Effects of dark rearing on the development of visual callosal connections

Summary It is now well established that during normal postnatal development there is a partial elimination of the callosal projections of cortical areas 17 and 18 in the cat and that visual experience early in life can modulate this process. In the present experiments, we quantitatively studied the influence of light, per se, by rearing cats in total darkness. Dark rearing exaggerates the normally occurring partial elimination of immature callosal projections: it causes a significant reduction in the total number of neurons in both the supra-and infragranular layers that send an axon through the corpus callosum and slightly narrows the distribution of these neurons across areas 17 and 18. These data demonstrate that visual stimulation is not necessary either to initiate the partial elimination of immature callosal projections or to stabilize a large fraction of the callosal projections present at birth. However, normal visual stimulation is necessary for the stabilization of the normal complement of callosal projections.     

Neonatal superior collicular lesions alter visual callosal development in hamster

Summary Visual callosal connections were examined using autoradiographic (ARG) and horse-radish peroxidase (HRP) techniques in normal adult hamsters, and in adults subjected to ablation of the superficial tectal laminae at birth. Additional ARG and HRP experiments were carried out in hamsters 1–27 days of age in order to describe the normal development of this pathway. Neonatal collicular lesions, which deprived visual cortical neurons of a major terminal zone in the midbrain, substantially altered the visual callosal pathway. In the lesioned animals, the numbers of supragranular callosal cells in the 17–18a border region and lamina VI callosal neurons in medial area 17 were significantly greater than normal. The ARG experiments demonstrated additional clearcut abnormalities in the visual callosal pathway of the lesioned hamsters. First, the mediolateral extent of the supragranular callosal zone around the 17–18a border was increased. Secondly, dense label was visible over lower layer V and lamina VI throughout area 17. Finally, labelling in lamina I could also be observed across the entire mediolateral extent of area 17.Experiments in the developing hamsters suggested that some of the abnormalities observed in the lesioned animals may have resulted from the maintenance of normally transient developmental states. During the first postnatal week, both callosal cells and anterograde labelling were evenly distributed throughout the dorsal posterior neocortex, but only in the subplate region. During the second postnatal week, supragranular callosal cells were also labelled in both medial and lateral area 17, but from their first appearance, they were always most numerous in the 17–18a border region. At the same time callosal axons invaded the supragranular laminae, but only near the 17–18a border. By the end of the second postnatal week, the visual callosal pathway was very similar to that in the adult.     

Effects of alternating monocular occlusion on the development of visual callosal connections

Summary During normal postnatal development there is a partial elimination of the callosal projections of cortical areas 17 and 18 in the cat. Visual experience early in life can modulate this process. In the present study, we investigated how restricting visual experience to alternating monocular occlusion affects the development of the callosal connections of cortical areas 17 and 18. Alternating monocular occlusion exaggerates the normally occurring partial elimination of immature callosal projections: it causes a significant reduction in the total number of neurons in the supragranular layers that send an axon through the corpus callosum and marginally increases the distribution of these neurons across areas 17 and 18. Examination of these data in the context of the effects of other types of abnormal early visual experience on the corpus callosum and on the anatomy and physiology of areas 17 and 18 indicates that the postnatal development of the corpus callosum is under the control of multiple, interacting influences which differ in the magnitude and quality of their effects. The data also support the conclusion, drawn from our results in prior studies, that normal visual stimulation is necessary for the stabilization of the normal complement of callosal projections.     

Pharmacological testing of intracortical interneuronal connections

The present study comprises an attempt to investigate the influence of acetylcholine on the functional connections of the cortical cells and their frequency characteristics. The multineuronal activity was recorded in the sensorimotor cortex of immobilized and freely moving rats, and was subsequently analyzed using the method of cross-correlational analysis. In the first series of experiments, the influence of the neuromediator, acetylcholine (ACh), and calcium chelation, ethyleneglycol tetraacetate (EGTA), on the functional characteristics of adjacent neurons during the iontophoretic application of these substances to cells of the sensorimotor cortex of unanesthetized immobilized rats was investigated. In this case, the inotophoretic application of ACh led to a change in the frequency characteristics of individual neurons, and in the majority of cases did not influence the character of the interneuronal interactions. The application of EGTA led to a decrease in the average frequency of impulse activity for the majority of the neurons, as well as to the disappearance, independent of the running frequency, of excitatory connections in the cross-correlograms, with their subsequent recovery following the termination of exposure to the EGTA. In the second series of experiments, carried out in freely moving rats with a chronically implanted recording electrode, the systemic administration of the acetylcholinesterase blocker, galantamine, led to a substantial intensification of the impulse activity of the cortical neurons, and at the same time did not exert a substantial influence on the network activity of the same neurons. The hypothesis is advanced that the intracortical neuronal interactions may be accomplished independently of extracortical influences that are expressed in the fluctuations of the baseline impulse activity of individual cells. The qualitative assessment that was carried out of the influence of ACh on the functional characteristics of the cortical neurons does not make it possible to identify an influence of ACh (including a modulatory influence) on the formation of intracortical connections. The methods used in this investigation may be used for a further study of the influence of various mediator systems of the brain on the functioning of intracortical interneuronal connections. Deceased Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow. Translated from Zhurnal Vysshei Nervnoi Deyatel'nosti imeni I. P. Pavlova, Vol. 44, No. 6, pp. 1016–1025, November–December, 1994     

The postnatal development of somatosensory callosal connections after partial lesions of somatosensory areas

Summary The distribution of S1 (first somatosensory area) and S2 (second somatosensory area) neurons projecting to the contralateral S2 was studied with horseradish peroxidase in normal adult cats and in cats aged between 129 and 248 days in which the injected S2 area had been deprived of some of its input by an earlier lesion (on postnatal days 3 to 30; day of birth = day 1) of ipsilateral S1, alone or combined with a lesion of contralateral S2. In animals with S1 lesions, as in the normal controls, labeled neurons were selectively distributed to the regions of the trunk representation and to parts of the forelimb and hindlimb representations; however, the normally acallosal region in the forepaw representation contained scattered labeled neurons in three of the four animals whose S1 had been lesioned during the first postnatal week. In these animals, the distribution of labeled neurons in the contralateral S2 was apparently normal. Furthermore, the additional lesion of this area during the first postnatal week (one animal) did not increase the degree of filling-in of the normally acallosal parts of S1.The partial filling-in of the acallosal parts of S1 is probably due to the preservation to adulthood of some of the callosal neurons which are present in these regions during the early postnatal life. Possibly, these neurons did not disappear (or lose their callosal axons) because the neonatal lesion (i) allowed their successful competition for terminal space in contralateral S2 or (ii) induced a reorganization of the peripheral input to this area.This work was supported by the Swiss National Science Foundation grant 2.219.0.78 to G.M. Innocenti and by the CNR. R. Caminiti was the recipient of a fellowship from the European Science Foundation     

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     

Effects of neonatal splitting of the optic chiasm on the development of feline visual callosal connections

During normal postnatal development, there is an overproduction and subsequent partial elimination of the callosal projections of cortical areas 17 and 18 in the cat. In the present study, we investigated how neonatal splitting of the optic chiasm affects this process. Our results indicate that neonatal splitting of the optic chiasm exaggerates the normally occurring partial elimination of immature callosal projections: it causes a significant reduction in the total number of neurons in the supragranular layers that send an axon through the corpus callosum. It does not, however, cause a significant change in the number of callosally projecting neurons in the infragranular layers. These data suggest that in addition to other factors previously described, the level or spatial distribution of correlated binocular input to visual cortical neurons may influence the stabilization/elimination of immature callosal connections.     

Distribution patterns and individual variations of callosal connections in the albino rat

Summary After complete callosotomy the distribution of degeneration products was re-investigated in adult albino rats. Three to seven days post operation, coronal, horizontal and flattened sections were impregnated according to the new methods of Gallyas et al. (1980) which stain degenerating axons and terminals, respectively. The regional distribution patterns of callosal terminals were directly visualized with dark field illumination at low magnification. With this technique the distribution pattern of axons and terminals could be compared between different cortical regions and individuals.Callosal terminals tend to accumulate in patches or bands along the borders of cortical regions and areas. The concentration of callosal terminals was especially high at the common corners of more than two cortical areas. The callosal system shows a rather constant distribution pattern which is composed of column shaped subunits. Considerable individual variations were recognized concerning the number, position, shape, density and contiguity of the columnar units either occupied by callosal connections or empty. Although the laminar distribution of callosal terminals shows some similarities in different areas of the cortex, there is no common laminar pattern characteristic either for the whole neocortex or for any cortical region. The comparison between consecutive sections stained either for degenerating fibers or degenerating axon terminals revealed that the callosal axons do not determine directly the arrangement and packing density of callosal synapses. Whatever determines the position and amount of callosal synapses this influence seems to be exerted via translation into the columnar organization.     

Postnatal shaping of callosal connections from sensory areas

Summary Horseradish peroxidase (HRP) was injected unilaterally into the first and second visual areas (VI and V2; areas 17 and 18) of 20 kittens aged between 2 and 90 days and into the second somatosensory area (S2) of 16 kittens aged between 1 and 52 days. The radial and tangential (normal and parallel to the pial surface, respectively) distributions of neurones giving origin to callosal axons (callosal neurones) were studied. In adult cats, callosal efferent zones (CZs) are defined by the distribution of callosal neurones. CZs occupy, in the visual cortices, tangentially and radially restricted parts of areas 17, 18, 19 of the lateral suprasylvian gyms and in the somatosensory cortices, parts of SI and S2. At birth, callosal neurones are distributed throughout the tangential extent of visual and somatosensory areas; they are also more widespread in depth than in the adult. During the first postnatal month, as a result of the gradual disappearence of callosal neurones from parts of the visual and somatosensory areas, the adult CZs emerge. The CZ in areas 17 and 18 undergoes a further tangential reduction during the second and third postnatal months.Supported by the Swiss National Science Foundation (3.492.075 and 3.319-0.78)Part of these experiments was carried out at the Institute of Physiology of the University of Ancona     

Reciprocal heterotopic callosal connections between the two striate areas in Tupaia

Summary WGA-HRP injections were placed into area 17 close to the border with area 18 of Tupaia belangeri in order to study the callosal connections of the striate area in this animal. Most callosal neurons were found in the striate cortex (57.6–86.9%), some in the extrastriate area 18 (10.6–28.1%), and a few in even more temporal regions (2.5–14.3%). Concerning only the area 17, reciprocal homotopic connections could be observed as a strip along the area 17/18 border. Additionally, heterotopic callosal connections could be seen in regions representing the binocular visual field, especially the lower part. The area 17 cells were mostly located in the supragranular layers II and III (94.1–97.2%). But neurons could also be found in the infragranular layers, especially layer VI (2.6–5.2%) and in layer IV (0.2–1.1%). Homotopic projections were mostly seen in layers IIIc and V. The majority of the supragranular and infragranular neurons are pyramidal cells. However, a newly defined subpopulation of neurons, most probably stellate cells, were discovered forming a band in sublayer IIIc, very close to the layer III/IV border.     

Functional organization of the callosal connections of the cat auditory cortex

In acute experiments on immobilized cats, using a method of topographical recording of homotopic and heterotopic transcallosal responses, the functional organization of the callosal connections of the auditory cortex was investigated. It was established that the homotopic potentials of the primary projection field (AI) have the greatest amplitude, minimal temporal parameters, and the maximal stability of these characteristics as compared with the associative fields of the auditory cortex (AII, AIV, Ep). The heterotropic transcallosal responses in field AI appeared during stimulation of the analogous field, while in field Ep, they were recorded both during stimulation of the analogous field, and of fields AI and AII of the opposite hemisphere. It is hypothesized that the structure of the transcallosal connections of the primary projection fields of the auditory cortex is characterizised by homotopy, whereas in the associative auditory fields the role of heterotopic transcallosal interactions increases. It is possible that such a structure of the transcallosal connections assures a significant role for interhemispheric interactions in the mechanisms of spatial audition.Translated from Fiziologicheskii Zhurnal SSSR imeni I. M. Sechenova, Vol. 73, No. 7, pp. 860–867, July, 1987.     

Area 17 of anthropoid primates does participate in visual callosal connections

Injections of retrograde tracers into the border region of areas 17 and 18 in Callithrix and Macaca labeled a small group of neurons in the border region of contralateral area 17, in addition to cells in contralateral area 18. It is concluded that area 17 of anthropoid primates sends (and receives) fibers through the corpus callosum.     

The pattern of callosal connections in posterior neocortex of congenitally anophthalmic rats

Summary In an effort to assess the innate capacity of the central visual system to specify corticocortical connectivity in the absence of retinal afferents, we examined the tangential distribution of callosal cells and terminations in posterior neocortex of congenitally anophthalmic rats. Although our results indicate that the callosal pattern is clearly anomalous in these rats, all features of the normal visual callosal pattern are recognizable in mutant rats, indicating that central visual pathways can generate many aspects of normal interhemispheric connectivity in the absence of input from the periphery. On the other hand, the presence of anomalies in the pattern indicates that the eyes are necessary to finetune the distribution of callosal connections at some developemental stage. Moreover, the fact that abnormalities in the callosal pattern of mutant rats are the same as those previusly described in rats enucleated at birth suggests that the eyes begin to exert their influence on callosal development after birth.