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Organization of geniculocortical projections in turtles: isoazimuth lamellae in the visual cortex.

The projection from the dorsal lateral geniculate complex to the visual cortex in Pseudemys and Chrysemys turtles was examined by using the anterograde transport of horseradish peroxidase (HRP) in vitro and the retrograde transport of HRP in vivo. In vitro HRP injections into the lateral forebrain bundle were used to fill geniculocortical axons anterogradely, which were then analyzed in cortical wholemount preparations. Geniculocortical axons gain access to the visual cortex along its entire rostral-caudal extent. They course in slightly curved trajectories for up to 2 mm from the lateral edge of the cortex through both the lateral (or pallial thickening) and medial parts of Desan's cortical area D2. Single axons are of fine caliber. They tend to cross each other and sometimes branch in the pallial thickening, but are generally unbranched in the medial part of D2. They bear small, fusiform varicosities at irregular intervals along their lengths. Although axons show small variations in the number of varicosities per 100 microns segment, no consistent variation in varicosity number as a function of distance could be detected. These results indicate that geniculocortical axons project to the visual cortex in an orderly pattern. The retrograde transport experiments provide some clue as to the significance of this pattern. Small, ionotophoretic injections of HRP in the visual cortex retrogradely labeled neurons in the dorsal lateral geniculate complex. Injections in the rostral visual cortex retrogradely labeled neurons in the caudal pole of the geniculate complex. Injections at progressively more caudal loci within the visual cortex labeled neurons at progressively more rostral loci within the geniculate complex. Thus, there is a representation of the rostral-caudal axis of the geniculate complex along the caudal-rostral axis of the visual cortex. Consistent with the anterograde transport experiments that showed individual geniculocortical axons coursing through both lateral and medial parts of the visual cortex, HRP injections restricted to the medial edge of the visual cortex retrogradely labeled neurons along the entire dorsal-ventral axis of the geniculate complex at the appropriate rostral-caudal position. The neurophysiological studies of Mazurskaya ('72: J. Evol. Biochem. Physiol. 8:550-555; respond to a small, moving stimulus anywhere in visual space, implying a convergence of inputs from all points in visual space somewhere along the retinogeniculocortical pathway. The experiments reported here suggest a convergence in the geniculocortical projections of information along the vertical meridians, or azimuth lines, of visual space onto neurons lying along lateral to medial transects through the visual cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Synaptic organization of cortico-cortical connections from the primary visual cortex to the posteromedial lateral suprasylvian visual area in the cat.

The synaptic organization of the projection from the cat striate visual cortex to the posteromedial lateral suprasylvian cortical area (PMLS) was examined. The anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L) was iontophorectically delivered into area 17, and anterogradely labeled fibers were revealed in PMLS by means of an immunocytochemical detection method. Most axons and presumptive terminal swellings were found in layers III and IV. The neuronal elements (n = 190) that were postsynaptic to anterogradely labeled boutons were quantitatively analyzed. All anterogradely labeled cortico-cortical boutons (n = 182) established type 1 synapses. The results show that 83% of the postsynaptic targets were dendritic spines, probably belonging to pyramidal cells. Dendritic shafts constituted 17% of the targets. The dendritic shafts postsynaptic to cortico-cortical boutons were studied for the presence of gamma-aminobutyric acid (GABA) with a postembedding immunogold method. Most dendritic shafts (85%) that were tested were found to be GABA-positive, demonstrating that they originate from local inhibitory neurons. Taking into account that most postsynaptic targets were spines and extending the results of the immunocytochemical testing to the total population of postsynaptic dendrites, it was calculated that at least 14% of targets originated from GABA-positive cells. Thus cortico-cortical axons establish direct monosynpatic connections mainly with pyramidal and to a lesser extent with GABAergic nonpyramidal neurons in area PMLS, providing both feedforward excitation and feedforward inhibition to a visual associational area known to be involved in the processing of motion information. The results are consistent with previously demonstrated deficits in physiological properties of neurons in PMLS following removal of cortico-cortical afferents.

Animals

Activity-dependent decrease in NMDA receptor responses during development of the visual cortex.

Plasticity of the developing visual system has been regarded as the best model for changes of neuronal connections under the influence of the environment. N-methyl-D-aspartate (NMDA) receptors are crucial for experience-dependent synaptic modifications that occur in the developing visual cortex. NMDA-mediated excitatory postsynaptic currents (EPSCs) in layer IV neurons of the visual cortex lasted longer in young rats than in adult rats, and the duration of the EPSCs became progressively shorter, in parallel with the developmental reduction in synaptic plasticity. This decrease in NMDA receptor-mediated EPSC duration is delayed when the animals are reared in the dark, a condition that prolongs developmental plasticity, and is prevented by treatment with tetrodotoxin, a procedure that inhibits neural activity. Application of L-glutamate to outside-out patches excised from layer IV neurons of young, but not of adult, rats activated prolonged bursts of NMDA channel openings. A modification of the NMDA receptor gating properties may therefore account for the age-dependent decline of visual cortical plasticity.

Action Potentials

The pattern of ocular dominance columns in flat-mounts of the cat visual cortex.

Ocular dominance (OD) columns in the cat visual cortex were visualized with autoradiography after intravitreal injection of (3H)proline. Extending previous studies, a flat-mount technique was applied that enabled the analysis of the distribution of label throughout extensive regions of the visual cortex without requiring reconstruction from serial sections. OD-columns were confined to layer IV and consisted of isolated patches and short bands. The latter were parallel to each other and regularly spaced, the main trajectory being orthogonal to the 17/18 border. This pattern of the geniculo-cortical terminals was similar in the hemispheres ipsi- and contralateral to the injected eye. The mean periodicities of the OD-bands were virtually identical in the two hemispheres of the same animal: 850 microns and 830 microns in cat D1 and 770 microns and 800 microns in cat D2. However, the ipsilateral OD-columns appeared smaller, more heavily labeled and more sharply delineated than the contralateral columns.

Animals

Neurophysiological mechanisms of recovery from visual cortex damage in cats: properties of lateral suprasylvian visual area neurons following behavioral recovery.

Damage to visual cortical areas 17, 18, and 19 in the cat produces severe and long-lasting deficits in performance of form and pattern discriminations. However, with extensive retraining the animals are able to recover their ability to discriminate form and pattern stimuli. Recent behavioral experiments from this laboratory have shown that a nearby region of cortex, the lateral suprasylvian visual area (LS area), plays an important role in this recovery (Wood et al., 1974; Baumann and Spear, 1977b). The present experiment investigated the underlying neurophysiological mechanisms of the recovery by recording from single neurons in the LS area of cats which had recovered from long-term visual cortex damage. Five adult cats received bilateral removal of areas 17, 18, and 19. They were then trained to criterion on two-choice brightness, form, and pattern discriminations. Recording from LS area neurons was carried out after the behavioral training, from 3 to 7 months after the visual cortex lesions. The properties of these neurons were compared to those of LS area neurons in normal cats (Spear and Baumann, 1975) and in cats with acute or short-term visual cortex damage and no behavioral recovery (Spear and Baumann, 1979). The results showed that all of the changes from normal which were produced by acute visual cortex damage were also present after the behavioral recovery. Moreover, all of the response properties of LS area neurons which remain after acute visual cortex damage were present in similar form after the behavioral recovery. There was no evidence for any functional reorganization in the LS area concomitant with its role in the behavioral recovery. These results suggest that functional reorganization plays little or no role in recovery from visual cortex damage in adult cats. Rather, the recovery of form and pattern discrimination ability appears to be based upon the functioning of residual neural processes in the LS area which remain after the visual cortex damage.

Animals

Sex differences in cortical thickness and the dendritic tree in the monocular and binocular subfields of the rat visual cortex at weaning age.

The visual cortex of adult rats is sexually dimorphic at both the gross size and dendritic levels [Brain Res., 295 (1984) 27-34; J. Comp. Neurol., in press]. In addition, sex differences in the dendritic tree are dynamic and can be altered by environmental conditions imposed at weaning [Brain Res., 295 (1984) 27-34]. The present study examines sex differences in cortical thickness and in the dendritic tree of the monocular (Oc1M) and binocular (Oc1B) subfields in littermate male and female pairs of Long-Evans rats at weaning age (25 days). From Nissl-stained tissue, it was found that the whole cortex and layer II-IV of Oc1B was thicker in males than females. No sex differences were found in the thickness of Oc1M. Golgi-Cox-stained pyramidal neurons in layer III from the Oc1M and Oc1B regions were quantified in 7 littermate pairs of weaning-age rats. There were no sex differences in the basilar tree, while the apical oblique branches were sexually dimorphic, especially in the monocular region. Females had greater total dendritic length and longer terminal branches in Oc1M compared to males. Females also had longer bifurcating branches in both Oc1M and Oc1B than males. The present study found that sex differences at weaning age do not completely mirror the dimorphisms found in the visual cortex of the adult rat. This study also indicates that related subfields can differ in their morphology and should be examined separately.

Analysis of Variance

Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex.

Neurons of the visual cortex of the cat were penetrated with intracellular electrodes and postsynaptic potentials evoked by visual stimuli recorded. By alternately polarizing the cell with steady current injected through the recording electrode, IPSPs and EPSPs could be recorded and analyzed independently. Hyperpolarizing current suppressed IPSPs and enhanced EPSPs by moving the membrane potential toward the IPSP equilibrium potential. Depolarizing the cell toward the EPSP equilibrium potential enhanced IPSP. The responses to electrical stimulation of the LGN, where EPSPs and IPSPs could be distinguished easily by virtue of their characteristic latencies and shapes, were used to set the current injection to the appropriate level to view the two types of synaptic potential. EPSPs were found to be well oriented in that maximal depolarizing responses could be evoked at only one stimulus orientation; rotating the stimulus orientation in either direction produced a fall in the EPSP response. IPSPs were also well tuned to orientation, and invariably the preferred orientations of EPSPs and IPSPs in any one cell were identical. In addition, no systematic difference in the width of tuning of the two types of potential was seen. This result has been obtained from penetrations of over 30 cortical cells, including those with simple and complex receptive fields. It is concluded that orientation of cortical receptive fields is neither created nor sharpened by inhibition between neurons with different orientation preference. The function of inhibition evoked simultaneously with excitation by optimally oriented stimuli has yet to be determined, though it is likely to be the mechanism underlying other cortical receptive field properties, such as direction selectivity and end-stopping.

Animals

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

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

Age Factors

Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex.

Neurons in the primary visual cortex of higher mammals are arranged in columns, and the neurons in each column respond best to light-dark borders of particular orientations. The basis of cortical cell orientation selectivity is not known. One possible mechanism would be for cortical cells to receive input from several lateral geniculate nucleus (LGN) neurons with receptive fields that are aligned in the visual field (Hubel and Wiesel, 1962). We have investigated the relationship between the arrangement of the receptive fields of geniculocortical afferents and the orientation preferences of cortical cells in the orientation columns to which the afferents provide visual input. Radial microelectrode penetrations were made into primary visual cortex of anesthetized adult sable ferrets. Cortical cells were recorded throughout the depth of the cortex, and their orientation preferences were determined. Cortical cell responses were then eliminated by superfusion of the cortex with either kainic acid (Zahs and Stryker, 1988) or muscimol. After the drug treatment, responses from many single units with distinct receptive fields were recorded. These responses were presumed to be those of geniculocortical afferents, because they had the response properties characteristic of LGN neurons, and because they could be recorded only in cortical layers that receive geniculate input. In 16 of 18 cases, the afferent receptive fields recorded in a single penetration covered an elongated region of visual space. In these penetrations, the best-fit line through the centers of the afferent receptive fields generally paralleled the preferred orientation of cortical cells recorded at the same site in cortex. These results are consistent with the Hubel and Wiesel (1962) model for the construction of oriented visual cortical receptive fields from geniculate inputs with aligned receptive fields.

Afferent Pathways

Synaptic development in the rabbit superior colliculus and visual cortex.

The development of synapses in the visual cortex (VC) and superior colliculus (SC) of the rabbit has been examined with the electron microscope. In both areas, the number of synapses reaches adult levels by 20--25 days of postnatal age, but the development in the visual cortex is delayed in comparison to that in the superior colliculus. When S synapses (spheroidal vesicles, asymmetric thickening) are compared with F synapses (flattened vesicles, symmetric thickening), even greater differences are seen. In both the VC and SC, S synapses develop earlier than F synapses, though there is considerable overlap. Of interest is that fact that synapses in the visual cortex seem to overshoot their adult levels late in development, suggesting that an excess of synapses may be formed in this system. Multiple synapses, probably of retinal origin, increase in the first 3 weeks of synaptic development in the SC, but never are present in significant proportions in the VC. Synapse formation most often is characterized by formation of a junction and a postsynaptic thickening, followed by acquisition of synaptic vesicles. After 15 days, there is only a small number of such "non-vesicle synapses" in either the SC or VC.

Age Factors

'Real-motion' cells in area V3A of macaque visual cortex.

The stability of visual perception despite eye movements suggests the existence, in the visual system, of neural elements able to recognize whether a movement of an image occurring in a particular part of the retina is the consequence of an actual movement that occurred in the visual field, or self-induced by an ocular movement while the object was still in the field of view. Recordings from single neurons in area V3A of awake macaque monkeys were made to check the existence of such a type of neurons (called 'real-motion' cells; see Galletti et al. 1984, 1988) in this prestriate area of the visual cortex. A total of 119 neurons were recorded from area V3A. They were highly sensitive to the orientation of the visual stimuli, being on average more sensitive than V1 and V2 neurons. Almost all of them were sensitive to a large range of velocities of stimulus movement and about one half to the direction of it. In order to assess whether they gave different responses to the movement of a stimulus and to that of its retinal image alone (self-induced by an eye movement while the stimulus was still), a comparison was made between neuronal responses obtained when a moving stimulus swept a stationary receptive field (during steady fixation) and when a moving receptive field swept a stationary stimulus (during tracking eye movement). The receptive field stimulation at retinal level was physically the same in both cases, but only in the first was there actual movement of the visual stimulus. Control trials, where the monkeys performed tracking eye movements without any intentional receptive field stimulation, were also carried out. For a number of neurons, the test was repeated in darkness and against a textured visual background. Eighty-seven neurons were fully studied to assess whether they were real-motion cells. About 48% of them (42/87) showed significant differences between responses to stimulus versus eye movement. The great majority of these cells (36/42) were real-motion cells, in that they showed a weaker response to visual stimulation during tracking than to the actual stimulus movement during steady fixation. On average, the reduction in visual response during eye movement was 64.0 +/- 15.7% (SD).(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

[Types of receptive fields of neurons in different laminae of the rabbit visual cortex].

Neurons of the primary rabbit visual cortex were classified into 7 large groups according to features of their receptive fields. The neurons with receptive fields were mostly revealed in the layers IV and VI, those with uniform directional receptive fields--in layer V, those with simple I-in layer VI, those with simple II--in layer II + III, and those with hypercomplex--in layer IV. The neurons with concentric receptive fields and those without responses to visual stimuli were equally distributed over the layers. The data obtained in rabbits, cats, and monkeys suggest that the tendency towards function stratification of primary visual cortex is successive in an evolutionary order of mammals.

Animals

A hexagonal orthogonal-oriented pyramid as a model of image representation in visual cortex.

Retinal ganglion cells represent the visual image with a spatial code, in which each cell conveys information about a small region in the image. In contrast, cells of primary visual cortex employ a hybrid space-frequency code in which each cell conveys information about a region that is local in space, spatial frequency, and orientation. Despite the presumable importance of this transformation, we lack any comprehensive notion of how it occurs. Here we describe a mathematical model for this transformation. The hexagonal orthogonal-oriented quadrature pyramid (HOP) transform, which operates on a hexagonal input lattice, employs basis functions that are orthogonal, self-similar, and localized in space, spatial frequency, orientation, and phase. The basis functions, which are generated from seven basic types through a recursive process, form an image code of the pyramid type. The seven basis functions, six bandpass and one low-pass, occupy a point and a hexagon of six nearest neighbors on a hexagonal sample lattice. The six bandpass basis functions consist of three with even symmetry, and three with odd symmetry. The three even kernels are rotations of 0, 60, and 120 degrees of a common kernel; likewise for the three odd kernels. At the lowest level, the inputs are image samples. At each higher level, the input lattice is provided by the low-pass coefficients computed at the previous level. At each level, the output is subsampled in such a way as to yield a new hexagonal lattice with a spacing square root 7 larger than the previous level, so that the number of coefficients is reduced by a factor of seven at each level. In the biological model, the input lattice is the retinal ganglion cell array. The resulting scheme provides a compact, efficient code of the image and generates receptive fields that resemble those of the primary visual cortex.

Computer Simulation

Types and spatial distribution of vasoactive intestinal polypeptide (VIP)-containing synapses in the rat visual cortex.

In the rat visual cortex vasoactive intestinal polypeptide (VIP)-containing structures were studied by means of light and electron microscopy and image analysis. VIP-immunoreactive axon terminals were found to form symmetric synapses with small dendritic shafts, dendritic spines and somata of pyramidal cells and interneurons. VIP-terminals often occurred in pairs with VIP-negative, asymmetric synapses on the same postsynaptic structure. VIP-immunostained dendrites and perikarya were contacted by a purely asymmetric and a mixed population of VIP-negative terminals, respectively. Synaptic connections between two VIP-neurons are seldom as compared to the other types of VIP-synapses. Quantitative studies obtained by the image analysis of VIP-stained boutons and dendritic particles in light microscopic preparations suggest a distinct laminar distribution. Dendritic particles are most frequent in layers I-II, whereas axonal boutons have three laminar accumulations: at the border of layers I-II, in layer IV and layer VI. Together with previous results, the present findings argue for a non-random spatial distribution of VIP-boutons.

Animals

Ultrastructure of PkC(II/III)-immunopositive structures in rat primary visual cortex.

In the primary visual cortex of adult rats the cellular and subcellular distribution of protein kinase C isozymes II and III (PkCII/III) was examined by immunohistochemical methods with a monoclonal antibody against PkCII/III. Strong PkC(II/III)-immunoreactivity was found in neurons and astrocytes. Immunopositive neurons exhibited morphological features characteristic for both pyramidal and non-pyramidal cells. They were distributed in layers II through VI but were concentrated in layers II/III. At the electron microscopic level immunoprecipitate was found predominantly in distinct regions of the somata, except the nuclei, and only a few labeled dendrites and axons were seen. Two different patterns of cytoplasmic immunoreactivity could be distinguished. In most neurons, PkC(II/III)-staining was confined to cytoplasmic spots associated with the Golgi complex, while a few neurons exhibited additional labeling in the vicinity of the cell membrane. Moreover, PkC(II/III)-immunoreactivity was present in numerous astroglial processes and in the perikaryal cytoplasm of a subpopulation of astrocytes. The present data provide morphological indications for specific functions of PkC isozymes II and III in neurons as well as in astrocytes.

Animals

Effects of NMDA antagonists on developmental plasticity in kitten visual cortex.

The existence of Hebb synapses in the visual cortex of young kittens has long been postulated. A mechanism for the correlation of activity in simultaneously active pre- and postsynaptic neurons could be provided by the properties of the N-methyl-D-aspartate (NMDA) receptor and its associated Ca2+ channel, which opens in a transmitter- and voltage-dependent manner. We have studied the effects on cortical plasticity of blocking NMDA receptors in different ways with competitive and non-competitive NMDA antagonists. In our first approach, the non-competitive NMDA antagonist ketamine, a short-acting dissociative anaesthetic, was injected systemically after each of a series of brief monocular exposures. This procedure prevented the development of an ocular dominance shift towards the experienced eye in the visual cortex. Other short-acting anaesthetics, such as xylazine or methohexital, while providing the same depth of anaesthesia, did not have the same effect on ocular dominance plasticity. We conclude, therefore, that ketamine quite specifically interferes with synaptic consolidation in the visual cortex. In order to establish a role of NMDA receptors for cortical plasticity directly in the visual cortex, we performed another series of experiments: 2-amino-5-phosphono-valerate (APV), a competitive NMDA antagonist, was infused intracortically by means of implanted osmotic minipumps in kittens, which were monocularly deprived for 1-2 weeks. Within a radius of 4-5 mm, the expected ocular dominance shift was prevented or reduced. In addition, however, physiologically determined cell density and responsiveness to visual stimuli were grossly abnormal around the infusion site, and histological cell density was also reduced. Similar effects were found when MK801 (a non-competitive NMDA antagonist) was used in the same type of experiment. The outcome of both experimental approaches makes it very likely that NMDA antagonists somehow interfere with cortical plasticity. Their mode of action, however, remains ambiguous. Although it is quite possible that blocking of the NMDA channel prevents the Hebbian correlative process necessary for synaptic consolidation, more complex effects, such as an interference with a neurotrophic action normally exerted via the NMDA receptor, may have to be taken into account as well.

2-Amino-5-phosphonovalerate