor and printed out for further inspection and com-parison.

Image AnalysisTwo types of image analyses were conducted: single-

condition analyses and two-condition subtraction analy-

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ses. Single-condition maps were obtained by subtractingthe blank image from those images obtained from eachgiven stimulus. Single-condition maps indicate the re-sponse magnitude at each location in the image for aparticular stimulus condition. Such blank subtractionsnot only measure change from baseline, but also reduceblood vessel artifact and minimize effects of uneven illu-mination. Dark pixels in single-condition maps indicate aresponse to that stimulus condition greater than that ofthe blank condition image; gray pixels indicate a responsenot different from blank; and lighter pixels could indicatesome level of activation less than that in blank.

Whereas single-condition maps reveal the presence ofresponse to a particular stimulus, stimulus subtractionreveals preference for one stimulus over another. The sumof images obtained for one stimulus condition (e.g., lefteye) is subtracted from that obtained under another (e.g.,right eye). In this case, dark pixels indicate preference forone condition, light pixels a preference for the other con-dition, and gray pixels equal preference for both. Single-condition maps provide the most reliable indication ofstimulus–specific activations, but this may occur at theexpense of signal-to-noise ratio. Difference maps yield bet-ter overall signal quality by accentuating the preferencefor one condition over another, but activations common toboth stimulus conditions are eliminated. In this article,because signal strength in the marmoset visual cortex wasweak in general, subtractions yielded much clearer mapsthan single-condition analysis. The images shown in thearticle are thus all difference maps.

HistologyAt the end of data collection, animals were then deeply

anesthetized with an intravenous dose of sodium pento-barbitol (85 mg/kg) and perfused through the heart with4% paraformaldehyde. Following extraction of the brain,the desired cortical region was removed, flattened, andimmersed in 30% sucrose solution. The cortical tissue wasthen sectioned tangentially at 30 �m and sections werereacted for cytochrome oxidase histochemistry (Wong-Ri-ley, 1979). Cytochrome sections were aligned with opticalimages by aligning imaged surface vasculature patternswith locations and sizes of vascular lumen in superficialsections of cortical tissue.

RESULTSFour adult male marmosets were available and used for

these studies. Because interpretation of the functionalimages were greatly aided by subsequent cytochrome ox-idase histology, we first present our method of tissuealignment with the tissue sections.

Alignment of Images With Cytochrome OxidaseHistology

To align the optical images with the cytochrome-stainedsections, we first aligned the cortical vessel map with acytochrome oxidase section from the superficial layers(200–300 �m depth; Fig. 1A–C). The largest blood vessellumen in cytochrome sections were marked with dots (Fig.2A; dots placed to the right of vessel lumen; red dots in V2,green dots in V1). This dot pattern was then overlaid ontothe vascular image (Fig. 1D) and shifted around until areasonable alignment was obtained between locations ofdots and locations where blood vessels dive into the corti-

cal surface (compare dots in Fig. 2A and B; Fig. 2B, dotsplaced to the right of locations where vessels dive intocortex). Since the cytochrome section is obtained from acortical depth of 300 �m, it is expected that the bloodvessel terminations will have small shifts (� 50 �m) fromthe surface locations. Despite these small shifts, the vesselalignments are quite reliable as only an appropriate align-ment will give a large number of match points. Further-more, because of the density and distribution of matchpoints across the entire imaged region, this method pro-duces an alignment with a degree of precision greaterthan the typical alignment obtained using a small numberof electrolytic lesions. We thus have reasonable confidencein the alignment of functionally and anatomically demar-cated domains and used this method to aide in our inter-pretation of visual activation patterns.

Functional Organization in V1 and V2

Orientation in V1. Optical imaging revealed orienta-tion maps that delineated areas V1 and V2 in the marmo-set. Figure 3A illustrates a map obtained by subtractingthe sum of all horizontal conditions (all left eye horizontaland all right eye horizontal, dark pixels) and the sum of allvertical conditions (all left eye vertical and all right eyevertical, light pixels). Similarly, Figure 2B illustrates thedifference between all acute (all left eye acute and all righteye acute, dark pixels) and oblique (all left eye oblique andall right eye oblique, light pixels) conditions. In area V1,clear interdigitating horizontal and vertical orientationdomains with a periodicity of about 400 �m were observed(Fig. 3A, indicated by red arrows). Obtuse and acute ori-entation domains with a similar spatial periodicity,though less regular, were also obtained (Fig. 3B, indicatedby red arrows). This periodicity is consistent with physi-ological recordings that found that “a 180-deg range oforientations (an orientation hypercolumn) was covered bya block of V1 some 400–800 �m wide” (Sengpiel et al.,1996).

Interestingly, unlike in the macaque monkey or in thecat, horizontal and vertical orientation domains appearedto be organized in an elongated fashion orthogonal to theV1/V2 border (particularly apparent in Fig. 3A), some-what reminiscent of the organization of ocular dominancecolumns in the macaque monkey and quite distinct fromthe more lattice-like organization for orientation found inmacaque monkeys [cf. Ts’o et al. (1990), Blasdel (1992),and Bartfeld and Grinvald (1992); for similar methods inMacaque, compare, e.g., Ramsden et al. (2001), Fig. 4].The apparent orthogonality of iso-orientation columns tothe V1/V2 border has also been described in the ferret(Chapman et al., 1996), the cat (Shmuel and Grinvald,2000), and owl monkey (Xu et al., 2004).

To examine the organization of this map, we generateda color-coded orientation vector map, in which the orien-tation of the strongest response (0, 45, 90, or 135) isindicated by a color. However, in contrast to the standardcolor-coded orientation maps with characteristic pin-wheels [e.g., see same analysis used in Macaque, Ramsdenet al. (2001), Fig. 3, Roe (2003), Fig. 6C], this analysisrevealed no structure at all and appeared relatively uni-form across the image (not shown). Although it is possiblethat this was due to weakness of signal, it may suggestbroad orientation tuning of marmoset visual cortical cellsor, alternatively, a significantly more mixed population oforientation preferences at each pixel location. In another

1215OPTICAL IMAGING OF MARMOSET VISUAL CORTEX

Fig. 1. Cytochrome oxidase section and cortical vascular pattern. A:Low-power image of cytochrome oxidase section taken from about 300�m depth. Scale bar � 1 mm. B: Same as A. V1/V2 border indicated byblack arrows. Region of cytochrome section shown in C indicated by

white box. C: Higher-power view of region indicated in B. V1/V2 borderindicated by downward arrow at top of image. D: Image of corticalvasculature corresponding to C (Fig. 2). Scale bar � 1 mm (C and D).

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study, a pinwheel-like organization was found in the mar-moset V1 (Liu and Pettigrew, 2003), possibly suggestingvariability in functional organization within the species.

Orientation in V2. The location of the V1 orientationmap border colocalizes with the V1/V2 border (Fig. 4D andF) as determined by alignment with the cytochrome oxi-dase sections. Consistent with V2 of other Old World andNew World monkeys, the thin and thick cytochrome oxi-dase stripes alternate in what can be described as a thin/pale/thick/pale cycle (Fig. 4A, alternating black and redarrows). As has been previously described, cytochromeoxidase stripes in the marmoset can be irregular andpatchy in appearance and thin and thick stripes cannotalways be distinguished (Rosa et al., 1997). In this case,the thick stripes appear less distinct and more irregularthan the thin stripes in the cytochrome section.

In contrast to the Macaque monkey, optical imaging oforientation response elicits much weaker activation in V2than in V1 (Fig. 3). It is possible that extrastriate areasare less easily activated in the marmoset and/or that thestimuli used were more effective for activation of V1. Un-

der our recording conditions in response to the limitedspatial frequencies presented, the optical signal in V2 wasroughly 30% the magnitude of the V1 signal. To accentu-ate the V2 signal, we clipped and rescaled the gray valuesof the image shown in Figure 3B and reillustrate thisimage in Figure 4C (because of the rescaling V1 appearsquite saturated).

However weak, this activation did reveal some orienta-tion structure consistent in some ways with what has beendemonstrated in Macaque V2. As shown in Figure 4C,there are narrow regions of either alternating orientationdomains in V2 (indicated by alternating white and blackdots in Fig. 4D). These regions of semiregular alternationappear within presumed pale stripe zones (approximatelocations indicated by white circles at left of Fig. 4C andE). Orientation domains in the central region that overliethe thick stripe appear less distinct. This apparent lack oforientation structure in the thick stripes differs from thatin the Macaque and could be due to a true differencebetween these species. However, further studies need tobe done to explore this issue. The imaged region overlying

Fig. 2. Alignment of cytochrome oxidase section with cortical vas-cular pattern. A: Enlarged view of Figure 1C. Larger blood vessel lumensin section were marked with dots (dots to right of lumen). Not all lumensare marked. Red dots overlie V2 lumen; green dots overlie V1 lumen.Red (V2) and green (V1) boxes help ease of comparison between E andF. B: The dot overlay shown in A was shifted around over surface

vascular image until reasonable alignment was found. Most vessel lu-mens are near locations where surface vessel penetrates cortex (seen asa vessel termination, marked by dots placed to right of terminations).Compare patterns of dots within each of red and green boxes in A andB. Scale bar � 1 mm.

1217OPTICAL IMAGING OF MARMOSET VISUAL CORTEX

the thin stripes (delimited by the red outlines in Fig. 4Dand F) exhibits relatively little structure. This is consis-tent with the demonstrated lack of orientation structurein Macaque thin stripes, characterized by a predominanceof cells that exhibit little preference for orientation (Ts’o etal., 1990; Malach et al., 1994; Roe and Ts’o, 1995, 1999).Thus, the V2 activation pattern in the marmoset is atleast in part consistent with the functional organization ofV2 in the macaque monkey.

Ocular dominance in V1. To examine whether mar-mosets exhibit ocular dominance, we obtained optical im-ages of V1 during monocular right eye and left eye stim-ulation. Ocular dominance maps were generated bysubtracting the sum of all orientation images obtainedthrough one eye from those through the other eye. Sincethese same images produced consistent orientation maps(Fig. 3), they are likely to reflect true stimulus-relatedresponse and not artifact.

Given the variation in reported strength and pattern ofocular dominance domains in marmosets, we expected toobtain clearer maps in some marmosets than others. Wepresent two cases, one with stronger (case 1) and one withweaker (case 2) ocular dominance columns. In both cases,subtraction of summed left and right eye stimulation con-ditions produced images suggestive of some segregation ofocular activation. In case 1 (Fig. 5B; same case as in Fig.6), in which only V1 was in the field of view, the oculardominance map reveals a pattern of irregular alternatinglight and dark bands, roughly 200–400 �m wide (darkregions outlined below in white). In case 2 (Fig. 5A; samecase as in Figs. 3 and 4), eye-specific activation is weak.However, there is some fluctuation of activity that sug-gests eye preference. In the upper part of the image, thereis a hint of a dark band of activation (left eye, outlined inwhite below) adjacent to a lighter band (right eye). In thelower part of this image, potential ocular dominance col-umns (outside of blood vessel artifact region indicated bywhite arrow) are punctuated by irregular dark patches(suggested patches encircled below by white outlines).Area V2, in contrast, appears as relatively even gray withno structure for ocular dominance. The imaged V1 pat-terns in these two cases are reminiscent of the irregularocular dominance columns seen in adult marmosets [cf.Chappert-Piquemal et al. (2001), Fig. 2] or in monocularlydeprived marmosets with stabilized ocular dominance col-umns (Sengpiel et al., 1996). Ocular dominance columnsin marmosets are reported to have an anatomical andphysiological periodicity of roughly 700 �m and often ap-pear in discontinuous patches rather than long continuouscolumns. Consistent with this architecture, the images inFigure 5 suggest a left/right cycle of about 600–700 �m(scale bar � 1 mm). Thus, these data support the view thatat least some adult marmosets have ocular dominancecolumns.

Direction. Previous studies in the ferret and the cathave demonstrated clear organization for direction pref-erence in primary visual cortex (Weliky et al., 1996); how-ever, no tangential organization for directionality hasbeen reported in V1 of macaque monkeys. To examinewhether the marmoset is more similar to carnivores or toOld World primates in this respect, we obtained opticalimages to moving gratings moving in eight different direc-tions (0, 45, 90, 135, 180, 225, 270, 315°). All images were

Fig. 3. Functional organization of orientation in area V1 in the mar-moset. A: HV, horizontal minus vertical orientation image. Dark (light)pixels are those that prefer horizontal (vertical) over vertical (horizontal).B: OB, acute minus oblique orientation image. Dark (light) pixels arethose that prefer acute (obtuse) over obtuse (acute). Analyses: cocktail.Sum of 18 trials. Same field of view as shown in Figure 1D. Red lineindicates V1/V2 border as determined by cytochrome oxidase in Figure1C and 2A.

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Fig. 4. Functional organization of area V2 in the marmoset. A: Cyto-chrome oxidase-stained section. Same as in Figure 1A. Dark stripe in V2are indicated by arrows. Thin stripes (indicated by red arrows) appearmost clearly. Thick stripes (indicated by black arrows) are somewhat lessdistinct. White box indicates region shown in B–F. B: Image of corticalvasculature, same as Figure 1D. C: Imaged V2 stripes. Same image asFigure 3B except analysis was done with different clipping values toaccentuate weaker orientation activation in V2. Locations of cytochromeoxidase stripes (seen in E) are indicated at left by black arrows (thickstripes), red arrows (thin stripes), and circles (pale stripes). D: Same as

C. Cytochromise oxidase thin stripe outlines (red) and V1/V2 border(white) superimposed on image. Note alternating dark and light patches(indicated by black and white dots) within presumed pale stripe zones.The orientation map in center thick stripe zone is less distinct. Thin stripezones are relatively even gray and do not contain structure for orienta-tion. E: Cytochrome oxidase of region within white box in A. Same fieldof view as C. Stripes indicated by arrows and circles at left as in C. F:Same image as E. Outline of thin stripes suggested by red outlines.V1/V2 border indicated by white line. Scale bar � 1 mm (B–F).

1219OPTICAL IMAGING OF MARMOSET VISUAL CORTEX

obtained monocularly. The images shown in Figure 6 areall obtained by appropriate summing of the identical set ofimages used in Figure 5B.

Figure 6A illustrates an orientation map obtained inthis case. Darker regions are sum of activations by 135°(up and to the right, monocular presentation to left eyeand right eye) and 315° (down and to the left, monocularpresentation to left eye and right eye) gratings. Lighterregions are sum of activations by 45° (up and to the left,monocular presentation to left eye and right eyes) and225° (down and to the right, monocular presentation toleft eye and right eyes) gratings. As in Figure 3, notice theelongation of the iso-orientation domains (extendingroughly from lower left to upper right of image).

To examine possible direction-specific activations, weused the same images collected for the orientation maps,but subtracted images obtained during presentation ofmoving gratings in opposing directions. Since the orienta-tion of the stimuli is common to both conditions, anyorientation-specific contribution to the signal should beeliminated in the subtraction. This result is illustrated inFigure 6B. Darker regions are more responsive to 45°gratings (moving up and to the left); light regions are moreresponsive to 225° gratings (moving down and to theright). Due to the small number of trials collected (12trials), this subtracted map is relatively weak. However,its structure appears distinctly different from that of theorientation map, lacking the elongated appearance of theorientation domains in Figure 6A and exhibiting a morepatchy appearance.

To examine qualitatively whether there is any relation-ship between the presumed direction activation zones andthe orientation domains, we circled the darker (45° pre-

ferring) direction domains in red and the lighter (225°preferring) direction domains in blue. When this red/bluepattern is overlaid on the orientation map in Figure 6A, oninspection there is no obvious relationship between thetwo maps, although the periodicities appear similar. Redcircles fall in dark zones, light zones, and on the borders oflight and dark zones of Figure 6A. Similarly, blue circlesfall in dark, light, and intermediate zones of Figure 6A.This is not dissimilar to the qualitative overlays of direc-tion and orientation maps seen in Weliky et al. (1996).

The relationship of directional map to ocular dominanceorganization is shown for comparison in Figure 6C (sameimage as shown in Fig. 5A). Clearly, the periodicity of thismap differs from those of the orientation and directionmaps. As shown by the overlay in Figure 6C (below), thereare putative directional columns of both types in each ofthe left eye and right eye ocular dominance domains (eachof the dark and light ocular dominance domains have bothred and blue circles). In sum, our data are suggestive ofdirectional domains in V1 of the marmoset and suggestpossible organization for direction merits further study inthe marmoset.

Blobs. In the macaque monkey, blobs are reported tohave a high concentration of nonoriented color cells (Liv-ingstone and Hubel, 1984) and typically have either ared-green or blue-yellow preference (Ts’o and Gilbert,1988; Landisman and Ts’o, 2002). In the marmoset, bluecone inputs project to the blobs via the interlaminar layersof the lateral geniculate nucleus (LGN) (Hendry and Yo-shioka, 1994; Martin et al., 1997). Furthermore, there is asex-linked dichotomy for color vision. Whereas both malesand females have blue cones, only females are true

Fig. 5. Possible ocular dominance organizationin V1. A: Case 2 (same case as shown in Figs. 3and 4). Ocular dominance image (left eye minusright eye). V1/V2 border indicated by heavy whiteline (same as shown in Fig. 4F). Part of image iscontaminated by prominent blood vessel artifact(dark vessel indicated by red arrow). Potential lefteye (dark) domains outside region of blood vesselartifact indicated by white outlines below. B: Case1 (same case as shown in Fig. 6). Ocular domi-nance image illustrating irregular banding of lefteye (darker) and right eye (lighter) activation in V1.Same image below with suggested banding out-lined. Periodicity of bands about 600–700 �m. Farright of image is saturated due to curvature of thecortex. Sum of 12 trials. To enhance visualizationof the weak signal, top and bottom quartile of grayvalue distribution was clipped and gray valueswere remapped to 0–255 scale. Sum of 18 trials.Scale bars � 1 mm (A and B).

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trichromats and males are dichromats (lack red-green pig-ment). As all the marmosets we studied were males andthus are presumed dichromats (Yeh et al., 1995), so we didnot expect any red-green vs. blue-yellow activation. In twomarmosets, we used isoluminant red-green and blue-yel-low gratings that have been used in imaging color blobsand stripes in Macaque monkeys (Ts’o et al., 1990; Roeand Ts’o, 1995, 1999). As expected, optical images re-vealed no preferential red-green vs. blue-yellow activa-tion. Neither did we observe any preferential activationwhen luminance was compared with red-green or withblue-yellow activation (cf. Roe and Ts’o, 1995).

Functional architecture. To examine possiblealignment of blob distribution and ocular dominance, weoverlaid the blob map on the ocular dominance map. Atleast in the several potential ocular dominance domains,

there was no obvious relationship. The centers of theocular dominance patches did not overlie the cytochromeblobs; neither did the patch centers fall consistently be-tween blobs. Examination of the relationship betweenblobs and orientation domains also revealed no obviousalignment.

DISCUSSIONOptical Imaging of Marmoset Visual Cortex

Because of the fragile nature of these small animals(weight 400–600 g), marmosets were often difficult tomaintain under anesthesia for long periods of time(Bourne and Rosa, 2003; Schiessl and McLoughlin, 2003).Data collection periods were therefore often limited. As aresult, typically 10–20 trials were collected per condition.Furthermore, due either to species-specific differences in

Fig. 6. Relationship of orientation, direction, and ocular dominance inV1 (same case as Fig. 5B). A: Orientation map: oblique orientationactivation (darker) minus acute orientation activation (lighter). Red andblue circle overlay obtained from directional map in B. B: Directional

preference map: 45° (darker) minus 225° (lighter). For purposes of align-ing with orientation map, directional zones are circled in red (dark, 45°)and blue (light, 225°). C: Ocular dominance map (same as shown in Fig.5A): left eye (darker) minus right eye (lighter) activation. Sum of 12 trials.

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cortical response or to anesthesia-related differences, op-tical signal strength in the marmoset in our hands wasweaker than that in the macaque (Ramsden et al., 2001).The images presented in this article demonstrate clearlydiscernible maps, although the signal-to-noise ratio wouldlikely have been improved with additional trials. Confi-dence in the imaged signal was bolstered by obtainingmultiple types of functional maps from single cortical lo-cations (e.g., Figs. 3–6). Signals due purely to artifact or togeneralized changes in optical response are unlikely toproduce maps that are specifically structured and distinctfrom one another and are likely to be due to stimulus-related responses. In addition, the clear correlation ofthese images with anatomical landmarks revealed in cy-tochrome oxidase makes it even less likely that the im-aged responses are artifactual.

Ocular Dominance Columns in MarmosetsThe presence of ODCs in marmosets has been contro-

versial. As in squirrel monkeys and owl monkeys (Kaas etal., 1976; Hendrickson et al., 1978; Livingstone, 1996;although see Rowe et al., 1978), it was previously believedthat adult marmosets lack anatomical ODCs (Spatz, 1979,1989; DeBruyn and Casagrande, 1981) and that thesecolumns could be stabilized with certain visual experi-ence, such as monocular lid suture, during development[Sengpiel et al. (1996); cf. Livingstone (1996) for similarresult by inducing strabismus in squirrel and owl mon-keys]. Despite the reported lack of ODCs, physiologicalexamination of normal marmoset V1 revealed some weakfluctuation of ocular dominance that extended outsidelayer 4 to layers 2/3 and 5 (Hubel and Wiesel, 1978; Roweet al., 1978; Sengpiel et al., 1996; Livingstone, 1996, forowl monkey and squirrel monkey). However, a recentstudy demonstrated the clear presence of anatomicalODCs in layer 4C of two normal adult marmosets (Chap-pert-Piquemal et al., 2001). Furthermore, functionalODCs can be induced in adult marmosets, but appear onlytransiently: following monocular silencing by intravitrealTTX injections in adult marmosets, ODCs are rapidlyinduced (within 24 hr, as revealed by staining for theimmediate early gene protein zif268), but surprisinglydisappear within 10–20 days (Markstahler et al., 1998; cf.Silveira et al., 1996 in Cebus apella). Thus, ODCs inmarmosets, either those in normal juveniles or induced inadults, do not appear to remain stable. Given the differingreports in adult animals and the apparent influence ofexperience on the appearance and disappearance of ODCsin marmosets, it is likely that there is a significant degreeof variability in the presence of ODCs within the adultmarmoset population. Indeed, this would be consistentwith ODC variability found in other New World monkeys,in which patterns range from strong and distinct, to weakor indistinct, to absent and where periodicity and patternof the columns vary from individual to individual (Adamsand Horton, 2003; cf. Kaas et al., 1976 vs. Rowe et al.,1978; Livingstone, 1996). Such variability could arise fromnormal genetic variation or from individual visual experi-ence during development.

The optical imaging data in this study is consistent withprevious studies. Consistent with hypothesized variabilityin ODC presence within the marmoset population, oculardominance columns were found in some marmosets andnot others (two out of four). In parallel with reported weakphysiological fluctuation (Sengpeil et al., 1996), optical

images exhibited some degree of ocular segregation, al-though weak. The patterns of imaged ODCs are consistentwith the “irregular islands” or “mosaic of irregular col-umns” previously shown and the widths were within therange previously reported: 250–400 �m/column width(Sengpeil et al., 1996; Markstahler et al., 1998; Chappert-Piquemal et al., 2001). These data provide the first imag-ing evidence of ocular dominance columns in New Worldmonkeys and are consistent with the view of ocular dom-inance variability within the marmoset monkey.

Different Cortical Magnification Factors?The periodicity of a single thin/pale/thick/pale stripe

cycle in marmosets is roughly 2 mm (see also Rosa et al.,1997). This is roughly two-thirds the period of that in thesquirrel monkey (Tootell et al., 1983; Malach et al., 1994)and owl monkey (Tootell et al., 1985; Xu et al., 2004), halfthat in the Macaque monkey (Tootell and Hamilton.,1989), and 40–50% that in humans (Horton et al., 1990;Horton, personal communication). Given that the sameamount of visual space is represented in V2, if the corticalmagnification factor of a single stripe cycle (thin/pale/thick/pale cycle) were constant across species, then thereshould be the same number of stripe cycles across speciesdespite differences in total area. However, published fig-ures do not support this. It is estimated that the numberof stripe cycles per dorsal hemisphere in the marmoset is6–8, in the owl monkey 8–10, in the macaque 12–13, andin the human 22–24. While some increase in the size ofstripes could be attributed to factors such as increase inneuropil, glia, and neuron size, the fact that there aremore stripe cycles in larger brains means that each stripecycle represents proportionately less visual space [i.e., thecortical magnification factor increases; cf. Roe and Ts’o(1995)]. The implied changes in magnification factor arenot likely to be due simply to differences in the numbers ofsensory inputs [e.g., in both macaques and humans thereare roughly 1 million retinal ganglion cells (Rakic andRiley, 1983; cf. Windrem and Finlay, 1991)]. These data,therefore, support the theory that increase in cortical size,while due in some part to increased modular size, is at-tributed largely to increase in the number of cortical mod-ules (Rakic, 1988; Purves et al., 1992; Huffman et al.,1999). Thus, if a stripe cycle is thought of as a functionalunit, then in primates with larger cortical area, each unitis devoted to a smaller amount of visual space; in corol-lary, more units are devoted to each degree of visual space(Roe and Ts’o, 1995; Rosa et al., 1997; Lyon et al., 2002;Schiessl and McLaughlin, 2003; Shmuel et al., 2005).

What do increased number of functional units offer?More units may be needed to process additional visualfeatures. Let us consider adding the representation ofanother visual feature, such as color, to the processingunit. The additional circuitry needed for such a represen-tation may exceed the limits of that unit size. That is, therequired increase in the number of neurons would alsohave increasing pressures on the number of synapses andextents of dendrite/axon arbor size. Potential limits onsynaptic number or arbor size may destroy the functionalunity of the module and may in turn lead to an anatomicaland thereby functional fractionation of the module. Whatmay result is a regrouping that then leads to increasednumber of modules. Alternatively, increased module num-ber may be needed to accommodate increased number ofconnections with other cortical loci. Even if there is no

1222 ROE ET AL.

increase in the numbers of features represented, given aconstant number of connections per neuron, an increase inthe number of neurons is accompanied by a disproportion-ately large increase in volume due to maintaining connec-tions (Ringo, 1991). This growth in connectional volumemay itself limit the growth of the functional unit size,thereby leading to the addition of units.

Cortical Architecture: Relationships BetweenRelatively Fixed and Highly Malleable Maps

In the adult macaque, orientation and ocular dominancehave a predictable relationship. That is, orientation sin-gularities tend to fall in the centers of ocular dominancecolumns and iso-orientation domains tend to cross oculardominance borders at right angles (Bartfeld and Grinvald,1992; Blasdel, 1992). The structure of orientation columnsis present from a very early age and appears highly resis-tant to dramatic changes in visual experience and to theconcomitant changes in geniculocortical inputs during al-tered visual experience (Antonini and Stryker, 1993; Kimand Bonhoeffer, 1994; Chapman et al., 1996). In contrast,ocular dominance columns exhibit varying degrees of seg-regation (ranging from sharp segregation, such as thatfollowing strabismus, to lack of segregation altogether,such as in the normal marmoset), varying degrees of biasin contralateral/ipsilateral distribution in layer 4, anddiffering patterns of columnar continuity or patchiness.These differences are not only seen from across speciescomparisons, but also following different visual experienceduring development. Thus, whereas ocular dominance col-umns are malleable and susceptible to visual deprivationparadigms, orientation columns appear much less so.

We consider two possible views of this dichotomy. Oneview suggests that orientation columns are a scaffold onwhich other features, such as ocular dominance columns,hang. In developmental terms, this could mean that spec-ification of orientation occurs before that of ocular speci-fication during development. Precedence for this develop-mental sequence has previously been shown in ferrets(Chapman et al., 1996). Another view is more functional.It is possible that orientation maps appear more constantbecause orientation is a continuous parameter, whereasocular dominance is more bimodal in nature. The compet-itive forces between multiple iso-orientation populationsmay be more computationally constraining than thosebetween two populations of ocular afferents. This differ-ence may then lead to the perceived constancy of orienta-tion maps.

The question remains as to how orientation and oculardominance maps may be established independent of oneanother. A key difference between these two featural do-mains is that ocularity is determined by individual genic-ulate afferents arising from either left eye layers or righteye layers in the geniculate. Orientation selectivity, how-ever, is not only determined by appropriate convergence ofgeniculate afferents (Hubel and Wiesel, 1977; Chapman etal., 1991; Ferster et al., 1996) but also highly influenced byintracortical mechanisms (Sillito, 1975; Fregnac et al.,1988; Greuel et al., 1988). Thus, during the period ofocular dominance plasticity when individual geniculocor-tical arbors are being remodeled, they must as a popula-tion still seek to maintain continuity of orientation repre-sentation and minimize total number of singularities orfractures. This constraint for continuity must be strongerthan the need to maintain a constant relationship with

overall ocular dominance pattern. Alternatively, as sug-gested by one recent study (Adams and Horton, 2003), thepresence or pattern of ocular dominance may be morestrongly determined by genetic constraints than by expe-rience or other functional constraints. In this case, onewould not expect to find a consistent relationship withorientation maps.

Whether cytochrome oxidase blobs are a fixed architec-tural feature of visual cortex is also a question. Blob pat-terns are present even after early binocular enucleationduring development (Kuljis and Rakic, 1990) and remainrelatively constant in number throughout development(Purves and LaMantia, 1993). As observed in other NewWorld monkeys, no consistent relationship between iden-tified ocular dominance domains and cytochrome oxidaseblobs was discerned in these data. Whether alignmentbetween ocular dominance and blobs is present in juvenilemarmosets is unknown. In normal macaque monkeys, cy-tochrome oxidase blobs are centers of high monocularityand align along the centers of ocular dominance columns(Ts’o et al., 1990). Following monocular enucleation ormonocular deprivation, blobs of the deprived eye shrink insize but retain their position along ocular dominance col-umn centers (Horton, 1984). However, disruption of thealignment has been demonstrated following anisome-tropic amblyopia induced with lens rearing (Roe et al.,1995) and following reduction of parvocellular geniculateinputs as a result of fetal X-irradiation (Roe et al., 1999).Thus, the blob/ocular dominance association is not a fixedarchitectural feature of primate visual cortex (Horton andHocking, 1996). Although this issue needs further inves-tigation, we suggest, given the relative persistence of blobpatterns across primate species and with different visualexperience paradigms, that any change in blob/oculardominance relationship is again primarily due to oculardominance malleability.

ACKNOWLEDGMENTSThe authors thank David Kornack and Jon Kaas for

helpful comments on this manuscript.

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