Ontogenetic Characteristics of the Organization of Corticocortical Connections between the Primary Visual Cortex and the Lateral Suprasylvian Area of the Cat Brain

Studies on 10 cats aged five and 12 weeks included qualitative and quantitative analyses of the distribution in field 17 of initial neurons organizing corticocortical connections with the posteromedial lateral suprasylvian gyrus (PMLS) of the brain using retrograde labeling with horseradish peroxidase. The PMLS area is a higher center for processing information relating to the movement of visual stimuli. Ontogenetic characteristics of the formation of the ordered (clustered) organization of initial neurons in field 17 were identified. An age-related decrease in the density of initial neurons in field 17 was found, from 125.2 ± 69.8 cells/mm² in kittens aged five weeks to 34.7 ± 17.4 cells/mm² in 12-week-old kittens (p = 0.05). During the period between postnatal weeks 5 and 12, there was an increase in the size of the labeled area containing the majority of initial neurons. The morphofunctional aspects of the formation of the ordered structure of corticocortical connections between field 17 and the PMLS during postnatal ontogenesis and its possible relationship with the development of the function of the visual perception of moving objects are discussed.     

Morphological analysis of the formation of cluster organization of neurons,forming the corticocortical connections in the cat visual cortex in early postnatal ontogenesis

The development of cluster organization of neurons forming direct interzonal associative projections from striate cortex (area 17) to extrastriate area 21a in cat was studied by a technique of horseradish peroxidase retrograde transport. Reconstruction of cortical region containing retrogradely labeled neurons was performed using continuous serial sections of the brain. The analysis of spatial organization was done and quantitative characteristics of distribution pattern of initial corticocortical neurons in striate cortex in kittens were obtained. Interzonal connections were detected since 14th postnatal day. Neuronal cluster organization started forming after day 21 while its pattern became similar to that in the adult animal both qualitatively and quantitatively by the end of the 2nd postnatal month, that is somewhat later than it was previously thought. The data obtained also demonstrate the age-dependent decrease in the convergence of the striate cortex projections to area 21a associated with the reduction of the area, occupied by initial neurons.     

Morphology of visual callosal neurons with different locations,contralateral targets or patterns of development

In kittens, callosally projecting neurons were labeled by retrograde transport of FITC- (fluorescein isothiocyanate)- and TRITC- (tetramethylrhodamine isothiocyanate)-conjugated latex microspheres injected in two different visual areas (17, 17/18, 19, or postero-medial lateral suprasylvian; PMLS) at postnatal day 3. At postnatal day 57 more than 1200 labeled neurons in visual cortical areas were intracellularly injected with 3% lucifer yellow (LY) in perfusion-fixed slices of the contralateral hemisphere. The distribution of labeled neurons was charted, and LY-filled neurons were classified on the basis of their area and layer of location, and dendritic pattern. The dendritic arbors of 120 neurons were computer reconstructed. For the basal dendrites of supragranular pyramidal neurons a statistical analysis of number of nodes, internodal and terminal segment lengths, and total dendritic length was run relative to the area of location and axonal projection. Connections were stronger between homotopic than between heterotopic areas. Overall tangential and laminar distributions depended on the area injected. Qualitative morphological differences were found among callosally projecting neurons, related to the area of location, not to that of projection. In all projections from areas 17 and 18, pyramidal and spinous stellate neurons were found in supragranular layers. In contrast, spinous stellate neurons lacked in projections from area 19, 21a, PMLS and postero-lateral lateral suprasylvian (PLLS). In all areas, the infragranular neurons showed heterogeneous typology, but in PMLS no fusiform cells were found. Quantitative analysis of basal dendrites did not reveal significant differences in total dendritic length, terminal, or intermediate segment length among neurons in area 17 or 18, and this was related to whether they projected to contralateral areas 17–18 or PMLS. All injections produced exuberant labeling in area 17. No differences could be found between neurons in area 17 (with transient axons through the corpus callosum) and neurons near the 17/18 border (which maintain projections to the corpus callosum). In conclusion, morphology of callosally projecting neurons seems to relate more to intrinsic specificities in the cellular composition of each area than to the area of contralateral axonal projection or the fate of callosal axons.     

Asymmetry of the internal connections of the striate cortex of the cat in the projection zone of the center of the field of vision

Studies were carried out on the organization of the internal connections of the striate cortex in cats in the projection zone of the center (0–5°) of the field of vision by microintophoretic application of horseradish peroxidase to electrophysiologically identified orientational columns. The area containing neurons showing retrograde labeling in most cases extended in the mediolateral direction. Labeled cells were located in the upper (II, III) and lower (V, VI) layers of the cortex, and the shapes and orientations of the areas containing labeled neurons in these layers coincided. Spatial asymmetry was detected in the distribution of labeled neurons relative to the orientational column studied. Labeled cells were located predominantly medial to the columns, regardless of the distance from the projection of the area centralis. Considering the visuotopical map of field 17, the asymmetry detected here provides evidence that neurons in orientational columns have more extensive connections with neurons of the peripheral part of the cortex. An asymmetrical distribution of “silent” zones around the receptive fields of neurons in orientational columns is suggested, and that these appear to receive influences from the periphery of the visual field. Laboratory of Visual Physiology and Laboratory of Central Nervous System Morphology, I. P. Pavlov Institute of Physiology, Russian Academy of Sciences, 6 Makarov Bank, 199034 St. Petersburg, Russia. Translated from Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 82, No. 12, pp. 23–29, December, 1996.     

Regular Structural Organization of Intrahemisphere Interzonal Connections in the Visual Cortex of the Cat

The aim of the present work was to conduct a morphometric analysis of the cluster organization of neurons forming interzonal corticocortical connections in the visual cortex. The investigations used a method based on retrograde transport of horseradish peroxidase and mathematical analysis of the spatial distribution of labeled cells. Measurements yielded the following quantitative characteristics of the cell distribution--the volume and linear sizes of clusters, the distance between the centers of gravity of clusters, and the periodicity in the distribution of clusters along the cortical surface. Age-related features of the distribution of cells giving rise to cortical interzonal connections were identified. The experiments showed that the pattern of the cluster organization typical of adult cats was formed by the end of the second month of life. Quantitative differences in the spatial organization of neuron groups in the cortex of visual fields 17 and 18 were demonstrated.     

Orderly structural organization of intrahemispheric interzonal connections in the cat visual cortex

The study was aimed at morphometric analysis of cluster organization of neurons, forming interzonal cortico-cortical connections within the visual cortex. The study employed the technique based on horseradish peroxidase retrograde transport and methods of mathematical analysis of spatial distribution of labeled cells. The quantitative characteristics of cell distribution were obtained including cluster volume and linear dimensions, distances between their centers of gravity, periodicity and distribution along cortical surface. Age-related peculiarities in the distribution of initial cells of cortical interzonal connections were found. It was demonstrated that adult cluster organization pattern was established by the end of the second postnatal month. Quantitative differences in the spatial distribution of neuronal groups in the visual cortical areas 17 and 18 were determined.     

Projections from visual cortical area 19, the posterior medial lateral suprasylvian area and the lateral posterior-pulvinar complex of the thalamus to areas 17 and 18 in young kittens

Retrogradely transported horseradish peroxidase (HRP) or HRP conjugated to wheat germ agglutinin was used to demonstrate projections from area 19, the posterior medial lateral suprasylvian area (PMLS) and the lateral posterior-pulvinar complex (LP-PC) of the thalamus to areas 17 and 18 of the visual cortex in young kittens. Areas 17 and 18 in kittens, as in adult cats, receive association fibres from cells lying mainly in deep cortical laminae in area 19 and PMLS, and projections from the LP-PC of the thalamus.     

The postnatal development of visual callosal connections in the absence of visual experience or of the eyes

Summary Counts of callosal neurons retrogradely labeled by horseradish peroxidase (visualized using multiple substrates) were obtained in areas 17 and 18 of five kittens reared with their eyelids bilaterally sutured and of three kittens which had undergone bilateral enucleation on postnatal days 1–4. These counts were compared with those obtained in normal adult cats.The normal adult distribution of the callosal neurons results from the gradual postnatal reduction of a more widespread juvenile population. Binocular visual deprivation by lid suturing dramatically decreases the final number of callosal neurons and narrows their region of distribution (callosal zone) in areas 17 and 18. A less severe reduction in the final number of callosal neurons is caused by bilateral enucleation, which also increases the width of the callosal zone compared to that of normal cats. Thus, visual experience is necessary for the normal stabilization of juvenile callosal connections. However, since some callosal neurons form connections in the absence of vision, other influences capable of stabilizing juvenile callosal neurons also exist. These influences are probably antagonized by destabilizing influences or inhibited, when the eyes are intact.This work was supported by Swiss National Science Foundation grant 2.219.0.78 to Dr. G.M. Innocenti; Dr. D.O. Frost received a fellowship from the American-Swiss Foundation for Scientific Exchange     

Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens

Summary Previous studies have shown that functional compensation is present in the cat's posteromedial lateral suprasylvian (PMLS) area of cortex after damage to areas 17, 18, and 19 (visual cortex) early in life but not after damage in adults. These studies all have investigated animals with a unilateral visual cortex lesion, whereas all behavioral studies of compensation for early visual cortex damage have investigated animals with a bilateral lesion. In the present experiment, we investigated whether functional compensation also is present in PMLS cortex after a bilateral visual cortex lesion early in life. We recorded from single neurons in the PMLS cortex of adult cats that had received a bilateral lesion of areas 17, 18, and 19 on the day of birth or at 8 weeks of age. We found that PMLS cells in both groups of cats had functional compensation (normal direction selectivity and ocular dominance) similar to that seen after a unilateral lesion at the same ages. These results are consistent with the hypothesis that PMLS cortex is involved in the behavioral compensation seen after early visual cortex damage. In addition, the results indicate that inputs from contralateral visual cortex are not necessary for the development of functional compensation seen in PMLS cortex.     

新生猫视皮质胼胝体神经元的DiI示踪研究

采用ＤｉＩ示踪法研究了新生猫视皮质的胼胝体神经元的分布和形态．ＤｉＩ标记的胼胝体神经元普遍分布于视皮质各区,包括在成年时缺乏胼胝体联系的１７区内侧部．这些标记的神经元位于除Ⅰ层外的皮质各层中,但大部分位于Ⅲ展并有成簇分布的倾向．ＤｉＩ标记的胼胝体神经元,特别是位于Ⅱ／Ⅲ层者大多呈“Ｇｏｌｇｉ样”标记,其树突走行和各级分支,甚至树突棘均清晰易辨．上述结果除证实以往用其他方法证明的新生猫视皮质胼胝体神经元的分布外,还显示了标记神经元的详细形态特点,表明ＤｉＩ示踪法是研究发育中的神经通路起源细胞及其突起形态的一种简单而有效的手段．     

The inhibitory effect of the ventrolateral periaqueductal grey matter on neurones in the rostral ventrolateral medulla involves a relay in the medullary raphe nuclei

We have investigated the expression of messenger RNA (mRNA) encoding substance P receptor (SPR) in the visual cortex of adult cats and 17-day-old kittens, using in situ hybridization histochemistry with two digoxigenin-labeled oligodeoxynucleotides complementary to the SPR mRNA. In the adult cortex, a subset of large pyramidal neurons of layer V and layer III is heavily labeled. Other, mainly pyramidal neurons in layers II, III and V are less intensely labeled, but most neurons in these layers appear unlabeled. Neurons in layer IV and VI, and in the white matter do not show hybridization signals above background levels. In the 17-day-old kitten, SPR mRNA-expressing cells are confined to layer V and to the upper white matter (subplate zone), whereas supragranular neurons do not yet contain SPR mRNA. A few neurons in layer VI display moderate labeling. Astrocytes, identified with anti-glial fibrillary acid protein antibodies, did not express detectable levels of SPR mRNA in both adult and kitten visual cortex. These results indicate that SPR mRNA expression is transient in neurons of the white matter, and is developmentally regulated in supragranular layers. In addition, the localization of SPR mRNA in a subset of pyramidal cells suggests that substance P modulates the excitability of certain projection neurons which are the origin of extrinsic connections.     

Zinc-rich afferents to the rat neocortex: projections to the visual cortex traced with intracerebral selenite injections

Infusion of sodium selenite to the occipital cortex of the rat was used for the specific tracing of zinc-rich pathways. Large numbers of labeled somata were found ipsilaterally in the visual, orbital and frontal cortices, and contralaterally in homotopic and heterotopic visual areas. Labeled neurons were also found ipsilaterally in the retrosplenial, parietal, sensory-motor, temporal and perirhinal cortex. In contrast to the cortico-cortical connections, ascending afferents to the visual cortex were not zinc-rich except for a few labeled neurons in the claustrum. Additional injections showed reciprocal zinc-rich connections between the visual cortex and the orbital and frontal cortices. The latter cortices also received ascending zinc-rich afferents from the claustrum. Selenite injections revealed the layered distribution and the morphology of these labeled neurons in the neocortex. Zinc-rich neurons were found in layers II–III, V and VI. However, none was found in layer IV. Zinc-rich somata appeared as pyramidal and inverted neurons. The contrasting chemical properties of cortical and subcortical visual afferents may account for the functional differences between these systems.     

Characteristics of Cytochrome Oxidase Activity in Visual System Neurons in Kittens Reared in Conditions of Flashing Illumination

The studies reported here addressed the effects of flashing (15 Hz) lights on the metabolic activity of visual system neurons in animals reared in condition of crepuscular illumination. Activity of the respiratory enzyme cytochrome oxidase was detected in the cortex of visual areas 17 and 18 and in the lateral geniculate body in kittens. The results showed that kittens subjected to this stimulation, unlike intact kittens and kittens reared in conditions of crepuscular illumination, showed a change in the pattern of cytochrome oxidase distribution in cortical field 17 consisting of the appearance of alternating areas of increased and decreased enzyme activity in layers III and IV. In cortical field 18 and the lateral geniculate body, experimental kittens showed no changes in the cytochrome oxidase activity distribution pattern. It is suggested that flashing illumination leads to disturbance of the balance in activity in the Y and X conducting channels of the visual system.__________Translated from Morfologiya, Vol. 126, No. 5, pp. 20–23, September–October, 2004.Doctor of Sciences F. M. Makarov     

How complete is physiological compensation in extrastriate cortex after visual cortex damage in kittens?

Summary Previous studies indicate that neurons in the cat's posteromedial lateral suprasylvian (PMLS) visual area of cortex show physiological compensation after neonatal but not adult damage to areas 17, 18, and 19 of the visual cortex (collectively, VC). Thus, VC damage in adults produces a loss of direction selectivity and a decrease in response to the ipsilateral eye among PMLS cells, but these changes are not seen in adult cats that received VC damage as kittens. This represents compensation for early VC damage in the sense that PMLS neurons develop properties they would have had if there had been no brain damage. However, this is only a partial compensation for the effects of VC damage. A full compensation would involve development of properties of the VC cells that were removed in the damage. The present study investigated whether this type of compensation occurs for detailed spatial- and temporal-frequency processing. Single-cell recordings were made in PMLS cortex of adult cats that had received a VC lesion on the day of birth or at 8 weeks of age. Responses to sine-wave gratings that varied in spatial frequency, contrast, and temporal frequency were assessed quantitatively. We found that the spatial- and temporal-frequency processing of PMLS cells in adult cats that had neonatal VC damage were not significantly different from PMLS cells in normal cats. Therefore, there was no evidence that PMLS cells can compensate for VC damage by developing properties that are better than normal and like those of the striate cortex cells that were damaged.We also assessed the effects of long-term VC damage in adult cats to determine whether the normal properties seen in cats with neonatal VC damage represent a compensation for abnormalities in PMLS cortex present after adult damage. In a previous study, we found that acute VC damage in adult cats has small but reliable effects on maximal response amplitude, maximal contrast sensitivity, and spatial resolution (Guido et al. 1990b). In the present study, we found that long-term VC damage in adult cats does not increase these abnormalities as a result of secondary degenerative changes. In fact, the minor abnormalities that were present after an acute VC lesion were virtually absent following a long-term adult lesion, perhaps because they were due to transient traumatic effects. Therefore, there was little evidence for abnormalities in spatial- or temporal-frequency processing following long-term adult VC damage for which PMLS cells might show compensation following long-term neonatal damage.Our results thus indicate that there is little or no difference in the spatial- or temporal-frequency processing of PMLS cells in normal cats and cats with long-term VC damage received early in life or as adults. These findings are discussed in relation to the inputs to PMLS cortex and to the behavioral abilities of cats with VC damage at different ages. The implications for under-standing the role of lateral suprasylvian visual cortex in behavioral recovery from VC damage is considered.     

猫视皮层17区一氧化氮合酶阳性神经元的生后发育

用ＮＡＤＰＨ ｄ 黄递酶组化技术观察了生后不同年龄段猫视皮层１７ 区中一氧化氮合酶阳性神经元的生后发育状况。结果显示： 生后１ 周内,一氧化氮合酶阳性细胞仅出现于皮层的第５／６ 层以及皮质下板（白质）中,皮质板中极少;生后２ 周时,一氧化氮合酶阳性细胞见于２／３ 和４ 层;在随后的发育中,２／３ 层与４ 层中阳性细胞逐渐增多,第５ 周时呈现与成年动物相似的分布模式。一氧化氮合酶阳性细胞的发育模式反映了皮质板的形成过程,即“由内向外”的皮层片层成熟模式;成年动物的皮层１７ 区中一氧化氮合酶阳性细胞远远高于幼年。猫视皮层１７ 区中一氧化氮合酶阳性细胞发育的时空表达模式与猫视皮层发育的关键期无明显吻合关系,推测视皮层中内源性一氧化氮与视皮层的眼优势柱的可塑性无关,为Ｒｅｉｄ 等和Ｒｕｔｈａｚｅｒ 等的电生理学研究结果提供了形态学证据。     

Structure of Internal Interneuronal Connections in Field 17 of the Cat Cerebral Cortex

The spatial distribution of horizontal internal connections in field 17 of the cat cortex was studied after microiontophoretic application of horseradish peroxidase to individual cortical columns. Cluster analysis of the distribution of labeled cells in the superficial layers in the tangential plane of the cortex was performed. Field 17 included 7 +/- 1 clusters of up to five cells. Clusters were distributed into two layers, separated by 1.2 +/- 0.3 mm. The distance between the centers of the clusters forming rows was 0.8 +/- 0.3 mm. The spatial characteristics of the grouping of cells sending axons into the cortical column were compared with published data based on optical visualization of the activity of neurons in orientational and eye-dominant columns of the visual cortex. It is suggested that columns in field 17 are associated with 6-8 hypercolumns, though only with a single type of neuron within these hypercolumns, in terms of eye dominance and orientational preference.     

Development of orientation tuning in simple cells of primary visual cortex

Orientation selectivity and its development are basic features of visual cortex. The original model of orientation selectivity proposes that elongated simple cell receptive fields are constructed from convergent input of an array of lateral geniculate nucleus neurons. However, orientation selectivity of simple cells in the visual cortex is generally greater than the linear contributions based on projections from spatial receptive field profiles. This implies that additional selectivity may arise from intracortical mechanisms. The hierarchical processing idea implies mainly linear connections, whereas cortical contributions are generally considered to be nonlinear. We have explored development of orientation selectivity in visual cortex with a focus on linear and nonlinear factors in a population of anesthetized 4-wk postnatal kittens and adult cats. Linear contributions are estimated from receptive field maps by which orientation tuning curves are generated and bandwidth is quantified. Nonlinear components are estimated as the magnitude of the power function relationship between responses measured from drifting sinusoidal gratings and those predicted from the spatial receptive field. Measured bandwidths for kittens are slightly larger than those in adults, whereas predicted bandwidths are substantially broader. These results suggest that relatively strong nonlinearities in early postnatal stages are substantially involved in the development of orientation tuning in visual cortex.     

Effects of visual deprivation on the postnatal development of the geniculocortical projection in kittens

In kittens reared with either monocular, binocular or reverse suture, beginning before the physiological eyelid opening (around one week of age) and lasting until after one month, the cortical laminar distribution of geniculocortical afferents to area 17 was examined by using orthograde transport of wheat germ agglutinin conjugated with horseradish peroxidase, and compared with that in normal kittens. In normal kittens, at birth, the afferents were distributed most densely in layer I and, to a lesser extent, widely from the upper part of layer II to layers V or VI. After one month, the afferents were found mainly in and around layer IV and very sparsely in layer I. Neither binocular nor monocular suture affected this normal development. In contrast, when the present procedure of monocular suture had been followed by opening the sutured lid and suturing the other lid (reverse suture) for one week, the distribution was altered. The density of the afferents in layer I was increased while the labelled terminals in deeper layers were as segregated in and around layer IV as observed in normal kittens. Such increase in density of the afferents resulted only when the injected tracer covered the medial or intermediate part of the C complex of the lateral geniculate nucleus. To confirm these findings, geniculate neurons retrogradely labelled by horseradish peroxidase injections into layer 1 of area 17 were examined in normal and reverse-sutured kittens. In both kinds of kittens, the labelled neurons were dense in the C complex, and absent or sparse in the A laminae. But, the number was higher in reverse-sutured kittens. These results suggest an involvement of geniculocortical layer I projections in reorganization of neuronal circuits in the visual cortex.     

Afferent bases of spatial- and temporal-frequency processing by neurons in the cat's posteromedial lateral suprasylvian cortex: effects of removing areas 17, 18, and 19

1. We investigated whether spatial- and temporal-frequency processing by neurons in the cat's posteromedial lateral suprasylvian (PMLS) extrastriate cortex depends on inputs from ipsilateral areas 17, 18, and 19 (visual cortex; VC) or occurs in parallel with those cortical areas. 2. Single neurons were recorded in PMLS cortex of normal adult cats and adult cats that had ipsilateral VC removed within 24 h before recording. Receptive-field properties were characterized, and responses to sine-wave gratings of different spatial frequencies, contrasts, and temporal frequencies were measured and Fourier analyzed. 3. As in previous studies, removing inputs from VC led to a reduction in the proportion of direction-selective PMLS cells. In addition there were statistically significant reductions in response amplitude and variability, although signal-to-noise ratios were unchanged. Contrast sensitivity also was reduced at all spatial frequencies. Spatial resolution was reduced slightly; however, this reduction appears to be secondary to the overall reduction in response amplitude and sensitivity. 4. The shape of the spatial-frequency contrast-sensitivity functions and the distribution of optimal spatial frequencies were unaffected by removing inputs from VC. In addition, once response threshold was reached, the slope of the contrast-response function (contrast gain) at the optimal spatial frequency was similar for PMLS cells in normal cats and cats with a VC lesion. 5. When tested at the optimal spatial frequency, temporal-frequency bandwidths, high and low temporal-frequency cutoffs, and optimal temporal frequencies were similar for PMLS cells in normal cats and cats with VC removed. 6. The results thus indicate that inputs from VC are important for the elaboration of direction selectivity and affect response amplitude and contrast sensitivity among PMLS neurons. However, visual-cortical inputs have little or no influence on spatial- and temporal-frequency processing by PMLS neurons. These properties depend on inputs from other cortical areas or the thalamus and are processed in parallel with areas 17, 18, and 19.     

Neuronal connections of eye-dominance columns in the cat cerebral cortex after monocular deprivation

Plastic changes in intrahemisphere neuronal connections of the eye-dominance columns of cortical fields 17 and 18 were studied in monocularly deprived cats. The methodology consisted of microintophoretic administration of horseradish peroxidase into cortical columns and three-dimensional reconstruction of the areas of retrograde labeled cells. The eye dominance of columns was established, as were their coordinates in the projection of the visual field. In field 17, the horizontal connections of columns receiving inputs from the non-deprived eye via the crossed-over visual tracts were longer than the connections of the "non-crossed" columns of this eye and were longer than in normal conditions; the connections of the columns of the deprived eye were significantly reduced. Changes in the spatial organization of horizontal connections in field 17 were seen for the columns of the non-deprived eye (areas of labeled cells were rounder and the density of labeled cells in these areas were non-uniform). The longest horizontal connections in deprived cats were no longer than the lengths of these connections in cats with strabismus. It is suggested that the axon length of cells giving rise to the horizontal connections of cortical columns has a limit which is independent of visual stimulation during the critical period of development of the visual system.