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

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.

2006 ◽  
Vol 96 (5) ◽  
pp. 2253-2264 ◽  
Author(s):  
Daniel L. Adams ◽  
Jonathan C. Horton

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.


1997 ◽  
Vol 82 (8) ◽  
pp. 2596-2600 ◽  
Author(s):  
Monika Lessl ◽  
Michael Klotzbuecher ◽  
Silvia Schoen ◽  
Angela Reles ◽  
Klaus Stöckemann ◽  
...  

To shed light on the molecular mechanisms involved in the pathogenesis of uterine leiomyomas, transcript levels of the immediate early genes c-fos, c-myc, and c-jun and of the estrogen receptor (ER) and progesterone receptor (PR) were determined in tissue samples of human myometrium and leiomyoma. The messenger RNA (mRNA) content was analyzed by RT-PCR. mRNAs for c-fos, c-myc, c-jun, ER, and PR were detected in all 18 samples of leiomyoma and corresponding myometrial tissue collected in this study. Interestingly, in contrast to healthy tissues, we found a distinct and significant reduction of c-fos mRNA in the tumor. These data were substantiated by the finding of lowered c-Fos protein levels in leiomyomas tissues. Moreover, transcripts of c-jun and c-myc were less abundant in most of the leiomyomas than in the myometrium. This different expression of the protooncogenes in leiomyomas and myometrium was independent of the phase of the menstrual cycle in which samples were collected. In contrast to the reduced transcript levels observed for the immediate early genes, the ER and PR mRNA contents of the leiomyomas and myometrium did not differ. These results were confirmed by immunohistochemical studies for ER and PR protein. In conclusion, our data show that the deregulated expression of protooncogenes, especially of c-fos, is linked to the pathogenesis of leiomyomas. Confirmation of a potential role of downregulated c-fos levels for the benign character of these tumors requires further investigation. Additionally, the findings suggest that sex steroids do not influence the different expression patterns of c-fos, c-myc, and c-jun in leiomyomas, as compared with myometrium.


2000 ◽  
Vol 17 (4) ◽  
pp. 495-508 ◽  
Author(s):  
JONATHAN C. HORTON ◽  
DAVINA R. HOCKING ◽  
DANIEL L. ADAMS

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.


2006 ◽  
Vol 23 (5) ◽  
pp. 795-805 ◽  
Author(s):  
DANIEL L. ADAMS ◽  
JONATHAN C. HORTON

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.


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 .


1998 ◽  
Vol 15 (2) ◽  
pp. 289-303 ◽  
Author(s):  
JONATHAN C. HORTON ◽  
DAVINA R. HOCKING

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.


1996 ◽  
Vol 13 (4) ◽  
pp. 787-795 ◽  
Author(s):  
Jonathan C. Horton ◽  
Davina R. Hocking

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.


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