Identification of Eye-Specific Domains and Their Relation to Callosal Connections in Primary Visual Cortex of Long Evans Rats.

Ocular dominance columns (ODCs) exist in many primates and carnivores, but it is believed that they do not exist in rodents. Using a combination of transneuronal tracing, in situ hybridization for Zif268 and electrophysiological recordings, we show that inputs from both eyes are largely segregated in the binocular region of V1 in Long Evans rats. We also show that, interposed between this binocular region and the lateral border of V1, there lies a strip of cortex that is strongly dominated by the contralateral eye. Finally, we show that callosal connections colocalize primarily with ipsilateral eye domains in the binocular region and with contralateral eye input in the lateral cortical strip, mirroring the relationship between patchy callosal connections and specific sets of ODCs described previously in the cat. Our results suggest that development of cortical modular architecture is more conserved among rodents, carnivores, and primates than previously thought.

Role of retinal input on the development of striate-extrastriate patterns of connections in the rat.

Previous studies have shown that retinal input plays an important role in the development of interhemispheric callosal connections, but little is known about the role retinal input plays on the development of ipsilateral striate-extrastriate connections and the interplay that might exist between developing ipsilateral and callosal pathways. We analyzed the effects of bilateral enucleation performed at different ages on both the distribution of extrastriate projections originating from restricted loci in medial, acallosal striate cortex, and the overall pattern of callosal connections revealed following multiple tracer injections. As in normal rats, striate-extrastriate projections in rats enucleated at birth consisted of multiple, well-defined fields that were largely confined to acallosal regions throughout extrastriate cortex. However, these projections were highly irregular and variable, and they tended to occupy correspondingly anomalous and variable acallosal regions. Moreover, area 17, but not area 18a, was smaller in enucleates compared to controls, resulting in an increase in the divergence of striate projections. Anomalies in patterns of striate-extrastriate projections were not observed in rats enucleated at postnatal day (P)6, although the size of area 17 was still reduced in these rats. These results indicate that the critical period during which the eyes influence the development of striate-extrastriate, but not the size of striate cortex, ends by P6. Finally, enucleation did not change the time course and definition of the initial invasion of axons into gray matter, suggesting that highly variable striate projections patterns do not result from anomalous pruning of exuberant distributions of 17-18a fibers in gray matter.

Retinal input influences the size and corticocortical connectivity of visual cortex during postnatal development in the ferret.

Retinal input plays an important role in the specification of topographically organized circuits and neuronal response properties, but the mechanism and timing of this effect is not known in most species. A system that shows dramatic dependence on retinal influences is the interhemispheric connection through the corpus callosum. Using ferrets, we analyzed the extent to which development of the visual callosal pattern depends on retinal influences, and explored the period during which these influences are required for normal pattern formation. We studied the mature callosal patterns in normal ferrets and in ferrets bilaterally enucleated (BE) at postnatal day 7 (P7) or P20. Callosal patterns were revealed in tangential sections from unfolded and flattened brains following multiple injections of horseradish peroxidase in the opposite hemisphere. We also estimated the effect of enucleation on the surface areas of striate and extrastriate visual cortex by using magnetic resonance imaging (MRI) data from intact brains. In BEP7 ferrets we found that the pattern of callosal connections was highly anomalous and the sizes of both striate and extrastriate visual cortex were significantly reduced. In contrast, enucleation at P20 had no significant effect on the callosal pattern, but it still caused a reduction in the size of striate and extrastriate visual cortex. Finally, retinal deafferentation had no significant effect on the number of visual callosal neurons. These results indicate that the critical period during which the eyes influence the development of callosal patterns, but not the size of visual cortex, ends by P20 in the ferret.

Neonatal enucleation during a critical period reduces the precision of cortico-cortical projections in visual cortex.

Previous studies have reported that intrahemispheric connections between area 17 (V1, striate cortex) and other cortical visual areas are not point-to-point, but instead have some degree of convergence and divergence. Many pathological conditions can interfere with the normal development of patterns of cortico-cortical connections, but there is little information regarding whether or not early pathological insults can also induce permanent changes in the convergence and divergence of cortical connections. Obtaining this information is important because loss of precision in neural projections can contribute to functional deficits and behavioral impairment. In the present study we investigated whether retinal input is required for the development of normal values of convergence and divergence in the visual callosal pathway. We found that enucleation performed at birth induced significant increases in convergence and divergence compared to control animals. In contrast, values of convergence and divergence in rats enucleated at postnatal day 7 (P7) were similar to those in controls. Previous studies have shown that retinal input during the first postnatal week is required for the specification of the overall distribution and internal topography of visual callosal pathways. Our present results therefore extend these previous finding by showing that retinal input during the first postnatal week also specifies the precision of cortico-cortical projections. These findings raise the possibility that the precision of neural connections may be reduced in other pathological conditions that affect early development of neural connections.

Retinal influences induce bidirectional changes in the kinetics of N-methyl-D-aspartate receptor-mediated responses in striate cortex cells during postnatal development.

Development of the visual callosal projection in rodents goes through an early critical period, from postnatal day (P) 4 to P6, during which retinal input specifies the blueprint for normal topographic connections, and a subsequent period of progressive pathway maturation that is largely complete by the time the eyes open, around P13. This study tests the hypothesis that these developmental stages correlate with age-related changes in the kinetics of synaptic responses mediated by the N-methyl-D-aspartate subclass of glutamate receptors (NMDARs). We used an in vitro slice preparation to perform whole-cell recordings from retrogradely-labeled visual callosal cells, as well from cortical cells with unknown projections. We analyzed age-related changes in the decay time constant of evoked as well as spontaneous excitatory postsynaptic currents mediated by N-methyl-D-aspartate subclass of glutamate receptors (NMDAR-EPSCs) in slices from normal pups and pups enucleated at different postnatal ages. In normal pups we found that the decay time constant of NMDAR-EPSCs increases starting at about P6 and decreases by about P13. In contrast, these changes were not observed in rats enucleated at birth. However, by delaying the age at which enucleation was performed we found that the presence of the eyes until P6, but not until P4, is sufficient for inducing slow NMDAR-EPSC kinetics during the second postnatal week, as observed in normal pups. These results provide evidence that the eyes exert a bidirectional effect on the kinetics of NMDARs: during a P4-P6 critical period, retinal influences induce processes that slow down the kinetics of NMDAR-EPSCs, while, near the age of eye opening, retinal input induces a sudden acceleration of NMDAR-EPSC kinetics. These findings suggest that the retinally-driven processes that specify normal callosal topography during the P4-P6 time window also induce an increase in the decay time constant of NMDAR-EPSCs. This increase in response kinetics may play an important role in the maturation of cortical topographic maps after P6. Using ifenprodil, a noncompetitive NR2B-selective blocker, we obtained evidence that although NR1/NR2B diheteromeric receptors contribute to evoked synaptic responses in both normal and enucleated animals, they are not primarily responsible for either the age-related changes in the kinetics of NMDAR-mediated responses, or the effects that bilateral enucleation has on the kinetics of NMDAR-EPSCs.

The retinal input to calbindin-D28k-defined subdivisions in macaque inferior pulvinar.

Several studies have provided evidence for direct retinal input to the pulvinar of macaques monkeys, but there is no general agreement regarding the extent of this projection. Moreover, it is not known how retinal input correlates with chemoarchitectonic subdivisions recently recognized within the large, classical divisions of the pulvinar. The potential implications of this correlation have become more evident after reports that chemoarchitectonic subdivisions of the inferior pulvinar (PI) have specific patterns of connections with cortical visual areas. We have therefore re-examined the retino-PI projection using intraocular injections of horseradish peroxides, and correlated it with pulvinar subdivisions revealed using an antibody for calbindin-D28k. Retinal projections were found preferentially within the medial subdivision of the PI, with some involvement of the posterior and central calbindin-D28k defined subdivisions.

Callosal connections correlate preferentially with ipsilateral cortical domains in cat areas 17 and 18, and with contralateral domains in the 17/18 transition zone.

Previous studies have shown that the distribution of callosal connections in the 17/18 callosal zone of the cat is patchy at a small scale, but the mechanisms that determine this periodic pattern remain unclear. The present study investigated this issue by correlating the distribution of retrogradely labeled callosal cells with the underlying patterns of ocular dominance columns (ODCs) revealed transneuronally after intraocular injections of wheat germ agglutinin-horseradish peroxidase. The density of labeled callosal cells was found to vary significantly between adjacent territories dominated by different eyes, indicating that the distribution of callosal cells is significantly biased toward domains that are eye specific. Moreover, callosal connections relate to the pattern of ODCs in a rather unique way: callosal cells correlate preferentially with contralateral ODCs within the 17/18 transition zone (TZ), and with ipsilateral ODCs in regions of areas 17 and 18 located outside the TZ. Similar results were obtained in cats raised with strabismus, indicating that the overlap between right and left ODCs present in normal cats does not influence the correlation between callosal neurons and ODCs. The results are consistent with the hypothesis that callosal linkages are stabilized during development by interhemispheric correlated activity driven by bilateral projections from temporal retina. It is proposed that developmental constraints imposed by both this retinally driven mechanism and the pattern of ODCs are likely to determine not only the association of callosal clusters with specific sets of ODCs, but also important aspects of the functional characteristics of the callosal pathway in cat striate cortex.

Organization of callosal linkages in visual area V2 of macaque monkey.

In visual area V2 of the macaque monkey callosal cells accumulate in finger-like bands that extend 7-8 mm from the V1/V2 border, or approximately half the width of area V2. The present study investigated whether or not callosal connections in area V2 link loci that are located at the same distance from the V1/V2 border in both hemispheres. We analyzed the patterns of retrograde labeling in V2 resulting from restricted injections of fluorescent tracers placed at different distances from the V1/V2 border in contralateral area V2. The results show that varying the distance of V2 tracer injections from the V1/V2 border led to a corresponding variation in the location of labeled callosal cells in contralateral V2. Injections into V2 placed on or close to the V1 border produced labeled cells that accumulated on or close to the V1 border in contralateral V2, whereas injections into V2 placed away from the V1 border produced labeled cells that accumulated mainly away from the V1 border. These results provide evidence that callosal fibers in V2 preferentially link loci that are located at similar distances from the V1/V2 border in both hemispheres. Relating this connectivity pattern to the topographic map of V2 suggests that callosal fibers link topographically mirror-symmetrical regions of V2, i.e., callosal fibers near the V1/V2 border interconnect areas representing visual fields on, or close to, the vertical meridian, whereas callosal connections from regions away from the V1/V2 border interconnect visuotopically mismatched visual fields that extend onto opposite hemifields.

A morphological anomaly of the dorsal lateral geniculate nucleus in Macaca fascicularis.

In the present report we describe a morphological anomaly of the thalamus. In three macaque monkeys (Macaca fascicularis), we observed up to five finger-like protrusions that emanated from the posterior pole of the dorsal lateral geniculate nucleus (LGN) and extended posteriorly between the lateral pulvinar and reticular nucleus of the thalamus. These anomalous fingers measured up to 1.7 mm in length and contained dense accumulations of neurons and glia. The fingers received a direct retinal input from the contralateral eye indicating that they were part of the LGN rather than of other adjacent thalamic nuclei. In order to determine with which subcompartment(s) of the LGN the fingers were associated (parvocellular, magnocellular, or intercalated layers), we examined the immunochemical properties and size of neurons in the fingers and LGN subcompartments. We concluded that the fingers were not associated with the intercalated layers, since neurons in the fingers did not stain with an antibody to calbindin-D28k, whereas intercalated neurons stained intensely with this antibody. In addition, neurons located in the fingers were significantly smaller than those found in the magnocellular layers but were not significantly different in size from neurons in the parvocellular layers. We therefore consider that the fingers are an anomaly of the parvocellular subcompartment of the LGN. Interestingly, in two of the three cases with anomalous fingers, we also observed subsidiary parvocellular laminae, suggesting that these two anomalies were related. In five additional animals, however, we observed subsidiary parvocellular laminae without anomalous fingers. Thus, if there are common mechanisms underlying the development of both anomalous fingers and subsidiary layers, our data indicate that they do not always result in the concomitant expression of both anomalies.

The global pattern of cytochrome oxidase stripes in visual area V2 of the macaque monkey.

In primate visual area V2, histochemical staining for cytochrome oxidase (CO) reveals a tripartite pattern of densely labeled thick and thin stripes separated by pale interstripes. This modularity is believed to be related to functionally distinct processing streams that course through the hierarchy of visual areas. Here, we studied the overall pattern of CO stripes in V2 of the macaque monkey, using tissue that had been physically unfolded and flattened prior to histological sectioning. CO stripes were identified on the basis of their physical dimensions and on their differential immunoreactivity for the monoclonal antibody Cat-301. We observed several distinctive features of compartmental organization in V2. The most prominent was a dorso-ventral asymmetry in the stripe pattern, occurring in the majority of cases studied. In dorsal V2, most stripes measure approximately 10 mm in length and run roughly orthogonal to both the posterior and anterior borders of V2. In contrast, many stripes in ventral V2 have a curved or oblique trajectory, and some extend up to 20 mm in length. Stripes following a curved trajectory often become nearly parallel to the anterior border of V2. These differences imply an asymmetry in how the visual field maps onto dorsal versus ventral stripes. Occasionally, thin stripes fail to alternate with thick stripes but instead occur next to one other, separated only by interstripes. In three most complete reconstructions, we found that unfolded V2 is approximately 110 mm in length, approximately 900 mm2 in surface area, and that it contains approximately 28 complete sets of stripes (one thick, one thin and two interstripes), yielding an average of approximately 4 mm per set of stripes. The maximum width of ventral V2 (13-14 mm) exceeds that of dorsal V2 (10 mm), and there is a consistent narrowing of V2 in the region of foveal representation (3-5 mm).

Distribution of neurons projecting to the superior colliculus correlates with thick cytochrome oxidase stripes in macaque visual area V2.

In visual area V2 of macaque monkeys, cytochrome oxidase (CO) histochemistry reveals a pattern of alternating densely labeled thick and thin stripe compartments and lightly labeled interstripe compartments. This modular organization has been associated with functionally separate pathways in the visual system. We examined this idea further by comparing the pattern of CO stripes with the distribution of neurons in V2 that project to the superior colliculus. Visually evoked activity in the superior colliculus is known to be greatly reduced by blocking magnocellular but not parvocellular layers of the lateral geniculate nucleus (LGN). From previous evidence that V2 thick stripes are closely associated with the magnocellular LGN pathway, we predicted that a significant proportion of V2 neurons projecting to the superior colliculus would reside in the thick stripes. To test this prediction, the tangential distribution of retrogradely labeled corticotectal cells in V2 was compared with the pattern of CO stripes. We found that neurons projecting to the superior colliculus accumulated preferentially into band-like clusters that were in alignment with alternate CO dense stripes. These stripes were identified as thick stripes on the basis of their physical appearance and/or by their affinity to the monoclonal antibody Cat-301. A significantly smaller proportion of labeled cells was observed in thin and interstripe compartments. These data provide further evidence that the spatial distribution of subcortically projecting neurons can correlate with the internal modular organization of visual areas. Moreover, they support the notion that CO compartments in V2 are associated with functionally different pathways.

The distribution of callosal connections correlates with the pattern of cytochrome oxidase stripes in visual area V2 of macaque monkeys.

In visual area V2 of monkeys, cytochrome oxidase (CO) histochemistry reveals a system of stripe-like subregions where densely labeled thick and thin stripes and pale interstripes can be recognized. Several lines of evidence suggest that CO stripe-like subregions are associated with functional streams in the visual cortex. In the present study, the distribution of retrogradely labeled callosal cells in V2 and the pattern of CO staining were correlated using tangential sections through the flattened cortex. Spectral and coherency analyses of the callosal and CO patterns were performed to assess quantitatively the degree of spatial correlation between these two patterns. The results showed that labeled callosal cells accumulated along the V1/V2 border and in finger-like bands that protruded up to 7-8 mm into V2. These callosal bands were in register with thick and thin CO stripes, with relatively few labeled callosal cells found in interstripe regions. This finding supports the notion that the distribution of callosal connections in the visual cortex is dictated not only by the topography of visual areas, but also by the arrangement of cortical functional streams. Further, these results extend to interhemispheric pathways the notion of functional specificity currently associated mainly with some visual intrahemispheric pathways.

The distribution of corticotectal projection neurons correlates with the interblob compartment in macaque striate cortex.

While much attention has been given to the correlation between cytochrome-oxidase (CO) compartments and patterns of cortico-cortical projections originating from supragranular layers in the striate cortex, little is known in this regard about patterns of cortico-subcortical projections originating from infragranular cortex. We studied the tangential distribution of the striate cortex neurons projecting to the superior colliculus and used two approaches to analyze the relationship of this distribution to the arrangement of CO "blobs." First, chi-square analysis indicated that significantly fewer labeled neurons were found within the CO blob compartment than the number expected for a random distribution. Second, spatial cross-correlation analysis--which circumvents the inherent subjectivity of delineating blob boundaries--revealed an area around blob centers in which there was a decreased probability of encountering labeled cells. The size of this area compared well with that of our outlines of CO blobs. We conclude that corticotectal projection neurons in the striate cortex are distributed preferentially within the interblob compartment of the infragranular striate cortex. These results demonstrate that the spatial distribution of cortico-subcortical projection neurons within infragranular cortex can correlate with the CO architecture of the primary visual cortex.

Non-mirror-symmetric patterns of callosal linkages in areas 17 and 18 in cat visual cortex.

In the cat, callosal connections in area 17 are largely confined to a 5-6-mm-wide strip at the 17/18 border. It is commonly thought that callosal fibers extending from between the 17/18 border regions interconnect loci that are mirror-symmetric with respect to the midline of the brain, but this idea has not been tested experimentally. The present study examined the organization of callosal linkages in the 17/18 border region of normal adult cats by analyzing the patterns of connections revealed in one hemisphere after small injections of different fluorescent tracers into the opposite 17/18 callosal region. The location of the injection sites within areas 17 and 18 was assessed by examining architectonic data and by inspecting the labeling pattern in the ipsilateral visual thalamus. Area 17 and 18 were separated by a 1-1.5-mm-wide zone of cytoarchitectonic transition rather than by a sharp border. The results show that, in general, callosal fibers interconnect loci that are not mirror-symmetric with respect to the midline. Thus, area 17 injections placed nearly 3 mm away from the 17/18 transition zone produced discrete labeled areas located preferentially within the contralateral 17/18 transition zone. However, when the injection site was within the 17/18 transition zone, labeled cells were found primarily medial and lateral to, but not within, the 17/18 transition zone in the contralateral hemisphere. Previous studies have indicated that the 17/18 transition zone contains a representation of a strip of the ipsilateral visual field. Comparison of the retinotopy of the 17/18 border region with the mirror-reversed pattern of callosal linkages found in the present study suggests that callosal fibers link points that are in retinotopic correspondence in both hemispheres.

Distribution of visual callosal neurons in normal and strabismic cats.

It has been suggested that synchronous activation of cortical loci in the two cerebral hemispheres during development leads to the stabilization of juvenile callosal connections in some areas of the visual cortex. One way in which loci in opposite hemispheres can be synchronously activated is if they receive signals generated by the same stimulus viewed through different eyes. These ideas lead to the prediction that shifts in the cortical representation of the visual field caused by misalignment of the visual axes (strabismus) should change the width of the callosal zone in the striate cortex. We tested this prediction by using quantitative techniques to compare the tangential distribution of callosal neurons in the striate cortex of strabismic cats to that in normally reared cats. Animals were rendered strabismic surgically at 8-10 days of age and were allowed to survive a minimum of 18 weeks, at which time multiple intracortical injections of the tracer horseradish peroxidase (HRP) were used to reveal the distribution of callosally projecting cells in the contralateral striate cortex. HRP-labeled cells were counted in coronal sections, and data from four animals with divergent strabismus (exotropia) and four with convergent strabismus (esotropia) were compared to those from four normally reared animals. Although our data from strabismic cats do not differ markedly from those reported previously, we find that the distribution of callosal cells in the striate cortex of these cats does not differ significantly from that in our normally reared control cats. These results do not bear out the prediction that surgically shifting the visual axes leads to stabilization of juvenile callosal axons in anomalous places within the striate cortex.

The callosal pattern in striate cortex is more patchy in monocularly enucleated albino than pigmented rats.

We investigated the effect of neonatal monocular enucleation on the pattern of interhemispheric connections through the corpus callosum in occipital cortex of pigmented and albino rats. Callosal connections were revealed in tangential sections through the flattened cortex following multiple injections of horseradish peroxidase into the opposite hemisphere. In pigmented rats, we found that monocular enucleation induces the development of an anomalous band-like accumulation of callosal connections in middle portions of striate cortex in the hemisphere ipsilateral to the remaining eye, as reported previously. In one-eyed albino rats, we also found callosal connections anomalously placed in middle portions of striate cortex, but they tended to form several patches of labeling rather than a single continuous band as in pigmented rats. Densitometric analysis of the callosal patterns revealed that this difference between rat strains was statistically significant. The increased patchiness in the callosal pattern of one-eyed albino rats may reflect differences in the ipsilateral retinal projections in albino versus pigmented rats.

Overall pattern of callosal connections in visual cortex of normal and enucleated cats.

The effect of neonatal bilateral enucleation on the overall distribution of callosal connections in striate and extrastriate visual cortex of the cat was studied using tangential sections from the physically unfolded and flattened cortex. Callosal neurons were labeled by administering the anatomical tracer horseradish peroxidase directly to the transected corpus callosum. The pattern of callosal connections in binocularly enucleated cats showed both consistent differences and consistent similarities with the pattern in normal cats. In agreement with previous studies, it was found that callosal labeling at the 17/18 border of enucleated cats was considerably sparser than in normal cats. Moreover, we found that the strip containing the majority of labeled cells at the 17/18 border was narrower than in normal cats. In both normal and enucleated cats, scattered cells were distributed on either side of the 17/18 callosal strip, well into areas 17 and 18. In much of extrastriate cortex, the pattern of callosal connectivity in enucleated cats looked surprisingly normal. Details of the callosal pattern that were consistently found in normal cats could also be recognized in binocularly enucleated cats, such as two to four bridges of labeling spanning areas 18 and 19. Also, four zones that were free of callosal connectivity in area 7, on the banks of the suprasylvian sulcus, and in the posterior suprasylvian sulcus were found in both normal and enucleated cats. Finally, as in normal cats, dense cell labeling occurred on the crown of the suprasylvian gyrus at its posterior end, from which it extended laterally across both banks of the suprasylvian sulcus and into the fundus of this sulcus. The results of this study suggest that, although the stabilization of callosal connections at the 17/18 border region appears to depend on visual input, this input plays a less prominent role in the stabilization of callosal connections in extrastriate visual cortex.

Occipital cortico-pyramidal projection in hypothyroid rats.

It is well established that the progressive disappearance of a transient occipito-spinal projection in neonatal rats involves the selective elimination of axonal collaterals. We studied whether the development of the occipito-spinal pathway was affected by hypothyroidism induced by treatment with the goitrogen 6n-propyl-2-thiouracil (PTU) beginning prenatally. Using both anterograde (biocytin and Dil) and retrograde (horseradish peroxidase and Fast Blue) tracing techniques in adult hypothyroid rats, we found that many cells with projections into the pyramidal tract are present in regions of visual cortex that are devoid of such cells in normal adult rats. Our results suggest that hypothyroidism induced by PTU treatment leads to the maintenance of occipito-spinal projections that are normally transient.

Effects of neonatal enucleation on the organization of callosal linkages in striate cortex of the rat.

Lewis and Olavarria ([1995] J. Comp. Neurol. 361:119-137) showed that the mediolateral organization of callosal linkages differs markedly between medial and lateral regions of striate cortex in the rat. Thus, callosal fibers originating from medial regions of striate cortex interconnect loci that are mirror-symmetric with respect to the midsagittal plane. In contrast, fibers from lateral regions of striate cortex show a reversed pattern of connections: tracer injections into the 17/18a border produce retrograde cell labeling in regions medial to the contralateral 17/18a border, whereas injections placed somewhat medial to the 17/18a border label cells located at the contralateral 17/18a border. Based on the interpretation that callosal fibers from lateral striate cortex connect retinotopically corresponding loci (Lewis and Olavarria [1995] J. Comp. Neurol. 361:119-137) we propose here that the development of the reversed pattern of connections in lateral portions of striate cortex is guided by activity-dependent cues originating from spontaneously active ganglion cells in temporal retina. In the present study we have attempted to falsify this hypothesis by investigating the effects of neonatal bilateral enucleation on the organization of callosal linkages in striate cortex of the rat. Once enucleated rats reached adulthood, we studied the mediolateral organization of callosal connections by placing small injections of different fluorescent tracers into different loci within medial and lateral striate cortex. The analysis of the distribution of retrogradely labeled callosal cells indicated that connections from lateral portions of striate cortex were no longer organized in a reversed fashion, rather, they resembled the mirror image pattern normally found in the medial callosal region, i.e., injections at the 17/18a border produced labeled cells at the opposite 17/18a border, whereas injections into slightly more medial regions produced labeled cells in the opposite, mirror-symmetric location. In addition, we found that enucleation does not alter the organization of callosal linkages in medial portions of striate cortex. Thus, by showing that enucleation significantly changes the pattern of connections from lateral portions of striate cortex, the present study does not falsify, but rather strengthens the hypothesis that interhemispheric correlated activity driven from the temporal retinal crescent guides the normal development of reversed callosal linkages in lateral portions of rat striate cortex. Furthermore, the present study shows that, in the absence of the eyes, the pattern of callosal linkages in lateral portions of striate cortex resembles the mirror image pattern normally found only in medial striate cortex.

Two rules for callosal connectivity in striate cortex of the rat.

In the rat, callosal cells occupy lateral as well as medial portions of striate cortex. In the region of the border between areas 17 and 18, which contains a representation of the vertical meridian of the visual field, cells projecting through the corpus callosum are concentrated throughout the depth of the cortex. In contrast, in medial portion of striate cortex, where peripheral portions of the visual field are represented, callosal cells are preferentially found in infragranular layers. These differences in topography and laminar distribution suggest that these callosal regions, referred to as medial and lateral callosal regions in the present study, subserve different functions. We explored this possibility by analyzing the patterns of callosal linkages in these two callosal regions. We charted the location of retrogradely labeled cells within striate cortex of one hemisphere after placing restricted injections of one or more fluorescent tracers into selected sites in the contralateral striate cortex. We found the medial and lateral callosal regions have distinctly different topographic organizations. Injections into medial striate cortex of one hemisphere produced labeled cells predominantly in mirror-symmetric loci in medial portions of contralateral striate cortex. The arrangement of these connections suggests that they mediate direct interactions between cortical regions representing visual fields located symmetrically on opposite sides of the vertical meridian of the visual field. In contrast, the mapping in the lateral callosal region is reversed: injections into the 17/18a border produced labeled fields located medial to the contralateral 17/18a border, while injections slightly medial to the 17/18a border produced labeled fields located at the contralateral 17/18a border.(ABSTRACT TRUNCATED AT 250 WORDS)