Spatial frequency columns in primary visual cortex.

Using the activity-dependent 2-[14C]deoxy-D-glucose technique, we have demonstrated a columnar organization of spatial frequency--specific sensitivity in striate cortex. Cats viewing patterns containing a single spatial frequency presented at all orientations show columns of increased deoxyglucose uptake extending through all cortical layers. A control stimulus containing all spatial frequencies presented at all orientations produces no columnar density differences within the striate cortex.

Deoxyglucose analysis of retinotopic organization in primate striate cortex.

We have anatomically analyzed retinotopic organization using the 14C-labeled 2-deoxy-D-glucose method. The method has several advantages over conventional electrophysiological mapping techniques. In the striate cortex, the anatomical substrate for retinotopic organization is surprisingly well ordered, and there seems to be a systematic relationship between ocular dominance strips and cortical magnification. The 2-deoxyglucose maps in this area appear to be largely uninfluenced by known differences in long-term metabolic activity. This method should prove useful in analyzing retinotopic organization in various visual areas of the brain and in different species.

Functional organization of the second cortical visual area in primates.

The functional organization of the second cortical visual area was examined with three different anatomical markers: 2-[14C]deoxy-D-glucose, cytochrome oxidase, and various myelin stains. All three markers revealed strips running throughout the area, parallel to the cortical surface. The boundaries of these strips provide an anatomical criterion for defining the borders of this extrastriate region. Further, the demonstration of these strips allows a functional and anatomical analysis of modules in the area, just as the recent demonstration of spots in the primary visual cortex has allowed an analysis of modules there. The strips differ structurally and functionally from interstrip regions and these differences are similar to those seen between the spots and the interspot regions in the primary visual cortex. In the macaque the strips and spots differ with regard to binocular organization.

Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging.

The borders of human visual areas V1, V2, VP, V3, and V4 were precisely and noninvasively determined. Functional magnetic resonance images were recorded during phase-encoded retinal stimulation. This volume data set was then sampled with a cortical surface reconstruction, making it possible to calculate the local visual field sign (mirror image versus non-mirror image representation). This method automatically and objectively outlines area borders because adjacent areas often have the opposite field sign. Cortical magnification factor curves for striate and extrastriate cortical areas were determined, which showed that human visual areas have a greater emphasis on the center-of-gaze than their counterparts in monkeys. Retinotopically organized visual areas in humans extend anteriorly to overlap several areas previously shown to be activated by written words.

The retinotopy of visual spatial attention.

We used high-field (3T) functional magnetic resonance imaging (fMRI) to label cortical activity due to visual spatial attention, relative to flattened cortical maps of the retinotopy and visual areas from the same human subjects. In the main task, the visual stimulus remained constant, but covert visual spatial attention was varied in both location and load. In each of the extrastriate retinotopic areas, we found MR increases at the representations of the attended target. Similar but smaller increases were found in V1. Decreased MR levels were found in the same cortical locations when attention was directed at retinotopically different locations. In and surrounding area MT+, MR increases were lateralized but not otherwise retinotopic. At the representation of eccentricities central to that of the attended targets, prominent MR decreases occurred during spatial attention.

Cortical mechanisms specific to explicit visual object recognition.

The cortical mechanisms associated with conscious object recognition were studied using functional magnetic resonance imaging (fMRI). Participants were required to recognize pictures of masked objects that were presented very briefly, randomly and repeatedly. This design yielded a gradual accomplishment of successful recognition. Cortical activity in a ventrotemporal visual region was linearly correlated with perception of object identity. Therefore, although object recognition is rapid, awareness of an object's identity is not a discrete phenomenon but rather associated with gradually increasing cortical activity. Furthermore, the focus of the activity in the temporal cortex shifted anteriorly as subjects reported an increased knowledge regarding identity. The results presented here provide new insights into the processes underlying explicit object recognition, as well as the analysis that takes place immediately before and after recognition is possible.

Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys.

To reduce the information gap between human neuroimaging and macaque physiology and anatomy, we mapped fMRI signals produced by moving and stationary stimuli (random dots or lines) in fixating monkeys. Functional sensitivity was increased by a factor of approximately 5 relative to the BOLD technique by injecting a contrast agent (monocrystalline iron oxide nanoparticle [MION]). Areas identified as motion sensitive included V2, V3, MT/V5, vMST, FST, VIP, and FEF (with moving dots), as well as V4, TE, LIP, and PIP (with random lines). These regions sensitive for moving dots are largely in agreement with monkey single unit data and (except for V3A) with human fMRI results. Moving lines activate some regions that have not been previously implicated in motion processing. Overall, the results clarify the relationship between the motion pathway and the dorsal stream in primates.

Retinotopy and color sensitivity in human visual cortical area V8.

Prior studies suggest the presence of a color-selective area in the inferior occipital-temporal region of human visual cortex. It has been proposed that this human area is homologous to macaque area V4, which is arguably color selective, but this has never been tested directly. To test this model, we compared the location of the human color-selective region to the retinotopic area boundaries in the same subjects, using functional magnetic resonance imaging (fMRI), cortical flattening and retinotopic mapping techniques. The human color-selective region did not match the location of area V4 (neither its dorsal nor ventral subdivisions), as extrapolated from macaque maps. Instead this region coincides with a new retinotopic area that we call 'V8', which includes a distinct representation of the fovea and both upper and lower visual fields. We also tested the response to stimuli that produce color afterimages and found that these stimuli, like real colors, caused preferential activation of V8 but not V4.

New images from human visual cortex.

Recent developments in imaging and histology have greatly clarified our understanding of the nature and organization of human visual cortex. More than ten human cortical visual areas can now be differentiated, compared with the approximately 30 areas described in macaque monkeys. Most human areas and columns described so far appear quite similar to those in macaque but distinctive species differences also exist. Imaging studies suggest two general information-processing streams (parietal and temporal) in human visual cortex, as proposed in macaque. Several human areas are both motion- and direction-selective, and a progression of motion-processing steps can be-inferred from the imaging data. Human visual areas for recognizing form are less well defined but the evidence again suggests a progression of information-processing steps and areas, beginning posterior to the human middle temporal area (or V5), and extending inferiorly then anteriorly. This is consistent with findings from macaque, and with human clinical reports.

The representation of illusory and real contours in human cortical visual areas revealed by functional magnetic resonance imaging.

Illusory contours (perceived edges that exist in the absence of local stimulus borders) demonstrate that perception is an active process, creating features not present in the light patterns striking the retina. Illusory contours are thought to be processed using mechanisms that partially overlap with those of "real" contours, but questions about the neural substrate of these percepts remain. Here, we employed functional magnetic resonance imaging to obtain physiological signals from human visual cortex while subjects viewed different types of contours, both real and illusory. We sampled these signals independently from nine visual areas, each defined by retinotopic or other independent criteria. Using both within- and across-subject analysis, we found evidence for overlapping sites of processing; most areas responded to most types of contours. However, there were distinctive differences in the strength of activity across areas and contour types. Two types of illusory contours differed in the strength of activation of the retinotopic areas, but both types activated crudely retinotopic visual areas, including V3A, V4v, V7, and V8, bilaterally. The extent of activation was largely invariant across a range of stimulus sizes that produce illusory contours perceptually, but it was related to the spatial frequency of displaced-grating stimuli. Finally, there was a striking similarity in the pattern of results for the illusory contour-defined shape and a similar shape defined by stereoscopic depth. These and other results suggest a role in surface perception for this lateral occipital region that includes V3A, V4v, V7, and V8.

From retinotopy to recognition: fMRI in human visual cortex.

Recent advances in functional magnetic resonance imaging (fMRI) have furnished increasingly informative and accurate maps of the retinotopy and functional organization in human visual cortex. Here we review how information in those sensory-based maps is topographically related to, and influenced by, more cognitive visuo-spatial dimensions, such as mental imagery, spatial attention, repetition effects and size perception.

Rod photoreceptors and scotopic vision in ground aquirrels.

Ground squirrel retinas contain a relatively small complement of rods (5--10% of all photoreceptors) which are thought to provide the basis for a weak scotopic visual capacity. In a previous investigation of the California ground squirrel (Spermophilus beecheyi) involving the recording of a retinal gross potential, the electroretinogram (ERG), electrophysiological evidence for a viable scotopic signal could be obtained from some, but not all of the ground squirrels examined. To further pursue the possibility that there is a structural/functional discrepancy in the relationship between rod photoreceptors and scotopic vision in the ground squirrel, several experiments involving electrophysiological, behavioral, and anatomical observations have been conducted. We found that although about one-third of the ERGs recorded from a large sample of California ground squirrels lack those characteristics which would indicate the presence of a viable scotopic signal, the retinas of all the squirrels appear to contain the same small population of rod photoreceptors. Additional experiments on the golden-mantled ground squirrel (Spermophilus lateralis), including behavioral as well as ERG measurements and anatomical observations, lead to this same conclusion.

Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT.

We have used optical imaging based on intrinsic signals to explore the functional architecture of owl monkey area MT, a cortical region thought to be involved primarily in visual motion processing. As predicted by previous single-unit reports, we found cortical maps specific for the direction of moving visual stimuli. However, these direction maps were not distributed uniformly across all of area MT. Within the direction-specific regions, the activation produced by stimuli moving in opposite directions overlapped significantly. We also found that stimuli of differing shapes, moving in the same direction, activated different cortical regions within area MT, indicating that direction of motion is not the only parameter according to which area MT of owl monkey is organized. Indeed, we found clear evidence for a robust organization for orientation in area MT. Across all of MT, orientation preference changes smoothly, except at isolated line- or point-shaped discontinuities. Generally, paired regions of opposing direction preference were encompassed within a single orientation domain. The degree of segregation in the orientation maps was 3-5 times that found in direction maps. These results suggest that area MT, like V1 and V2, has a rich and multidimensional functional organization, and that orientation, a shape variable, is one of these dimensions.

Magnetic resonance imaging mapping of brain function. Human visual cortex.

Magnetic resonance imaging (MRI) studies of human brain activity are described. Task-induced changes in brain cognitive state were measured using high-speed MRI techniques sensitive to changes in cerebral blood volume (CBV), blood flow (CBF), and blood oxygenation. These techniques were used to generate the first functional MRI maps of human task activation, by using a visual stimulus paradigm. The methodology of MRI brain mapping and results from the investigation of the functional organization and frequency response of human primary visual cortex (V1) are presented.

Modified technique for cytochrome oxidase histochemistry: increased staining intensity and compatibility with 2-deoxyglucose autoradiography.

Staining the brain for cytochrome oxidase (CO) produces patterns which can resemble the patterns produced by 2-deoxyglucose (2-DG) autoradiography. In order to assess the differences between CO patterns of long-term metabolic activity and 2-DG patterns of short-term activity, comparisons should, ideally, be made on the same section. Consequently, we have made certain modifications in the standard CO histologic procedure which improve the stain and allow both 2-DG autoradiography and CO staining on the same section.

Two methods for flat-mounting cortical tissue.

Two procedures are described which allow cortical grey matter to be unfolded and flattened. Tangential sections of the flat-mounted tissue can reveal clear histological views of horizontal variations in cortical structure and function; these anatomical variations would be hard to see in sections cut by conventional techniques. Examples are presented from non-human primate tissue, but the technique has also been used successfully in a number of other mammalian species, including man. Advantages and disadvantages of the various methods for extracting topographical patterns from the cortex are discussed.

Picture processing techniques applied to autoradiographic studies of visual cortex.

Picture processing techniques are applied to 2-deoxyglucose autoradiographs of sections from striate cortex and to patterns resulting from staining these sections for cytochrome oxidase. This procedure allows computer identification of deoxyglucose active and inactive regions in the autoradiographs and cytochrome active and inactive regions in the stain patterns. Subsequently, the topographical relationship between these patterns can be quantitatively analyzed by means of overlap and density distribution measures and can be displayed using color enhanced graphics. The processing techniques have been applied in studies of the functional organization of visual cortex in primates. Computer graphic techniques have allowed implementation of split-field presentations of stimuli in deoxyglucose experiments. An application of this split-field technique for presenting multiple-stimuli to distinct parts of the visual field is described and an autoradiograph from a split-field experiment is shown.

Mapping visual cortex in monkeys and humans using surface-based atlases.

We have used surface-based atlases of the cerebral cortex to analyze the functional organization of visual cortex in humans and macaque monkeys. The macaque atlas contains multiple partitioning schemes for visual cortex, including a probabilistic atlas of visual areas derived from a recent architectonic study, plus summary schemes that reflect a combination of physiological and anatomical evidence. The human atlas includes a probabilistic map of eight topographically organized visual areas recently mapped using functional MRI. To facilitate comparisons between species, we used surface-based warping to bring functional and geographic landmarks on the macaque map into register with corresponding landmarks on the human map. The results suggest that extrastriate visual cortex outside the known topographically organized areas is dramatically expanded in human compared to macaque cortex, particularly in the parietal lobe.