Transcallosally evoked responses in the visual cortex of normal and monocularly enucleated rabbits

Summary In visual cortex of normal adult rabbits, callosal projections are restricted to a 2 mm wide band at the area 17/18 border. In adult rabbits which are monocularly enucleated (ME) on the day of birth, the callosal zone extends 4 mm into the medial region of area 17 in the cortex ipsilateral to the remaining eye. In this study, the function of these anomalous callosal projections in ME rabbits was investigated using electrophysiological techniques. A microelectrode was placed in the visual cortex ipsilateral to the enucleated eye at the 17/18 border, bipolar stimulating electrodes were placed in a homotopic location in the contralateral cortex, and averaged evoked responses (AERs) to stimulation were recorded. The stimulating electrodes were then moved mediolaterally in 1 mm steps, and the AERs were recorded for each location of the stimulating electrodes. In the normal rabbit, a maximal short latency evoked response was recorded when the stimulating electrodes were at a location homotopic to the recording electrode. When the stimulating electrodes were moved a distance of 1 mm or more from this optimal position, this short latency response was either absent or dramatically decreased in amplitude, reflecting the precise topographic pattern of the normal callosal projection. In contrast, in ME rabbits, a consistent response was evoked at the 17/18 border when the stimulating electrodes were moved as much as 3 mm medial to the homotopic position. Since antidromically activated responses and both pre- and post-synaptic orthodromically activated responses contribute to the AER, recordings were also made from single cells in some animals. Orthodromically activated single cell responses were evoked by electrical stimulation in the abnormal medial callosal zone of ME rabbits. The data indicate that abnormal callosal projections in ME rabbits can mediate functional interactions between nonhomotopic areas of the primary visual cortices.     

The role of crossed and uncrossed optic pathways mediating black-white discrimination in rats with one eye enucleated at birth

It has been reported that rats with one eye enucleated at birth (OEB) are able to relearn a black-white discrimination task originally learned with both the visual cortices intact faster than rats monocularly enucleated at three months of age (OET) when relearning is made after the visual cortex contralateral to the remaining eye is destroyed. Two experiments examined the hypothesis that functional enhancement of uncrossed optic pathways produced by monocular enucleation at birth might be the sole factor to produce such a phenomenon. The results showed that faster relearning in OEBs could not be totally explained by the hypothesis, and suggest that only when (1) there is a learning effect in the visual cortex ipsilateral to the remaining eye produced by interaction of visual information through the callosal fibers with an increased amount of information through uncrossed optic pathways during original learning and (2) relearning is mediated by enhanced functioning of uncrossed optic pathways, would such phenomenon be produced.     

Altered expression of parvalbumin and calbindin in interneurons within the primary visual cortex of neonatal enucleated hamsters

In the present study, we tested the hypothesis that the expression of calcium binding proteins (CaBPs), parvalbumin (PV), calretinin (CR) and calbindin (CB), is dependent upon sensory experience as emphasized in visual deprivation and deafferentation studies. The expression of CaBPs was studied in interneurons within the primary and extrastriate visual cortices (V1, V2M, V2L) and auditory cortex (AC) of adult hamsters enucleated at birth. The effects of enucleation were mainly confined to area V1 where there was a significant volume reduction (26%) and changes in the laminar distribution of PV and CB immunoreactive (IR) cells. The density of PV-IR cell bodies was significantly increased in layer IV and reduced in layer V. Moreover, the density of CB-IR neurons was inferior in layer V of V1 in enucleated hamsters (EH) compared to controls. These results suggest that some features of the laminar distribution of specific CaBPs, in primary sensory cortices, are dependent upon or modulated by sensory input.     

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     

ECoG effects of peripheral deafferentation of prepyriform and visual cortices in rats

Freely-behaving Wistar albino male rats were prepared for chronic recording of the electrocorticographic (ECoG) activity of neo- and paleocortical areas and of the electromyogram of dorsal neck muscles. The effects of the uni- or bilateral removal of the main olfactory bulbs and adjacent structures on the prepyriform cortex (PPC) ECoG, and the possible ECoG modifications in the area 17 after bilateral eye enucleation were studied. In spite of the fact that the PPC general cycling pattern along the sleep-wakefulness cycle (SWC) was not appreciably affected by the olfactory deafferentation, this experimental maneuver did cause very marked alterations in the PPC ECoG during all of the observed SWC phases. On the other hand, no appreciable ECoG modifications could be detected in area 17 after the visual deafferentation. A comparison of these results with pertinent literature for cats and monkeys allows the formulation of some working hypotheses that deserve experimental testing in the future.     

Long term effects of callosal lesions in the auditory cortex of rats of different ages

The corpus callosum was sectioned in groups of rats 3, 12, and 24 months of age, and the auditory cortex was examined three months later to determine whether there were age-related differences in the morphological response to the partial deafferentation. Material from the three groups of long-term callosally-lesioned rats were compared with three groups of age-matched control animals. Analysis focused on those cortical layers known to receive the heaviest callosal projection (layers II and III) and those neurons known to be postsynaptic to callosal afferents (layer V pyramidal neurons). There were no age-related changes in cortical thickness or in the relative thickness of the cortical layers in the control groups. However, the apical dendrites of layer V pyramidal neurons did lose dendritic spines and became thinner with age. In all three lesion groups, the cortex became thinner without altering the relative thickness of cortical layers; there was a decrease in the relative density of apical dendrite spines in layer III, but an increase in the density of these spines in layer IV. Both effects varied with age. Spine decreases in layer III were greatest in older animals and spine increases in layer IV were greatest in younger animals. The mean diameters of apical dendrites decreased in the youngest group of lesioned animals but increased in the oldest group. The results indicate that the effects of callosal deafferentation are age dependent.     

Spatial distribution of cingulate cortical cells projecting to the primary motor cortex in the rat

We examined the location and spatial distribution of cingulate cortical cells projecting to the primary motor cortex (M1) in rats, using a double retrograde-labeling technique. The orofacial, forelimb, and hindlimb areas of M1 were physiologically identified based on the findings of intracortical microstimulation and single cell recording. Two different tracers, diamidino yellow and fast blue, were injected into two sites of M1 in each rat. Retrograde-labeled cells in the cingulate cortex were plotted with an automated plotting system. Cells projecting to the orofacial and forelimb areas of M1 were distributed in the anterior cingulate cortex (area 24) but not in the posterior cingulate cortex (retrosplenial cortex; area 29), according to topographical mapping. On the other hand, few or no cells of the cingulate cortex were observed projecting to the hindlimb area of M1. These findings suggest that the cingulate cortex projecting to the M1 in the rat are involved in the regulation of motor activity that involves the orofacial and forelimb, but not hindlimb, parts of the body.     

Serotonin nerve fibers in the primary visual cortex of the monkey. Quantitative and immunoelectronmicroscopical analysis

Summary A quantitative and immunoelectronmicroscopical analysis of serotonin nerve fibers in the primary visual cortex of the monkey (Macaca fuscata) was made using a sensitive immunoperoxidase method for serotonin. The overall numerical density of serotonin-containing varicosities in the primate striate cortex was approximately 770,000/mm³ and the highest concentration of immunore-active varicosities (ca. 1,400,000/mm³) was observed in the upper portion of layer IVc, the next highest concentration being in layer IVb (ca. 1,180,000/mm³). At the ultrastructural level, the electron dense immunoreactive products were observed in the small granules (10–65 nm in diameter). The varicosities were usually small (0.5–1.0 m in diameter) and made contact with both stellate and pyramidal cells. Serotonin fibers were often in close apposition to the poorly myelinated axons in layers IVb, V, and VI, and they rarely formed distinct synaptic structures with unlabelled neuronal elements.Supported by grant (No. 57214028) from the Ministry of Education, Science and Culture, Japan     

Direction selectivity of simple cells in the primary visual cortex: comparison of two alternative mathematical models. I: response to drifting gratings

Two models of a single hypercolumn in the primary visual cortex are presented, and used for the analysis of direction selectivity in simple cells. The two models differ as to the arrangement of inhibitory connections: in the first ("antiphase model") inhibition is in phase opposition with excitation, but with a similar orientation tuning; in the second ("in-phase model"), inhibition is in phase with excitation, but with broader orientation tuning. Simulation results, performed by using drifting gratings with different orientations, and different spatial and temporal frequencies, show that both models are able to explain the origin of direction preference of simple cells.     

Protracted postnatal development of corticospinal projections from the primary motor cortex to hand motoneurones in the macaque monkey

We have studied the development of corticospinal projections from the hand area of the primary motor cortex to the spinal cord using anterograde transport of WGA-HRP. In the neonate, as in the adult, corticospinal projections to the intermediate zone at the C8/T1 spinal level were clearly present. However, in contrast to the adult, there was only very faint and barely visible labelling in the dorso-lateral motor nuclei which supply the hand muscles. No aberrant projections to other motor nuclei were seen. By 2.5 months, a ring of dense labelling was present around the dorso-lateral motor nuclei, but labelling was still sparse in the central region. This labelling was more pronounced at 11 months, but was still not as heavy as in the adult. There was no labelling among the ventral motoneurones at any age. The conduction velocity (c.v.) of the fastest corticospinal fibres was determined in each of the monkeys. There was an age-related increase in c.v. within the spinal cord. At birth, the fastest axons had a c.v. of only 8 m·s^-1. At 11 months c.v. was still substantially slower (55 m·s^-1) than the adult value of 73 m·s^-1. In contrast, by 11 months, the axonal c.v. within the brain was close to the adult value, suggesting a rostro-caudal maturation of the corticospinal system. Our results demonstrate that corticospinal projections in the macaque monkey mature gradually over a period of at least 11 months, much longer than previously thought.     

The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex

Disturbances of the orbitofrontal-striatal pathways in humans have been associated with several psychopathologies including obsessive-compulsive disorder and drug addiction. In nonhuman primates, different subareas of the orbitofrontal cortex project topographically to central and ventromedial parts of the striatum. Relatively little is known about the anatomical organization of the rat orbital cortex while there is a growing interest in this cortical area from a functional and behavioral point of view. The aim of the present neuroanatomical tracing study was to determine in rats the striatal target area of the projections of the orbital cortex as well as the topographical organization within these projections. To this end, anterograde tracers were injected in the different cytoarchitectonically distinct subareas of the orbital cortex. The results show that the individual orbital areas, i.e. medial orbital area, ventral orbital area, ventrolateral orbital area and lateral orbital area, project to central parts of the caudate-putamen, exhibiting a mediolateral and, to a lesser degree, rostrocaudal topographical arrangement. Orbital projections avoid the most dorsal, as well as rostral and caudal parts of the caudate-putamen. Terminal fields from cytoarchitectonically different areas show a considerable overlap. Superficial cortical layers project preferentially to the striatal matrix, deep layers to the patch compartment. The projections from the ventrolateral orbital area are strongest and occupy the most extensive striatal area. In addition to projections to the caudate-putamen, the ventrolateral, lateral and dorsolateral orbital areas have a scarce projection to the most lateral part of the nucleus accumbens shell in the ventral striatum. In contrast to nonhuman primates, the remainder of the rat nucleus accumbens is virtually free of orbital projections.     

Direction selectivity of simple cells in the primary visual cortex: comparison of two alternative mathematical models. II: Velocity tuning and response to moving bars

The two models of direction selectivity, presented in a previous paper, are used to investigate the response of simple cells to moving bars with different length, luminance and orientation. Most results agree with experimental data reported in the literature. However, a striking difference between the models is observable after a reduction in bar length. The antiphase model predicts that the optimal direction of movement for a short bar is equal to the optimal direction for a long bar, whereas the in-phase model predicts that the two optimal directions are orthogonal. This difference may allow experimental discrimination between the two models.     

Tactile impoverishment and sensorimotor restriction deteriorate the forepaw cutaneous map in the primary somatosensory cortex of adult rats

We investigated the effects of sensory deprivation on the forepaw representation in the primary somatosensory cortex (SI) in the adult rat. Cortical maps were constructed from high-resolution multiunit recordings of the response of layer IV neurons to somatosensory stimuli. The main features of the forepaw representation were described in terms of areal extent and topography of the cortical map, and sensory submodality, size, and location of the receptive field (RF) of small clusters of the cortical neurons. After being weaned, two groups of Long-Evans rats were housed in a standard (SE) or impoverished (IE) environment for 65–115 days. A third group of SE rats was subjected to severe sensorimotor restriction (SR) of one forepaw for 7 days or 14 days, by using a one-sleeved cast. A concomitant effect of unilateral forelimb immobilization was a forced use of the nonrestricted forelimb in postural balance. The maps of both forepaws were derived 24 h after the cast was removed and the animal was allowed normal limb use. In a fourth group, SE rats experienced a 7-day immobilization followed by symmetrical limb use for 7 days before we mapped the hemisphere contralateral to the casted limb. For the SE and IE rats, the total areal extent of the cutaneous forepaw representation was similar, but IE rats exhibited a significant expansion of cortical islets serving high-threshold, presumably noncutaneous inputs, which were included in the cutaneous maps. In addition, SI neurons of IE rats had greatly enlarged glabrous, but not hairy, skin RFs. For the SR rats, the areal extent of the cutaneous map of the casted forepaw decreased by about 50%, after both 7- and 14-day forelimb immobilization. Large cortical sectors presumed to be formerly activated by cutaneous inputs were driven by high-threshold inputs that disrupted the somatotopic representation of the forepaw skin surfaces. These ”emergent” representational sectors were topographically organized. By contrast, the areal extent and topography of the noncasted forepaw representation did not differ from those of SE rats. The size of glabrous RFs on the casted forepaw was similar to that of SE rats. On the contrary, glabrous RFs on the noncasted forepaw of SR rats were larger than those on their casted forepaw. The size of hairy RFs was not altered by the forelimb restriction. Interestingly, alteration of the somatotopic features of the casted forepaw map persisted after 7 days of symmetric use of the forelimbs. The present study demonstrates that continuous sensory experience is needed for the organizational features of SI maps to be maintained. Received: 22 February 1999 / Accepted: 8 July 1999     

The local domain for divergence of subcortical afferents to the striate and extrastriate visual cortex in the common marmoset (Callithrix jacchus): a multiple labelling study

Summary In the common marmoset (Callithrix jacchus), the cortical projection from the pulvinar and other diencephalic structures into the striate and prestriate cortex was investigated with various fluorescent retrograde tracers. Single cortical injections as well as multiple injections at distances of 1–2 mm with one tracer into an extended but coherent cortical region were applied. Fields with multiple injections were placed so that they touched each other (minimal distances 2 to 3 mm). Retrogradely labelled cells in the LGN and/or the pulvinar were arranged in coherent columns, volumes or slabs, but cell volumes resulting from neighbouring cortical injections overlapped at their border (for details of the thalamo-cortical topography see the companion paper Dick et al. (1991)). Double labelled cells (dl) were only found in the zones of overlap of the cell volumes labelled by the respective tracers. The relative number of dl-cells in these overlap zones was 6.2 ± 3.1%. The dl-frequency was the same in the various nuclei of the pulvinar and the LGN. In the main layers of LGN, dl-cells were found only in the overlap zone of two injection fields into area 17, but a few dl-cells were found in interlaminar cells after injections into area 17 and 18. Maximal cortical distances between injection fields which produced dl in the pulvinar, were 3 to exceptionally 4 mm but dl was highest at injection distances 2.5 mm and decreased sharply at wider distances. Such overlap zones were concerned with identical or overlapping regions of visual field representation in the cortex and probably also in the pulvinar. Although in individual experiments up to four different tracers were injected into different striate/prestriate regions, often embracing the same visual field representation, individual cells in the pulvinar showed dl from maximally only two tracers injected into neighbouring cortical regions. We conclude that dl in the posterior thalamic projection nuclei is determined essentially by cortical distance and thus reflects the local domain of branching of thalamo-cortical afferents. Pruning of such branches during development may further restrict bifurcating axons to identical visual field representations, but representation of identical visual field regions in different visual areas is not, per se, a sufficient condition for dl. It is not found if such regions are further apart from each other than the typical local domain of 2–3 mm, exceptionally up to 4 mm in one experiment after injections into area 17 and MT. Dl in the intralaminar nucleus CeL (5.0 ± 4.6%), the claustrum (5.4 ± 3.6%) and in the amygdala (5.7 ± 1.9%) was of the same order as in the pulvinar and LGN. In the hypothalamus around 10% and in the Nucleus basalis Meynert 15.8% of the cells labelled by visual cortical injections were double labelled. In all these extrathalamic regions dl was also restricted to overlap zones, but overlap of labelled fields in these nuclei was much wider and included the whole striate/prestriate cortex except for some topographical separation of striate and prestriate projection zones in the claustrum. Only in the Nucl. basalis Meynert and the hypothalamus some cells were labelled by three tracers.