Efferent projections of the pretectum in the cat

Summary Direct projections from the pretectum in the cat were investigated by means of the Nauta-Gygax and the Fink-Heimer method in an attempt to identify the morphological substrates subserving possible neural mechanisms involved in visual behaviour and reflexes.Degeneration in the diencephalon was found ipsilaterally in the nucleus limitans, lateral pulvinar nucleus, lateral posterior nucleus, lateral dorsal nucleus, dorsal and ventral lateral geniculate nuclei, centre medianparafascicular complex, central medial nucleus, paracentral nucleus, central lateral nucleus, ventroanterior and ventrolateral nuclear complex, zona incerta, H field of Forel and the reticular nucleus. The pretectal fibers projecting to the ventral lateral geniculate nucleus appeared to be topically organized.In the midbrain, the pretectal fibers were observed to terminate ipsilaterally within the superior colliculus, nucleus of Darkschewitsch, dorsolateral portion of the red nucleus, lateral terminal nucleus of the accessory optic tract and the reticular formation, and bilaterally within the central gray, interstitial nucleus of Cajal and the rostral portion of the nucleus of Edinger-Westphal. Degeneration in the superior colliculus was marked in laminae II, III and IV. The fibers arising from more anterior part of the pretectum appeared to be distributed more medially in laminae II and III.The pretectopontine fibers terminated ipsilaterally in the paramedial and the dorsolateral pontine nuclei as well as the reticular formation. In the inferior olivary complex, degeneration was found in caudal levels of the dorsal cap and -nucleus, and additionally in the rostral portion of the dorsal accessory olive.     

Development of horizontal intrinsic connections in cat striate cortex

Summary Intracortical injections of horseradish peroxidase conjugated with wheat-germ agglutinin (WGA-HRP) reveal a characteristic patchy staining pattern within the superficial layers of cat striate cortex. The patches consist of a dense accumulation of labeled neurons and axonal arborizations. We have investigated the tangential organization and the development of these intrinsic cortical connections by using a flat-mount preparation of area 17. The diameter of the patches varied from 200 to 400 m, the center-to-center distance ranged from 400 to 800 m, and the spread of patches extended further in the anterior-posterior than in the medial-lateral direction. The expression of these horizontal patchy connections is age- and experience-dependent. From ten days to six weeks of age patches are exuberant and on occasion fuse to beaded bands extending radially from the injection site. From 6 weeks onwards the number and the tangential spread of the patches decreases to one or two rows of isolated clusters. Long-term binocular deprivation disrupts this pattern of intrinsic connections nearly completely. We infer from these results that there is an inborn pattern of discrete horizontal connections in striate cortex which is shaped by visual experience and requires contour vision for its maintenance.     

Strabismus modifies intrinsic and inter-areal connections in cat area 18

The development of long-range horizontal connections depends on visual experience. Previous experiments have shown that in area 17 of strabismic but not in normal cats, horizontal fibers preferentially connect cell groups driven by the same eye indicating that fibers between coactive neurons are selectively stabilized. To test whether this is a general organizing principle of intracortical long-range circuitry we extended our analyses to both intrinsic horizontal connections within area 18 and to inter-areal connections between areas 17 and 18. To this end, we visualized the functional architecture of area 18 by intrinsic signal imaging. Horizontal circuitry was labeled by injecting fluorescent latex microspheres into functionally identified domains. Additionally, domains sharing the same ocular dominance as the neurons at the injection sites were visualized by 2-deoxyglucose autoradiography to allow comprehensive labeling of functional domains in regions far from the injection sites. Quantitative analyses revealed that in strabismic cats, 72% of the retrogradely labeled neurons in area 18 and 68% of the neurons in area 17 were located in the same ocular dominance domains as the injection sites. In contrast, these numbers were 52% and 54% in normal animals. These data show that experience modifies both intrinsic connections within area 18 and inter-areal projections from area 17 to area 18 as has been previously described for intrinsic and callosal connections in area 17. This provides further evidence for the hypothesis that the correlation of activity is a major selection criterion for the stabilization of neuronal circuits during postnatal development.     

Hypercomplex cell types in area 18 of the cat

Summary Single unit recording has revealed the same orientation sensitive cell classes in cat area 18 as are to be found in area 17. These include particularly the various types of hypercomplex cell belonging to the S, C, and B cell families.On leave from Clinica delle Malattie Nervose e Mentali, University of Messina, Policlinico Universitario, Messina, ItalyIn this paper the nomenclature of Henry (1977) will be used instead of the classical one of Hubel and Wiesel (1962, 1965) both because it avoids the hierarchical implications of the older terms and lends itself to the discrimination of new cell types     

Corticocortical connections of cat primary somatosensory cortex

Summary The organization of corticocortical connections in the representation of the forepaw in cat primary somatosensory cortex (SI) was studied following injections of various tracers into different cortical cytoarchitectonic areas. Small injections of horseradish peroxidase, wheat germ agglutinin-conjugated HRP, Phaseolus vulgaris leukoagglutinin, or fast blue were placed into the representation of the forepaw in areas 3b, 1, or 2. The positions of labeled neurons in SI and the surrounding cortical areas were plotted on flattened surface reconstructions to determine the organization of the corticocortical connections within SI. A strong, reciprocal projection linked the two forepaw representations which have been described in area 3b and the part of area 2 which lies in the anterior bank of the lateral ansate sulcus (see Iwamura and Tanaka 1978a, b). Dense projections also linked these areas with SII, as previously reported (Burton and Kopf 1984a). Additional projections to area 3b arose primarily from areas 3a and 1. Projections to area 2 were more widespread than those to area 3b, and arose from all other areas of SI as well as from areas 4 and 5a. All injections into SI tended to label groups of neurons which lay in mediolateral strips. Corticocortical projection neurons which were most heavily labeled by SI injections were pyramidal cells in layer III. Additional projections from area 2 to 3b, area 5a to 2, and SII to areas 2 and 3b arose from layer VI as well. Although neurons of layers III and VI were always the most densely labeled, large injections into SI labeled neurons in layers II and V as well.     

Influence of the presentation of remote visual stimuli on visual responses of cat area 17 and lateral suprasylvian area

Summary Single units were recorded extracellularly from area 17 and lateral suprasylvian area (LSSA) in curarized cats. Visual stimuli, usually a 10 ° black spot, were introduced abruptly in the visual field remote from the discharge area of a neuron's receptive field and moved at a speed of about 30 °/sec. The effect of these remote stimuli (S₂) on the response to a restricted visual stimulus (S₁) crossing the discharge area was studied.It was found that most units in area 17 were not affected by the presentation of remote stimuli, the remainder being either slightly facilitated or slightly inhibited. In contrast the LSSA neurons were usually inhibited by the presentation of S₂: this effect was strong, was present in all classes of LSSA neurons and was independent of the relative directions of movement of S₁ and S₂.On the basis of these data and those previously obtained from the superior colliculus it is concluded that the way the extrageniculate centres respond to a stimulus abruptly introduced in the visual field is substantially different from that of the striate cortex. Only in the extrageniculate centres a new stimulus, besides exciting the neurons which correspond to the position of the stimulus in the field, concomitantly decreases the responses of neurons located in positions of the visual field remote from that stimulus. Possible behavioral implications of the findings are discussed.     

Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex

Summary Small iontophoretic injections of the lectin, Phaseolus vulgaris leucoagglutinin (PHA-L), were made into different layers of the primary auditory cortex (AI) of cats. Injections in layer I labeled two types of morphologically distinct fibers in layer I as well as a smaller number of axons in layers II and III. Layer II injections labeled descending axons that produced a dense plexus of terminal fibers in layers I–III of both AI and adjacent auditory fields. Injections in layer III also labeled a dense plexus of axon collaterals at the junction of layers V and VI and labeled patches of terminal fibers in both AI and adjacent auditory fields. These were densest in layers I–III but usually extended into layers IV and V as well. The patches were partly formed by axon collaterals of layer III pyramidal cells that traveled for over 4 mm in the gray matter. Injections confined to layer IV labeled axons in all layers of the cortex but none of these axons appeared to reach the white matter. The axons spread laterally in layer IV and up into the superficial layers and ramified especially layer I. Injections in layers V and VI labeled axons in all layers of the cortex but these were densest in the deep layers where labeling was fairly homogeneous. In the upper layers the labeling was arranged in semi-discrete patches. Large injections involving layers I–III were studied in tangential sections. Between 3 and 8 patches of terminal labeling were observed in AI and these were mainly arranged in a band with its long axis aligned approximately in the dorsoventral direction. However dense patches of terminal labeling also occurred both anterior and posterior to the injection site. In selected experiments portions of the tonotopic map in AI were mapped by single unit recording and subsequently the map was related to patches of anterogradely labeled fibers that surrounded injections of PHA-L. Rows of dorsoventrally oriented patches were among cells with a similar best frequency to those in the injection site. However patches located anterior or posterior to the injection site were among cells with higher or lower best frequencies. Two injections of PHA-L close together produce different patterns of labeling. One of the injections usually produces one or more patches that has no correlate among the patches of fibers labeled by the adjacent injection. This is clearest when one of the injections is made with biotinylated PHA-L that can be visualized directly without the use of primary antibodies. Thus the intrinsic connections of AI arising from nearby cylinders of neurons are not homogenous and clusters of cells can be identified by their unique pattern of connections within AI.     

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.     

Efferent connections of the cingulate gyrus in the rhesus monkey

Summary Efferent cortical connections of the cingulate gyrus are investigated in rhesus monkey using autoradiographic technique. The results indicate that the rostralmost part of the cingulate gyrus (area 32) sends projections to the lateral prefrontal and midorbitofrontal cortex and to the rostral portion of the superior temporal gyrus. In contrast, the other two major subdivisions of the cingulate gyrus, areas 24 and 23, have widespread connections within the cortex. Area 24, for example, projects to the pre-motor region (areas 6 and 8), the fronto-orbital cortex (area 12), the rostral part of the inferior parietal lobule, the anterior insular cortex, the perirhinal area and the laterobasal nucleus of amygdala. Area 23, likewise, sends its connections to the dorsal prefrontal cortex (areas 9 and 10), the rostral orbital cortex (area 11), the parieto-temporal cortex (posterior part of the inferior parietal lobule and the superior temporal sulcus), the parahippocampal gyrus (areas TH and TF), the retrosplenial region and the presubiculum. It seems that the connections of the rostralmost part of the cingulate gyrus resemble the efferent cortical connectional patterns described for lateral prefrontal and orbito-frontal cortex, whereas the projections of areas 24 and 23 are directed to the neocortical, the paralimbic and the limbic areas.This study was in part supported by NIH Grant NS09211 and V.A. Research Project No. 6901Preliminary results of this investigation were presented in abstract form (Pandya et al. 1979)     

Efferent connections of the ectostriatal core. An anterograde tracer study

In the present study the efferent connections of the ectostriatal core were investigated with biotinylated dextran-amine anterograde tracer in the chicken using light microscopy. The efferents of the ectostriatal core were labelled anterogradely, but retrograde labelling was also observed, which displayed the afferents of the same region. The ectostriatal belt received a few thin varicose fibres; retrogradely labelled cells also appeared. The most extended projection ended in the surrounding neostriatum, which turned out to be reciprocally connected to the ectostriatal core. On the basis of these connections, the neostriatum is said to be an important visual associative center. Efferent fibres reached the motor areas as well. A significant projection entered the paleostriatum augmentatum, especially the ventral part. The paleostriatum primitivum also received a few fibres. The other motor center, the medial part of the anterior archistriatum, was proved to be directly connected to the ectostriatal core as well. Considering that the archistriatum is also connected indirectly to the Wulst, the movements are able to be guided by well processed visual information.     

Physiological studies on the feedback connection to the striate cortex from cortical areas 18 and 19 of the cat

Summary The functional characteristics of the feedback connections from areas 18 and 19 to area 17 in the cat have been examined with electrophysiological techniques. The experiments involved single unit recording in laminae 2 and 3 of area 17 while stimulating electrically a small region of area 18 or 19. It was found that a precise retinotopic correspondence between the sites of recording and stimulation was necessary before neurons of area 17 could be activated by electrical stimulation in extrastriate areas. Latencies were long compared to those obtained after stimulation of the optic radiation. The mean latency for orthodromic drive from area 19 was 10.4 ms and 6.1 ms from area 18, suggesting that the conduction velocities in these pathways are of the order of 1 m/s. The jitter of the latency after repeated orthodromic stimulation was often shorter than 0.3 ms, indicating that a large number of the sampled neurons received a direct drive from area 18 or from area 19. The functional properties of neurons driven from area 19 were different from those of cells driven from area 18. Thus, most striate neurons orthodromically driven from area 19 were of the S_H and S type whereas the cells activated by area 18 stimulation belonged to the C and B categories.     

Orientational influences of layer V of visual area 18 upon cells in layer V of area 17 in the cat cortex

We examined the orientation tuning curves of 86 cells located in layer V of area 17, before, during, and after focal blockade of a small (300-m diameter) region of near-retinotopic register in layer V of area 18 of quantitatively established orientation preference. Such focal blockade revealed three distinct populations of area 17 layer V cells-cells with decreased responses to stimuli of some orientations (21%), cells with increased responses to stimuli of some orientations (43%), and cells unaffected by the focal blockade (36%). These effects were clearcut, reproducible, and generally directly related to the known receptive field properties of the cell recorded in area 18 at the center of the zone of blockade. These effects were also analyzed in terms of alterations in orientation bandwidth in the cells in area 17 as a result of the blockade-bandwidth increases (22%) and decreases (24%) were found; however, these changes were essentially unrelated to the measured receptive field properties. Inhibitory and excitatory effects were most pronounced when the regions in areas 17 and 18 were of like ocular dominance and were of similar orientation preference. Inhibitory effects (suggesting a normally excitatory input) were most dependent upon the similarity of receptive fields; excitatory effects (suggesting a normally inhibitory input) were less heavily dependent.     

Descending connections between the superior olivary and cochlear nuclear complexes in the cat studied by autoradiographic and horseradish peroxidase methods

Summary The descending pathways from the superior olivary complex (SO) to the cochlear nuclear complex (CN) were investigated in 58 cats using labelled aminoacid and horseradish peroxidase transport techniques. Descending connections were found coursing bilaterally through the trapezoid body (TB) and ipsilaterally in the intermediate and dorsal acoustic striae. The dorsolateral periolivary nucleus (DLPO) sends fibres through both the intermediate and dorsal striae, which are joined by others from the lateral preolivary nucleus (LPO). Both the latter nucleus and the medial preolivary nucleus (MPO) give rise to a bilateral descending projection which traverses TB. The distribution of these descending pathways within CN is described (although the technique did not permit precise synaptic identification). The possible implications of these pathways for response patterns at the level of CN are discussed.     

Influence of layer V of area 18 of the cat visual cortex on responses of cells in layer V of area 17 to stimuli of high velocity

Focal blockade of restricted regions in layer V of area 18 was used to assess the contribution of this region to the responses to high-velocity stimuli of cells in retinotopically matched, layer V in area 17. In 40% of cases, blockade within area 18 revealed responses of area 17 cells to high-velocity stimuli to which they previously showed only poor responses. Stimulus specificity of the cells in area 17 was otherwise unaltered. All effects were reversible and repeatable. We suggest that a component of the output of layer V from area 18 normally suppresses the responses of retinotopically matched cells within area 17 to stimuli of high velocity, thereby enhancing the specificity of those cells to stimuli of low velocity     

The contribution of GABA-ergic neurons to horizontal intrinsic connections in upper layers of the cat's striate cortex

Summary The contribution of neurons containing -aminobutyric acid (GABA) to horizontal intrinsic projections in layers I–III of cat's striate cortex was investigated by combining GABA-immunohistochemistry with axonal tracing. After intracortical injections of Rhodamine-labelled latex microspheres Rhodamine-labelled neurons form patch- or bandlike aggregations (clusters) separated from each other by regions containing fewer, evenly distributed or no labelled neurons. Of the Rhodamine-labelled neurons about 5% display GABA-immunoreactive material (double labelled = DL-neurons). Approximately 70% of the DL-neurons occur at distances of less than 1 mm, and the remaining 30% at distances between 1 mm and 2.5 mm from the injection. About 60% of the DL-neurons reside within clusters and 40% are located in regions between clusters; the respective percentages of the Rhodamine labelled GABA-negative neurons are about 85 and 15. Considering their small number and their spatial distribution inhibitory interneurons seem to make only minor contributions to the clustered pattern of intrinsic connections. Our results demonstrate that the topographical organization of neurons giving origin to lateral inhibitory interactions in upper layers of cat's striate cortex is different from that of neurons mediating excitatory functions.     

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.     

Comparison between habituation of the cat vestibulo-ocular reflex by velocity steps and sinusoidal vestibular stimulation in the dark

Changes in the horizontal vestibulo-ocular reflex (VOR) in darkness were investigated in naive cats during: (1) repeated sessions of angular velocity steps, (2) one continuous 1-h session of sinusoidal oscillations at 0.01, 0.02, 0.04, or 0.12 Hz, and (3) repeated sessions of 1-h sinusoidal oscillations at 0.02 and 0.04 Hz. Before and after each vestibular training, the VOR response parameters elicited by both velocity steps and sinusoidal oscillations were measured in order to evaluate the transfer of habituation from one stimulus to the other. After training with velocity steps, the amplitude and duration of the VOR to velocity steps decreased by about 67% and 52%, respectively. This vestibular habituation transferred to the VOR response generated by sinusoidal oscillations, since a decrease in VOR gain was observed at 0.02 and 0.04 Hz, and an increase in phase lead was observed at 0.02, 0.04, and 0.08 Hz. After 1 h exposure to sinusoidal oscillations, the VOR gain was only reduced by 21-28%, whereas VOR phase lead decreased. The same changes were observed during subsequent sessions, with no retention of the response decrements from one session to the next. At the end of sinusoidal training, the amplitude of the VOR generated by velocity steps was slightly altered. After sinusoidal training, the weak changes in the VOR gain accompanied by a decrease in the VOR phase lead, and the absence of retention of these effects from one session to the next, suggest these changes are not characteristics of a vestibular habituation. Previous reports of vestibular habituation induced by repeated sinusoidal oscillations may be confounded by the fact that the angular velocity steps used for quantifying the effects may have been responsible for this habituation.     

A comparison of magnification functions in area 19 and the lateral suprasylvian visual area in the cat

A retinotopic map can be described by a magnification function that relates magnification factor to visual field eccentricity. Magnification factor for primary visual cortex (VI) in both the cat and the macaque monkey is directly proportional to retinal ganglion cell density. However, among those extrastriate areas for which a magnification function has been described, this is often not the case. Deviations from the pattern established in V1 are of considerable interest because they may provide insight into an extrastriate area's role in visual processing. The present study explored the magnification function for the lateral suprasylvian area (LS) in the cat. Because of its complex retinotopic organization, magnification was calculated indirectly using the known magnification function for area 19. Small tracer injections were made in area 17, and the extent of anterograde label in LS and in area 19 was measured. Using the ratio of cortical area labeled in LS to that in area 19, and the known magnification factor for area 19 at the corresponding retinotopic location, we were able to calculate magnification factor for LS. We found that the magnification function for LS differed substantially from that for area 19: central visual field was expanded, and peripheral field compressed in LS compared with area 19. Additionally, we found that the lower vertical meridian's representation was compressed relative to that of the horizontal meridian. We also examined receptive field size in areas 17, 19, and LS and found that, for all three areas, receptive field size was inversely proportional to magnification factor.     

The distribution of degenerating axons after small lesions in the intact and isolated visual cortex of the cat

Summary The extent of the spread of axonal degeneration was investigated in the visual cortex of the cat after making small lesions restricted to the grey matter. Two series of experiments were undertaken. In the first, normal adult cats were used, and in the second, the cortex of the postlateral gyrus was isolated from its extrinsic afferents by surgical undercutting 3 months before making the lesions. The results were similar in the two series in most respects. 1. Horizontal fibres extended in considerable numbers for some 500 m from the lesion, mainly in layers I, III/IV and V, a few reaching 2–3 mm. These fibres were better seen in the intact than in the isolated cortex. Their spread was usually asymmetrical, being greater posteromedially than anterolaterally. 2. Oblique axons ran downwards from the middle layers into layers V and VI, or upwards into layers I and II. 3. Axons arising from layers II to VI descended vertically into the white matter. Degeneration patterns after lesions in areas 17 and 18 were compared.