Roger B. H. Tootell

High-resolution intersubject averaging and a coordinate system for the cortical surface.

The neurons of the human cerebral cortex are arranged in a highly folded sheet, with the majority of the cortical surface area buried in folds. Cortical maps are typically arranged with a topography oriented parallel to the cortical surface. Despite this unambiguous sheetlike geometry, the most commonly used coordinate systems for localizing cortical features are based on 3‐D stereotaxic coordinates rather than on position relative to the 2‐D cortical sheet. In order to address the need for a more natural surface‐based coordinate system for the cortex, we have developed a means for generating an average folding pattern across a large number of individual subjects as a function on the unit sphere and of nonrigidly aligning each individual with the average. This establishes a spherical surface‐based coordinate system that is adapted to the folding pattern of each individual subject, allowing for much higher localization accuracy of structural and functional features of the human brain. Hum. Brain Mapping 8:272–284, 1999.

Mechanisms of migraine aura revealed by functional MRI in human visual cortex

Cortical spreading depression (CSD) has been suggested to underlie migraine visual aura. However, it has been challenging to test this hypothesis in human cerebral cortex. Using high-field functional MRI with near-continuous recording during visual aura in three subjects, we observed blood oxygenation level-dependent (BOLD) signal changes that demonstrated at least eight characteristics of CSD, time-locked to percept/onset of the aura. Initially, a focal increase in BOLD signal (possibly reflecting vasodilation), developed within extrastriate cortex (area V3A). This BOLD change progressed contiguously and slowly (3.5 ± 1.1 mm/min) over occipital cortex, congruent with the retinotopy of the visual percept. Following the same retinotopic progression, the BOLD signal then diminished (possibly reflecting vasoconstriction after the initial vasodilation), as did the BOLD response to visual activation. During periods with no visual stimulation, but while the subject was experiencing scintillations, BOLD signal followed the retinotopic progression of the visual percept. These data strongly suggest that an electrophysiological event such as CSD generates the aura in human visual cortex.

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.

Faces and objects in macaque cerebral cortex

How are different object categories organized by the visual system? Current evidence indicates that monkeys and humans process object categories in fundamentally different ways. Functional magnetic resonance imaging (fMRI) studies suggest that humans have a ventral temporal face area, but such evidence is lacking in macaques. Instead, face-responsive neurons in macaques seem to be scattered throughout temporal cortex, with some relative concentration in the superior temporal sulcus (STS). Here, using fMRI in alert fixating macaque monkeys and humans, we found that macaques do have discrete face-selective patches, similar in relative size and number to face patches in humans. The face patches were embedded within a large swath of object-selective cortex extending from V4 to rostral TE. This large region responded better to pictures of intact objects compared to scrambled objects, with different object categories eliciting different patterns of activity, as in the human. Overall, our results suggest that humans and macaques share a similar brain architecture for visual object processing.

Functional anatomy of macaque striate cortex. II. Retinotopic organization

Macaque monkeys were shown retinotopically-specific visual stimuli during 14C-2-deoxy-d-glucose (DG) infusion in a study of the retinotopic organization of primary visual cortex (V1). In the central half of V1, the cortical magnification was found to be greater along the vertical than along the horizontal meridian, and overall magnification factors appeared to be scaled proportionate to brain size across different species. The cortical magnification factor (CMF) was found to reach a maximum of about 15 mm/deg at the representation of the fovea, at a point of acute curvature in the V1-V2 border. We find neither a duplication nor an overrepresentation of the vertical meridian. The magnification factor did not appear to be doubled in a direction perpendicular to the ocular dominance strips; it may not be increased at all. The DG borders in parvorecipient layer 4Cb were found to be as sharp as 140 micron (half-amplitude, half width), corresponding to a visual angle of less than 2′ of arc at the eccentricity measured. In other layers (including magnorecipient layer 4Ca), the retinotopic borders are broader. The retinotopic spread of activity is greater when produced by a low-spatial-frequency grating than when produced by a high-spatial-frequency grating. Orientation- specific stimuli produced a pattern of activation that spread further than 1 mm across cortex in some layers. Some DG evidence suggests that the spread of functional activity is greater near the foveal representation than near 5 degrees eccentricity.

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 objects 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.

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.

Location of human face‐selective cortex with respect to retinotopic areas

Functional Magnetic Resonance Imaging (fMRI) was used to identify a small area in the human posterior fusiform gyrus that responds selectively to faces (PF). In the same subjects, phase‐encoded rotating and expanding checkerboards were used with fMRI to identify the retinotopic visual areas V1, V2, V3, V3A, VP and V4v. PF was found to lie anterior to area V4v, with a small gap present between them. Further recordings in some of the same subjects used moving low‐contrast rings to identify the visual motion area MT. PF was found to lie ventral to MT. In addition, preliminary evidence was found using fMRI for a small area that responded to inanimate objects but not to faces in the collateral sulcus medial to PF. The retinotopic visual areas and MT responded equally to faces, control randomized stimuli, and objects. Weakly face‐selective responses were also found in ventrolateral occipitotemporal cortex anterior to V4v, as well as in the middle temporal gyrus anterior to MT. We conclude that the fusiform face area in humans lies in non‐retinotopic visual association cortex of the ventral form‐processing stream, in an area that may be roughly homologous in location to area TF or CITv in monkeys. Hum. Brain Mapping 7:29–37, 1999.

Stereopsis activates V3A and caudal intraparietal areas in macaques and humans.

Stereopsis, the perception of depth from small differences between the images in the two eyes, provides a rich model for investigating the cortical construction of surfaces and space. Although disparity-tuned cells have been found in a large number of areas in macaque visual cortex, stereoscopic processing in these areas has never been systematically compared using the same stimuli and analysis methods. In order to examine the global architecture of stereoscopic processing in primate visual cortex, we studied fMRI activity in alert, fixating human and macaque subjects. In macaques, we found strongest activation to near/far compared to zero disparity in areas V3, V3A, and CIPS. In humans, we found strongest activation to the same stimuli in areas V3A, V7, the V4d topolog (V4d-topo), and a caudal parietal disparity region (CPDR). Thus, in both primate species a small cluster of areas at the parieto-occipital junction appears to be specialized for stereopsis.