Rapid identification of ocular dominance columns in macaques using cytochrome oxidase, Zif268, and dark-field microscopy

2000 ◽  
Vol 17 (4) ◽  
pp. 495-508 ◽  
Author(s):  
JONATHAN C. HORTON ◽  
DAVINA R. HOCKING ◽  
DANIEL L. ADAMS
Keyword(s):  
Cytochrome Oxidase ◽  
Striate Cortex ◽  
Ocular Dominance ◽  
Rapid Identification ◽  
Dark Field ◽  
Easy Method ◽  
Ocular Dominance Columns ◽  
Monocular Enucleation ◽  
Dark Field Illumination ◽  
Abnormal Pattern

Strabismus induces an abnormal pattern of alternating light and dark columns of cytochrome oxidase (CO) activity in macaque striate cortex. This pattern may arise because visual perception is suppressed in one eye to avoid diplopia. To test whether CO activity is reduced in the ocular dominance columns of the suppressed eye, we performed monocular enucleation to co-label the ocular dominance columns with Zif268 immunohistochemistry in seven exotropic adult Macaca fascicularis. This approach was unsuccessful, for two reasons. First, Zif268 yielded inconsistent labelling, that was usually greater in the enucleated eye's ocular dominance columns, but was sometimes greater in the intact eye's columns. Therefore, Zif268 was not a reliable method for identifying the ocular dominance columns serving each eye. Second, in three control animals we found that a brief survival period following monocular enucleation (needed for Zif268 levels to change) was long enough to alter CO staining. For example, a survival time of only 3 h was sufficient to induce CO columns, indicating that the activity of this enzyme fluctuates more rapidly than realized previously. Independent of these findings, we have also discovered that acute monocular enucleation produces a vivid pattern of ocular dominance columns visible in unstained or CO-stained sections under dark-field illumination. The ocular dominance columns of the acutely enucleated eye appear dark. This was verified by labelling the ocular dominance columns with [3H]proline. Dark-field illumination of the cortex after acute monocular enucleation offers a new, easy method for identifying the ocular dominance columns in macaques.

Effect of early monocular enucleation upon ocular dominance columns and cytochrome oxidase activity in monkey and human visual cortex

1998 ◽  
Vol 15 (2) ◽  
pp. 289-303 ◽  
Author(s):  
JONATHAN C. HORTON ◽  
DAVINA R. HOCKING
Keyword(s):  
Cytochrome Oxidase ◽  
Critical Period ◽  
Striate Cortex ◽  
Ocular Dominance ◽  
Animal Experiments ◽  
Occipital Lobe ◽  
Silver Stain ◽  
Ocular Dominance Columns ◽  
Monocular Enucleation ◽  
Suitable Technique

We examined cytochrome oxidase (CO) activity in striate cortex of four macaque monkeys after monocular enucleation at ages 1, 1, 5, and 12 weeks. These animal experiments were performed to guide our interpretation of CO patterns in occipital lobe specimens obtained from two children who died several years after monocular enucleation during infancy for tumor. In the macaques, the ocular dominance columns were labelled by injecting [3H]proline into the remaining eye. After enucleation at age 1 week, ocular dominance columns were eliminated in layer IVcβ, resulting in a uniform pattern of autoradiographic label and CO staining. However, columns could still be seen in wet, unstained sections and with the Liesegang silver stain. Autoradiographs through layers IVcα and IVa showed residual, shrunken columns belonging to the missing eye, indicating that enucleation has less drastic effects in these layers. In the two human cases, enucleation at age 1 week also resulted in uniform CO staining in layer IVc. In the macaque after enucleation at age 5 weeks, ocular dominance columns belonging to the missing eye were severely narrowed, but still occupied 20% of layer IVcβ. CO revealed wide, dark columns alternating with thin, pale columns in layer IVcβ. The CO pattern and the columns labelled by autoradiography matched perfectly. After enucleation at age 12 weeks, only mild shrinkage of ocular dominance columns occurred. Enucleation at ages 1, 5, and 12 weeks did not alter the pattern of thin-pale–thick-pale stripes in V2. The main findings from this study were that (1) CO histochemistry accurately labels the boundaries of columns in layer IVcβ of macaque striate cortex after early monocular enucleation, making it a suitable technique for defining the critical period for plasticity of ocular dominance columns in human striate cortex; (2) enucleation causes more severe shrinkage of ocular dominance columns than eyelid suture; (3) early monocular enucleation obliterates ocular dominance columns in layer IVcβ, but their pattern remains visible in wet sections and with the Liesegang stain; and (4) enucleation does not affect CO staining in V2.

scholarly journals The Expression Patterns of Cytochrome Oxidase and Immediate-Early Genes Show Absence of Ocular Dominance Columns in the Striate Cortex of Squirrel Monkeys Following Monocular Inactivation

2021 ◽  
Vol 15 ◽  
Author(s):  
Shuiyu Li ◽  
Songping Yao ◽  
Qiuying Zhou ◽  
Toru Takahata
Keyword(s):  
Cytochrome Oxidase ◽  
Striate Cortex ◽  
Ocular Dominance ◽  
Expression Patterns ◽  
Immediate Early Genes ◽  
Squirrel Monkeys ◽  
Immediate Early ◽  
Ocular Dominance Columns ◽  
Early Genes ◽  
Layer 4

Because at least some squirrel monkeys lack ocular dominance columns (ODCs) in the striate cortex (V1) that are detectable by cytochrome oxidase (CO) histochemistry, the functional importance of ODCs on stereoscopic 3-D vision has been questioned. However, conventional CO histochemistry or trans-synaptic tracer study has limited capacity to reveal cortical functional architecture, whereas the expression of immediate-early genes (IEGs), c-FOS and ZIF268, is more directly responsive to neuronal activity of cortical neurons to demonstrate ocular dominance (OD)-related domains in V1 following monocular inactivation. Thus, we wondered whether IEG expression would reveal ODCs in the squirrel monkey V1. In this study, we first examined CO histochemistry in V1 of five squirrel monkeys that were subjected to monocular enucleation or tetrodotoxin (TTX) treatment to address whether there is substantial cross-individual variation as reported previously. Then, we examined the IEG expression of the same V1 tissue to address whether OD-related domains are revealed. As a result, staining patterns of CO histochemistry were relatively homogeneous throughout layer 4 of V1. IEG expression was also moderate and homogeneous throughout layer 4 of V1 in all cases. On the other hand, the IEG expression was patchy in accordance with CO blobs outside layer 4, particularly in infragranular layers, although they may not directly represent OD clusters. Squirrel monkeys remain an exceptional species among anthropoid primates with regard to OD organization, and thus are potentially good subjects to study the development and function of ODCs.

Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex

1984 ◽  
Vol 304 (1119) ◽  
pp. 255-272 ◽  
Keyword(s):  
Visual Cortex ◽  
Human Brain ◽  
Cytochrome Oxidase ◽  
Oxidase Activity ◽  
Striate Cortex ◽  
Ocular Dominance ◽  
Lateral Geniculate Body ◽  
Ocular Dominance Columns ◽  
Cytochrome Oxidase Activity ◽  
Transneuronal Degeneration

The cytochrome oxidase stain was applied to autopsy specimens of human brain. In primary visual cortex patches of darker enzyme staining were present in layers II, III, IV b, V, and VI. The patches were oval, about 400 by 250 µm, with a density of one patch per 0.6-0.8 mm 2 of cortex. They were organized into rows spaced about 1 mm apart, intersecting the 17-18 border at right angles. The patches also stained preferentially for AChE activity. The lateral geniculate body was examined in two patients who died many years after losing one eye as adults. In atrophied laminae cytochrome oxidase activity was severely reduced. In the visual cortex from three cases after monocular enucleation, regular alternating light and dark columns of cytochrome oxidase activity were visible in layer IV c, presumably corresponding to ocular dominance columns. In two cases their pattern was reconstructed over 200-400 mm 2 of striate cortex. The columns appeared as roughly parallel slabs about 1 mm wide, oriented perpendicular to the 17-18 border as in the macaque. In the upper layers light and dark rows of patches were present, which fit in register with the light and dark ocular dominance columns below. In layer IV the ocular dominance columns were also visible in Nissl stained sections as a consequence of secondary anterograde transneuronal degeneration. Darker Nissl stained columns matched lighter cytochrome oxidase stained columns corresponding to the missing eye. Quantitative measurements demonstrated a 10% loss of mean cell area and 35% increase in cell density in ocular dominance columns belonging to the missing eye, which accounts for their darker appearance in the Nissl stain. Patches were not present in a foetus at six months gestation. However, they were clearly formed in a six month old baby, although they appeared smaller and more closely spaced than in the adult. These results show that patches are present in man, in addition to other primates, although they appear proportionately larger. Ocular dominance columns are also present, in common with certain species of primates like the macaque, baboon and galago. Cytochrome oxidase histochemistry promises to be a useful technique for mapping anatomical features of the human brain post mortem .

Pattern of ocular dominance columns in human striate cortex in strabismic amblyopia

1996 ◽  
Vol 13 (4) ◽  
pp. 787-795 ◽  
Author(s):  
Jonathan C. Horton ◽  
Davina R. Hocking
Keyword(s):  
Cytochrome Oxidase ◽  
Optic Disc ◽  
Striate Cortex ◽  
Ocular Dominance ◽  
Strabismic Amblyopia ◽  
Ocular Dominance Columns ◽  
Ischemic Infarct ◽  
History Of ◽  
Accommodative Esotropia ◽  
The Right

AbstractPrevious experiments in animals have shown that early unilateral eyelid suture, a model of amblyopia induced by cataract, causes shrinkage of ocular dominance columns serving the deprived eye in the striate cortex. It is unknown whether the ocular dominance columns are affected in amblyopia produced by strabismus. We examined specimens of striate cortex obtained postmortem from a 79-year-old woman with a history of amblyopia in her left eye (20/800) since age 2 from accommodative esotropia. Four years prior to her death, she suffered an ischemic infarct of the left optic disc. This injury to the left optic disc made it possible to label the ocular dominance columns using cytochrome oxidase histochemistry. The pattern of ocular dominance columns was reconstructed throughout most of the right striate cortex. No shrinkage of columns was found. In the left cortex only half the column mosaic was labelled, because the patient had some residual vision in the temporal retina of her left eye. The columns within the labelled portion of the overall mosaic appeared normal. These findings indicate that shrinkage of ocular dominance columns does not occur in humans with amblyopia caused by accommodative esotropia. The ocular dominance columns are probably no longer susceptible to shrinkage at the age when most children with this condition begin to develop amblyopia.

Pattern of ocular dominance columns and cytochrome oxidase activity in a macaque monkey with naturally occurring anisometropic amblyopia

1997 ◽  
Vol 14 (4) ◽  
pp. 681-689 ◽  
Author(s):  
Jonathan C. Horton ◽  
Davina R. Hocking ◽  
Lynne Kiorpes
Keyword(s):  
Cytochrome Oxidase ◽  
Striate Cortex ◽  
Ocular Dominance ◽  
Macaque Monkey ◽  
Poor Vision ◽  
Ocular Dominance Columns ◽  
Anisometropic Amblyopia ◽  
The Core ◽  
The Poor ◽  
Naturally Occurring

AbstractUnilateral eyelid suture, a model for amblyopia induced by congenital cataract, produces shrinkage of the deprived eye's ocular dominance columns in the striate cortex. Loss of geniculocortical projections are thought to account for the poor vision in the amblyopic eye. It is uncertain whether ocular dominance columns become shrunken in other forms of amblyopia. We examined the striate cortex in a pigtailed macaque with natural anisometropia discovered at age 5 months. Amblyopia in the left eye was documented at 1 year by behavioral testing. At age 6 years, the left eye was injected with [3H]proline and the striate cortex was processed for autoradiography and cytochrome oxidase (CO). The ocular dominance columns in layer IVc labelled with [3H]proline were normal. CO staining showed a novel pattern of thin dark bands in layer IV. These bands occupied the core zones at the center of the ocular dominance columns. Their appearance resulted from relative loss of CO activity along the borders of the ocular dominance columns, regions specialized for binocular processing. These findings indicate that not all forms of amblyopia are accompanied by shrinkage of ocular dominance columns. The unusual pattern of CO staining in layer IVc reflected a subtle alteration in metabolic activity which may have resulted from impairment of binocular function in anisometropic amblyopia.

scholarly journals Monocular Cells Without Ocular Dominance Columns

2006 ◽  
Vol 96 (5) ◽  
pp. 2253-2264 ◽  
Author(s):  
Daniel L. Adams ◽  
Jonathan C. Horton
Keyword(s):  
Squirrel Monkey ◽  
Visual Processing ◽  
Striate Cortex ◽  
Single Cells ◽  
Ocular Dominance ◽  
Squirrel Monkeys ◽  
Ocular Dominance Columns ◽  
Receptive Field Property ◽  
Field Property ◽  
Made In

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.

scholarly journals Discrete reduction patterns of parvalbumin and calbindin D-28k immunoreactivity in the dorsal lateral geniculate nucleus and the striate cortex of adult macaque monkeys after monocular enucleation

1994 ◽  
Vol 11 (1) ◽  
pp. 1-11 ◽  
Author(s):  
Ingmar Blümcke ◽  
Eduardo Weruaga ◽  
Sandor Kasas ◽  
Anita E. Hendrickson ◽  
Marco R. Celio
Keyword(s):  
Calcium Binding ◽  
Ocular Dominance ◽  
Dorsal Lateral Geniculate Nucleus ◽  
Projection Neurons ◽  
Macaque Monkeys ◽  
Ocular Dominance Columns ◽  
Monocular Enucleation ◽  
Metabolic Marker ◽  
Cortical Interneurons ◽  
Calbindin D

AbstractWe analyzed the immunohistochemical distribution of the two calcium-binding proteins, parvalbumin (PV) and calbindin D-28k (CB), in the primary visual cortex and lateral dorsal geniculate nucleus (dLGN) of monocularly enucleated macaque monkeys (Macaca fascicularis and Macaca nemestrind) in order to determine how the expression of PV and CB is affected by functional inactivity. The monkeys survived 1–17 weeks after monocular enucleation. The distribution pattern of each of the proteins was examined immunocytochemically using monoclonal antibodies and compared with that of the metabolic marker cytochrome oxidase (CO). We recorded manually the number of immunostained neurons and estimated the concentration of immunoreactive staining product using a computerized image-acquisition system. Our results indicate a decrease of approximately 30% in the labeling of PV-immunoreactive (ir) neuropil particularly in those layers of denervated ocular-dominance columns receiving the geniculocortical input. There was no change in the number of PV-ir neurons in any compartment irrespective of the enucleation interval. For CB-ir, we found a 20% decrease in the neuropil labeling in layer 2/3 of the denervated ocular-dominance columns. In addition, a subset of pyramidal CB-ir neurons in layers 2 and 4B, which are weakly stained in control animals, showed decreased labeling. In the dLGN of enucleated animals, PV-ir and CB-ir were decreased only in the neuropil of the denervated layers.From these results, we conclude that cortical interneurons and geniculate projection neurons still express PV and CB in their cell bodies after disruption of the direct functional input from one eye. The only distinct decrease of PV and CB expression is seen in axon terminals from retinal ganglion cells in the dLGN, and in the axons and terminals of both geniculocortical projection cells and cortical interneurons in the cerebral cortex.

scholarly journals The cortical column: a structure without a function

2005 ◽  
Vol 360 (1456) ◽  
pp. 837-862 ◽  
Author(s):  
Jonathan C Horton ◽  
Daniel L Adams
Keyword(s):  
Receptive Field ◽  
Striate Cortex ◽  
Ocular Dominance ◽  
50Th Anniversary ◽  
Cortical Column ◽  
Cortical Function ◽  
Ocular Dominance Columns ◽  
Cortical Areas ◽  
Architectural Feature ◽  
Joint Receptors

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.

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