The dominant feature of the functional organization of the primary visual cortex is the visuotopic organization of its cells: the visual field is systematically represented across the surface of the cortex (Figure 25–11A).
Functional architecture of the primary visual cortex.
(Images from M. Kinoshita and A. Das, reproduced with permission.)
A. The surface of the primary visual cortex is functionally organized in a map of the visual field. The elevations and azimuths of visual space are organized in a regular grid that is distorted because of variation in the magnification factor (see Figure 25–10). The grid is visible here in the dark stripes (visualized with intrinsic-signal optical imaging), which reflect the pattern of neurons that responded to a series of vertical candy stripes. Within this surface map one finds repeated superimposed cycles of functionally specific columns of cells, as illustrated in B, C, and D.
B. The dark and light stripes represent the surface view of the left and right ocular dominance columns. These stripes intersect the border between areas V1 and V2, the representation of the vertical meridian, at right angles.
C. Some columns contain cells with similar selectivity for the orientation of stimuli. The different colors indicate the orientation preference of the columns. The orientation columns in surface view are best described as pinwheels surrounding singularities of sudden changes in orientation (the center of the pinwheel). The scale bar represents 1 mm. (Surface image of orientation columns on the left reproduced, with permission, from G. Blasdel.)
D. Patterns of blobs in V1 and stripes in V2 represent other modules of functional organization. These patterns are visualized with cytochrome oxidase.
In addition, cells in the primary visual cortex with similar functional properties are located close together in columns that extend from the cortical surface to the white matter. The columns are concerned with the functional properties that are analyzed in any given cortical area and thus reflect the functional role of that area in vision. The properties that are developed in the primary visual cortex include orientation specificity and the integration of inputs from the two eyes, which is measured as the relative strength of input from each eye, or ocular dominance.
Ocular-dominance columns reflect the segregation of thalamocortical inputs arriving from different layers of the lateral geniculate nucleus. Alternating layers of this nucleus receive input from retinal ganglion cells located in either the ipsilateral or contralateral retina (Figure 25–12). This segregation is maintained in the inputs from the lateral geniculate nucleus to the primary visual cortex, producing the alternating left-eye and right-eye ocular dominance bands (Figure 25–11B), which receive input from the respective layers of the lateral geniculate nucleus.
Projections from the lateral geniculate nucleus to the visual cortex.
The lateral geniculate nucleus in each hemisphere receives input from the temporal retina of the ipsilateral eye and the nasal retina of the contralateral eye. The nucleus is a laminated structure comprising four parvocellular layers (layers 3 to 6) and two magnocellular layers (layers 1 and 2). The inputs from the two eyes terminate in different layers: The contralateral eye projects to layers 1, 4, and 6, whereas the ipsilateral eye sends input to layers 2, 3, and 5. The parvocellular and magnocellular inputs to the primary visual cortex arrive in separate sublayers. The parvocellular layers project to layer IVCβ and the magnocellular layers to layer IVCα. In addition, the afferents from the ipsilateral and contralateral layers of the lateral geniculate nucleus are segregated into alternating ocular-dominance columns.
Cells with similar orientation preferences are also grouped into columns. Across the cortical surface there is a regular clockwise and counterclockwise cycling of orientation preference with the full 180° cycle repeating every 750 μm (Figure 25–11C). One full cycle of orientation columns is called a hypercolumn. Likewise, the left- and right-eye dominance columns alternate with a periodicity of 750 to 1,000 μm. The orientation and ocular dominance columns are crisscrossed over the cortical surface.
Both types of columns were first mapped by recording the responses of neurons at closely spaced electrode penetrations in the cortex. The ocular-dominance columns were also identified by making lesions or tracer injections in individual layers of the lateral geniculate nucleus. More recently a technique known as optical imaging has enabled researchers to visualize a surface representation of the orientation and ocular dominance columns in living animals. Developed for studies of cortical organization by Amiram Grinvald, this technique visualizes changes in surface reflectance associated with the metabolic requirements of active groups of neurons, known as intrinsic-signal optical imaging, or changes in fluorescence of voltage-sensitive dyes. Intrinsic-signal imaging depends on activity-associated changes in local blood flow and alterations in the oxidative state of hemoglobin and other intrinsic chromophores.
An experimenter can visualize the distribution of cells with left or right ocular dominance, for example, by subtracting the image obtained while stimulating one eye from that acquired while stimulating the other. When viewed in a plane tangential to the cortical surface, the ocular dominance columns appear as alternating left- and right-eye stripes, each approximately 750 μm in width (Figure 25–11B).
The cycles of orientation columns form various structures, from parallel stripes to pinwheels. Sharp jumps in orientation preference occur at the pinwheel centers and "fractures" in the orientation map (Figure 25–11C). Superimposed on these is a third columnar system of continuously changing directional preference.
Embedded within the orientation and ocular-dominance columns are clusters of neurons that have poor orientation selectivity but strong color preferences. These units of specialization, located within the superficial layers, were revealed by a histochemical label for the enzyme cytochrome oxidase, which is distributed in a regular patchy pattern of blobs and interblobs. In the primary visual cortex these blobs are a few hundred micrometers in diameter and 750 μm apart (Figure 25–11D). The blobs correspond to clusters of color-selective neurons. Because they are rich in cells with color selectivity and poor in cells with orientation selectivity, the blobs are specialized to provide information about surfaces rather than edges.
In area V2 thick and thin dark stripes separated by pale stripes are evident with cytochrome oxidase labeling (Figure 25–11D). The thick stripes contain neurons selective for direction of movement and for binocular disparity as well as cells that are responsive to illusory contours and global disparity cues. The thin stripes hold cells specialized for color. The pale stripes contain orientation-selective neurons.
For every visual attribute to be analyzed at each position in the visual field there must be adequate tiling, or coverage, of neurons with different functional properties. As one moves in any direction across the cortical surface, the progression of the visuotopic location of receptive fields is gradual, whereas the cycling of columns occurs more rapidly. Any given position in space can therefore be analyzed adequately in terms of the orientation of contours, the color and direction of movement of objects, and the stereoscopic depth. The small segment of visual cortex that deals with that particular part of the visual field represents all possible values of all the columnar systems (Figure 25–13).
A cortical computational module.
A chunk of cortical tissue roughly 1 mm in diameter contains an orientation hypercolumn (a full cycle of orientation columns), one cycle of left- and right-eye ocular-dominance columns, and blobs and interblobs. This module would presumably contain all of the functional and anatomical cell types of primary visual cortex, and would be repeated hundreds of times to cover the visual field. (Adapted, with permission, from Hubel 1988.)
The columnar systems serve as the substrate for two fundamental types of connectivity along the visual pathway. Serial processing occurs in the successive connections between cortical areas, connections that run from the back of the brain forward. At the same time parallel processing occurs simultaneously in subsets of fibers that process different submodalities such as form, color, and movement.
Many areas of visual cortex reflect this arrangement; for example, functionally specific cells in V1 communicate with cells of the same specificity in V2. These pathways are not absolutely segregated, however, for there is some mixing of information between different visual attributes (Figure 25–14).
Parallel processing in visual pathways.
The ventral stream is primarily concerned with object identification, carrying information about form and color. The dorsal pathway is dedicated to visually guided movement, with cells selective for direction of movement. These pathways are not strictly segregated, however, and there is substantial interconnection between them even in the primary visual cortex. (LGN, lateral geniculate nucleus; MT, middle temporal area.) (Retinal ganglion cell images from Dennis Dacey, reproduced with permission.)
Columnar organization confers several advantages. It minimizes the distance required for neurons with similar functional properties to communicate with one another and allows them to share inputs from discrete pathways that convey information about particular sensory attributes. This efficient connectivity economizes on the use of brain volume and maximizes processing speed. The clustering of neurons into functional groups, as in the columns of the cortex, allows the brain to minimize the number of neurons required for analyzing different attributes. If all neurons were tuned for every attribute, the resultant combinatorial explosion would require a prohibitive number of neurons.