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Daniel L Adams

Publications and source records attributed to Daniel L Adams.

8 recordsLinked to original sources

Monocular cells without ocular dominance columns.

In many regions of the mammalian cerebral cortex, cells that share a common receptive field property are grouped into columns. Despite intensive study, the function of the cortical column remains unknown. In the squirrel monkey, the expression of ocular dominance columns is variable, with columns present in some animals and not in others. By searching for differences between animals with and without columns, it should be possible to infer how columns contribute to visual processing. Single-cell recordings outside layer 4C were made in nine squirrel monkeys, followed by labeling of ocular dominance columns in layer 4C. In the squirrel monkey, compared with the macaque, cells outside layer 4C were more likely to respond to stimulation of either eye whether ocular dominance columns were present or not. In three animals lacking ocular dominance columns, single cells were recorded from layer 4C. Remarkably, 20% of cells in layer 4C were monocular despite the absence of columns. This observation means that ocular dominance columns are not necessary for monocular cells to occur in striate cortex. In macaques each row of cytochrome oxidase (CO) patches is aligned with an ocular dominance column and receives koniocellular input serving one eye only. In squirrel monkeys this was not true: CO patches and ocular dominance columns had no spatial correlation and the koniocellular input to CO patches was binocular. Thus even when ocular dominance columns occur in the squirrel monkey, they do not transform the functional architecture to resemble that of the macaque.

Animals↗

The cortical column: a structure without a function.

This year, the field of neuroscience celebrates the 50th anniversary of Mountcastle's discovery of the cortical column. In this review, we summarize half a century of research and come to the disappointing realization that the column may have no function. Originally, it was described as a discrete structure, spanning the layers of the somatosensory cortex, which contains cells responsive to only a single modality, such as deep joint receptors or cutaneous receptors. Subsequently, examples of columns have been uncovered in numerous cortical areas, expanding the original concept to embrace a variety of different structures and principles. A "column" now refers to cells in any vertical cluster that share the same tuning for any given receptive field attribute. In striate cortex, for example, cells with the same eye preference are grouped into ocular dominance columns. Unaccountably, ocular dominance columns are present in some species, but not others. In principle, it should be possible to determine their function by searching for species differences in visual performance that correlate with their presence or absence. Unfortunately, this approach has been to no avail; no visual faculty has emerged that appears to require ocular dominance columns. Moreover, recent evidence has shown that the expression of ocular dominance columns can be highly variable among members of the same species, or even in different portions of the visual cortex in the same individual. These observations deal a fatal blow to the idea that ocular dominance columns serve a purpose. More broadly, the term "column" also denotes the periodic termination of anatomical projections within or between cortical areas. In many instances, periodic projections have a consistent relationship with some architectural feature, such as the cytochrome oxidase patches in V1 or the stripes in V2. These tissue compartments appear to divide cells with different receptive field properties into distinct processing streams. However, it is unclear what advantage, if any, is conveyed by this form of columnar segregation. Although the column is an attractive concept, it has failed as a unifying principle for understanding cortical function. Unravelling the organization of the cerebral cortex will require a painstaking description of the circuits, projections and response properties peculiar to cells in each of its various areas.

Brain Mapping↗

The representation of retinal blood vessels in primate striate cortex.

The blood vessels that nourish the inner retina cast shadows on photoreceptors, creating "angioscotomas" in the visual field. We have found the representations of angioscotomas in striate cortex of the squirrel monkey. They were detected in 9 of 12 normal adult animals by staining flatmounts for cytochrome oxidase activity after enucleation of one eye. They appeared as thin profiles in layer 4C radiating from the blind spot representation. Angioscotomas can be regarded as a local form of amblyopia. After birth, when light strikes the retina, photoreceptors beneath blood vessels are denied normal visual stimulation. This deprivation induces remodeling of geniculocortical afferents in a distribution that corresponds to the retinal vascular tree. Angioscotoma representations were most obvious in monkeys with fine ocular dominance columns and were invisible in monkeys with large, well segregated columns. In monkeys without columns, their width corresponded faithfully to the inducing retinal shadow, making it possible to calculate the minimum shadow required to produce a cortical representation. The "amblyogenic threshold" was calculated as the fraction of the pupil area eclipsed to trigger remodeling of geniculocortical afferents. It was found to be constant over retinal eccentricity, vessel size, and shadow size. Ambliogenic shadows only three to four cones wide were sufficient to generate a cortical representation, testifying to the remarkable precision of the cortical map. The representations of retinal blood vessels separated by only 0.65 degrees were resolvable in the cortex, yielding an upper limit on cortical resolution of 340 microm in layer 4C.

Animals↗

A precise retinotopic map of primate striate cortex generated from the representation of angioscotomas.

Shadows cast by retinal blood vessels are represented in striate cortex of the squirrel monkey. Their pattern was exploited to generate a true retinotopic map of V1. For calibration, retinal landmarks were projected onto a tangent screen to measure their visual field location. Next, the retina was warped onto striate cortex, distorting it as necessary to match each retinal vessel to its cortical representation. Maps from four hemispheres of two normal adult squirrel monkeys were created and used to derive expressions for cortical magnification factor (M). A mean map was produced by averaging the individual maps. To address the controversial issue of whether the ratio of retinal ganglion cell (RGC) density to M is constant at all eccentricities, we stained a retinal whole mount from one of the two monkeys for Nissl substance. A ganglion cell density map was compiled by sampling the concentration of cells at 171 retinal points. Allowance was made for displaced amacrine cells and for the centripetal displacement of RGCs from central photoreceptors. After these corrections the V1 surface area and RGC density were compared at each eccentricity. The cortical representation of the macula was found to be amplified, even beyond the magnification expected from its high density of RGCs. For example, the central 4 degrees of visual field were allotted 27% of the surface area of V1 but were supplied by only 12% of RGCs. We conclude that, in monkey striate cortex, more tissue is allocated per ganglion cell for the analysis of information emanating from the macula as compared with the peripheral retina.

Amacrine Cells↗

Shadows cast by retinal blood vessels mapped in primary visual cortex.

The mammalian eye is a remarkable optical device, but its design is not perfect. The blood vessels that supply the inner retina are located in front of the photoreceptor layer, blocking access to light. Their shadows create a pattern of blindness in the field of vision that corresponds precisely to the location of the largest vessels in the eye. We show here that in squirrel monkeys, focal deprivation by blood vessels leads to rewiring of the eye's geniculocortical projections, imprinting an image of the retinal vascular tree onto the primary visual cortex. This process illustrates vividly that local imbalances in neuronal activity can influence column formation during normal development.

Animals↗

Complete flatmounting of the macaque cerebral cortex.

The elaborate folding of the brain surface has posed a practical impediment to investigators engaged in mapping the areas of the cerebral cortex. This obstacle has been overcome partially by the development of methods to erase the sulci and gyri by physically flattening the cortex prior to sectioning. In this study, we have prepared a step-by-step atlas of the flatmounting process for the entire cerebral cortex in the macaque monkey. The cortex was dissected from the white matter, unfolded, and flattened in a single piece of tissue by making three relieving cuts. The flatmount was sectioned at 60-75 microm and processed for cytochrome oxidase (CO) or myelin. From animal to animal there was nearly a twofold variation in the surface area of individual cortical regions, and of the whole cortex. In each specimen, a close correlation was found between V1 surface area (mean = 1343 mm2), V2 surface area (mean = 1012 mm2), hippocampal area (mean = 181 mm2), and total cerebral cortex area (mean = 10,430 mm2). The complete pattern of CO stripes in area V2 was labeled clearly in several cases; the number of cycles of thick-pale-thin-pale stripes ranged from 26 to 34. Characteristic patterns of strong CO activity were encountered in areas V3, MT, auditory and somatosensory cortex. In some animals we made injections of a retrograde tracer, gold-conjugated cholera toxin B subunit, into area V2 to identify all sources of cortical input. In addition to previously described inputs, we identified three new regions in the occipitotemporal region that project to V2. Flatmounting the cerebral cortex is a simple, efficient method that can be used routinely for mapping areas and connections in the macaque brain, the most widely used primate model of the human brain.

Animals↗

Ocular dominance columns in strabismus.

During development, the projection from the lateral geniculate nucleus to striate cortex becomes segregated into monocular regions called ocular dominance columns. Prior studies in cats have suggested that experimental strabismus or alternating monocular occlusion increases the width and segregation of columns. In the squirrel monkey, strabismus has been reported to induce the formation of ocular dominance columns. However, these studies are difficult to interpret because no animal can serve as its own control and the degree of inter-individual variability among normal subjects is considerable. We have re-examined the effect of strabismus on ocular dominance columns in a large group of strabismic and normal squirrel monkeys. Five animals rendered strabismic at age one week had well-developed, widely spaced columns. Among 16 control animals, a wide spectrum of column morphology was encountered. Some control animals lacked ocular dominance columns, whereas others had columns similar to those observed in strabismic animals. Natural variation in column expression in normal squirrel monkeys, and potential uncontrolled genetic influences, made it impossible to determine if strabismus affects ocular dominance columns. It was evident however, that strabismus does not affect the binocular projection from the lateral geniculate nucleus to each CO patch in the upper layers. In strabismic monkeys, just as in normal animals, each patch received input from geniculate afferents serving both the left eye and the right eye. In addition, in strabismic monkeys, as in normal animals, patches were not aligned with ocular dominance columns.

Animals↗