Anatomical demonstration of orientation columns in macaque monkey

Abstract

In the macaque monkey striate (primary visual) cortex, the grouping of cells into ocular dominance and orientation columns leads to the prediction of highly specific spatial patterns of cellular activity in response to stimulation by lines through one or both eyes. In t h e present paper these patterns have been examined by the 2-deoxyglucose autoradiographic method developed by Sokoloff and his group (Kennedy e t al, '76). An anesthetized monkey was given a n injection of I4C 2-deoxyglucose and then visually stimulated for 45 minutes with a large array of moving vertical stripes, with both eyes open. The 14C autoradiographs of striate cortex showed vertical bands of label extending through the full cortical thickness. Layer I was a t most only lightly labelled, and layers IV b and VI were t h e most dense. Layer IV c (the site of terminations of most geniculate afferents) was labelled uniformly along its length, a s expected from the lack of orientation specificity of units recorded in t h a t layer. In the other layers the pattern seen in tangential sections was complex, consisting of swirling stripes with many bifurcations and blind endings, but with occasional more regular regions where t h e stripes were roughly parallel. Interstripe distance was rather constant, a t 570 pm. Ocular dominance columns were examined in this same monkey, in t h e same region, by injecting one eye with H-proline two weeks before t h e deoxyglucose experiment, and preparing a second set of autoradiographs of the sections after prolonged washing to remove the 14C-deoxyglucose. As seen in tangential sections through layer IV c, these columns had the usual stripe-like form, with a period of 770 p m , but were simpler in their pattern than the orientation stripes, with fewer bifurcations and less swirling. A comparison of the two sets of columns in t h e same area showed many intersections, but no strict or consistent relationships: angles of intersection showed a distribution t h a t was not obviously different from t h a t expected for any two randomly superimposed sets of lines.Another monkey was stimulated with vertical stripes, but with only one eye open. Deoxyglucose autoradiographs of tangential sections showed regular uniform rows of label in layer IV c, with all t h e characteristic features of eye dominance columns. In the layers above and below IV c the rows in tangential view were broken up into regularly spaced patches of label, presumably representing aggregations of cells responsive to vertically oriented stimuli. The patches showed no consistent alignment across the ocular dominance rows, and indeed no such tendency would be expected, considering t h e complexity of the orientation columns. This pattern of labelling is again predicted from and confirms t h e previous physiological studies.Two functions of t h e primary visual cortex ganized in such a way t h a t cells after t h e iniof higher mammals have now been established tial stage respond best to specifically oriented (Hubel and Wiesel, '62, '68). The inf...

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

“…Some have attributed the visual phenomena to primary visual cortex (32,33), because the visual image is oriented and highly retinotopic, and striate cortex is also retinotopic and selective for oriented stimuli (34)(35)(36)(37). However, human occipital cortex is comprised of multiple cortical areas, many of which (like V1) are also retinotopic (24)(25)(26)(37)(38)(39) and orientation-selective (e.g., ref.…”

Orientation Selectivity without Orientation Maps in Visual Cortex of a Highly Visual Mammal

“…The probability we would miss Ͼ33% of square patches with 253 m sides is 3.5e-6, and the probability we would miss Ͼ50% of square patches with 291 m sides is 0.044. Because the width of a hypercolumn is ϳ550 m in tree shrew (Humphrey and Norton, 1980;Bosking et al, 1997), 570 m in monkey (Hubel et al, 1978), and 800 -1200 m in cat (Löwel et al, 1988), it is highly likely we would have observed evidence of structures of similar size in difference images from squirrel V1 if these structures existed.…”

“…Species and references are as follows: mouse, Mus sp. (Dräger, 1975;Prusky et al, 2000;Schuett et al, 2002); hooded rat, Rattus norvegicus (Espinoza and Thomas, 1983;Girman et al, 1999;Keller et al, 2000); mink, Mustela vision (Dustone et al, 1978;McConnell and LeVay, 1986;LeVay et al, 1987); tree shrew, Tupaia glis (Kaas et al, 1972;Petry et al, 1984;Bosking et al, 1997); squirrel, Sciurus carolinensis (Hall et al, 1971;Jacobs et al, 1982); ferret, Mustela furo (Law et al, 1988;Rao et al, 1997), cat, Felis domesticus (Hubel and Wiesel, 1963;Blake et al, 1974;LeVay and Gilbert, 1976;Tusa et al, 1978), marmoset, Callithrix jacchus (Fritsches and Rosa, 1996;Liu and Pettigrew, 2003); owl monkey, Aotus trivirgatus (Allman and Kaas, 1971;Jacobs, 1977;Sereno et al, 1995); macaque monkey, Macaca mulatta (Hubel et al, 1978;Tootell et al, 1982;Sereno et al, 1995 the location of the cell within the orientation map. Although spike output of all cells was highly tuned, cells in smoothly varying regions (iso-orientation domains) received highly orientation-tuned input, but cells near singularities (pinwheel centers) received broadly tuned input.…”

“…This organization has been described in many cortical areas, including visual, auditory, somatosensory, and prefrontal cortex (Mountcastle, 1997), and is thought to be important for information processing by facilitating connections among neurons with similar properties (BenYishai et al, 1995;Somers et al, 1995). In primary visual cortex (V1), neurons respond preferentially to images of bars or edges of a particular orientation, and, in V1 of primates (Hubel et al, 1978;Blasdel and Salama, 1986), carnivores (Hubel and Wiesel, 1963;Grinvald et al, 1986;McConnell and LeVay, 1986), ungulates (Clarke et al, 1976), and tree shrews (Humphrey and Norton, 1980;Bosking et al, 1997), these orientation-selective cells are arranged in a semiregular, smoothly varying map with local discontinuities. Curiously, whereas electrophysiological and imaging studies of many rodents, including mice (Metin et al, 1988;Schuett et a., 2002), rats (Girman et al, 1999), hamsters (Tiao and Blakemore, 1976), and a lagomorph, the rabbit (Murphy and Berman, 1979), have identified orientation-selective neurons in these species, no orderly orientation map has been found.…”

Localization of Functional Activity in the Central Nervous System by Measurement of Glucose Utilization with Radioactive Deoxyglucose

“…5C) (Kennedy et aI., 1976). It has been used by Hubel et al (1978) to do the same for the orientation columns in the striate cortex of the monkey. A byproduct of the studies of the ocu lar dominance columns was the identification of the loci of the visual cortical representation of the blind spots of the visual fields (Fig.…”