The development of synapses in kitten visual cortex during visual deprivation.
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The postnatal ontogeny of 3H-pirenzepine and 3H-oxotremorine-M binding to M1-and M2-muscarinic acetylcholine receptors, respectively, as well as 3H-nicotine binding to neuronal nicotinic acetylcholine receptors, 3H-phorbol-12,13-dibutyrate binding to protein kinase C and 3H-PN200-110 binding to dihydropyridine-sensitive calcium channels was studied in individual layers of the visual cortex in both normally raised and monocularly deprived rats (one eyelid sutured at the age of 11 days) using quantitative receptor autoradiography. Postnatal ontogeny of M1-muscarinic receptors is similar in each visual cortical layer reaching the highest receptor density at the age of 15 days, whereas M2-muscarinic binding sites increase gradually from day 7 up to day 34. Highest 3H-nicotine binding is reached in all visual cortical layers at postnatal day 15 followed by a considerable decrease in binding sites until day 25. Phorbol ester binding rises considerably from birth until the age of 15 days reaching nearly the adult value in the upper layers, whereas in layers V and VI a marked decrease in binding levels until adulthood can be observed. The developmental course of 3H-PN200-110 binding sites is similar in all visual cortical layers and exhibits a moderate rise in binding sites between postnatal days 7 and 15. Monocular deprivation results in permanent changes in the developmental profiles of phorbol ester as well as calcium antagonist binding sites, whereas the alterations in muscarinic and nicotinic cholinergic receptors following monocular deprivation are only of transient nature. The data presented suggest that acetylcholine plays a modulatory role during a certain period of early postnatal maturation of the visual cortex by affecting both cholinergic receptors and associated second messenger cascades.
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The visual cortex was studied in the mouse (C57 Black/6J strain) be recording from single units, and a topographic map of the visual field was constructed. Forty-five percent of the neurons in striate cortex responded best to oriented line stimuli moving over their receptive fields; they were classified as simple (17%), complex (25%) and hypercomplex (3%). Of all preferred orientations horizontal was most common. Fifty-five percent of recpetive fields were circularly symmetric: these were on-center (25%), off-center (7%) and homogeneous on-off in type (23%). Optimal stimulus velocities were much higher than those reported in the cat, mostly varying between 20 degrees and 300 degrees/sec. The field of vision common to the two eyes projected to more than one-third of the striate cortex. Although the contralateral eye provided the dominating influence on cells in this binocular area, more than two-thirds of cells could also be driven through the ipsilateral eye. The topography of area 17 was similar to that found in other mammals: the upper visual field projected posteriorly, the most nasal part mapped onto the lateral border. Here the projection did not end at the vertical meridian passing through the animal's long axis, but proceeded for at least 10 degrees into the ipsilateral hemifield of vision, so that at least 20 degrees of visual field were represented in both hemispheres. The magnification in area 17 was rather uniform throughout the visual field. In an area lateral to area 17 (18a) the fields were projected in condensed mirror image fashion with respect to the arrangement of area 17. Medial to area 17 a third visual area (area 18) was again related to 17 as a condensed mirror image.
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The receptive filelds of orientation-selective neurons were studied in the rabbit visual cortex. Two mechanisms of the selectivity were found: the mutual inhibition between on- and off-regions of the receptive field (simple type) and the orientation-dependent inhibition within the uniform region of the receptive field. The non-selective neurons could exhibit the lateral inhibition within the uniform region of the receptive field also. It is supposed that both "simple" and "complex" cells originate from the non-selective units.
Visual responses of the striate complex cells to stimuli orientation, direction and velocity of movement were studied in awakening, unanesthetized cats. "Complex" cells were divided into four groups according to the response characteristics which were obtained using a stationary slit, moving light spot and moving oriented stimulus. The first group units response characteristics suggest the presence of the orientation selectivity mechanism in their receptive field organization, the fourth group--the direction selectivity mechanisms, the second and third groups--the presence of both mechanisms. It is supposed that there are two separate mechanisms for coding the orientation and direction of the stimulus movement in the neuronal structures of the visual cortex.
1. The early visual experience of nine cats was restricted to viewing horizontal or vertical lines inside opaque goggles. 2. When the kittens were 3-4 mo old, extracellular recordings were made in the primary visual cortex. To obtain a representative sample of cortical cells, units were studied at regularly spaced intervals along the course of electrode penetrations traveling oblique to the cortical surface. An automated assessment of preferred orientation using a computer-driven optical display was employed, and during the recording session the experimenters did not know which orientation(s) each animal had viewed in early life. 3. In the cats that viewed horizontal lines with one eye and vertical lines with the other during rearing, two major findings of previous workers (14) were confirmed. First, a majority of units were not selective for orientation. Second, units with preferred orientations near vertical tended to be activated exclusively by the eye that had viewed vertical, and likewise for horizontal. 4. In cats that viewed lines of the same orientation with both eyes during rearing, a substantially smaller proportion of units were selective for orientation; the preferred orientations of these units also tended to match the orientation to which the cats had been exposed. 5. Portions of some electrode penetrations showed an orderly arrangement of cells according to preferred orientation similar to that seen in normal cats, but with regions over which only nonselective cells were found. Many penetrations appeared less orderly. 6. The results are consistent with a role for early visual experience in maintaining the responsiveness and innate selectivity of cortical neurons, although they cannot entirely rule out the possibility that experience may alter or determine the preferred orientation of some cells.
Electrical stimulation of human visual cortex produces punctuate phosphenes in the visual field. This phenomenon, which is being explored as the basis for a visual prosthesis for the blind, also provides the first electrophysiological information about the retinocortical map in man. Stimulation of points clustered on the surface of the visual cortex produces phosphenes clustered in visual space. However, adjacent surface electrodes located on opposite sides of a sulcus can produce widely separated phosphenes, because the intervening cortex is buried and inaccessible to stimulation. Such electrodes can also produce multiple phosphenes by simultaneously stimulating both banks of the sulcus. Electrodes which are widely spaced on the brain can produce phosphenes close together in visual space providing they stimulate cortex corresponding to overlapping maps in areas 17 and 18. Analysis of the phosphene map indicates that successive stimulation of points further from the tip of the occipital pole produces phosphenes progressively more distant from the fixation point. Successive stimulation of points along the orthogonal dorsoventral dimension produces a progressive change in phosphene bearing. These results confirm the general view of cortical organization derived from field defect studies in man, and from anatomical and electrophysiological studies in monkeys, and provide a new tool for more detailed study of retinotopic projections in man.
The responses of visual cortical neurons to patterned visual stimuli were studied in squirrel Sciurus vulgaris. The direction selective, orientation-selective and non-selective neurons were observed. Most direction-selective and non-selective neurons were sensitive to high speeds of stimulus movement--hundreds deg/s. The direction-selective neurons exhibited their selectivity at such high speeds in spite of the short time of the stimulus movement through the receptive field. Orientation-selective neurons (with simple or complex receptive fields) were sensitive to lower speeds of the stimulus movement (tens deg/s). Some mechanisms of the properties described are discussed.
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The influence of visual association cortex on the pattern of neuronal activity in the lateral geniculate body, during penicillin-induced discharges in visula cortex, was studied. In a majority of those geniculate cells which exhibited a pre-penicillin discharge increment in activity, that increment was abolished or significantly reduced during focal hypothermia of the visual association cortex. The frequency of penicillin discharges in visual cortex was, in most cases, reduced during cooling of association cortex. These findings are briefly discussed in terms of corticothalamic interactions.
Golgi preparations of rabbit visual cortex aged 1-25 days, as well as similar tissues from adults, were examined for the growth of the dendritic arbor, and in particular the development of dendritic spines. The layer 5 pyramidal neurons and layer 4 stellate neuron were chosen as representatives of larger classes of neurons in the visual cortex. It was determined that the growth of the dendritic arbor, determined by counts of total number of dendritic and total dendritic length, is quite similar for pyramidal and stellate neurons. Dendritic spine development, however, is more rapid in pyramidal neurons than in stellate. This disparity in the rate of dendritic spine development is discussed in the light of physiologic studies on the development of receptive field properties in the rabbit visual cortex.
Kittens were deprived of form vision by suturing the lids of both eyes, except for a brief period (1, 6 or 20 hours) on the 29th day when the right eye was opened. 6 space and 20 hours of monocular vision produced a distinct shift in the ocular dominance of visual cortical neurons towards the experienced eye, and an increase in the proportion of cells with obvious orientation selectivity. These modifications in the visual cortex were enhanced by a period of "consolidation": they were somewhat less obvious if recordings were taken immediately after the exposure but were complete 2 days later. Although remarkably little visual experience was needed for these changes, the results contrast with the effects of rearing in an environment of vertical stripes, where only 1 hour of exposure produces much more striking effects. A normal visual environment may have a less powerful organizing influence on cortical neurons than such an environment containing only one orientation.
Under anaesthesia the right visual cortex of the guinea pig was investigated with 1.5 M potassium citrate-filled glass microelectrodes. Single unit and small unit cluster response showed an organized three-part representation of the contralateral visual field on the animal's visual cortex. The major central division (V1) had the representation of a nasotemporally elongated visual field. This visual field extended for about 110 degrees horizontally and for about 70 degrees vertically. The nasal visual field was represented laterally on the cortex and the lower visual field anteriorly. The visual field representation was not uniformly magnified in V1; the magnification of the nasal field was higher than the rest of the visual field. On either side of V1, the guinea pig's cortex had two additional visually responsive strips. The strip V2L, situated lateral to V1, had a condensed representation of about 40 degrees of the animal's nasal visual field and mirror-imaged the visual field representation of the adjacent V1. The strip V2M, situated medial to V1, had a similar representation of about 40 degrees of the animal's temporal visual field and mirror-imaged the visual field representation of the area V1 adjacent to it. A binocularly responsive zone of cortex was observed on either side of the boundary between the areas V1 and V2L, representing between 10 degrees and 15 degrees of the nasal visual field on each side of the boundary line. Investigation of the retinal ganglion cell distribution of the animal showed a nasotemporally oriented 'visual streak' with a high ganglion cell density per unit area of the retina, near the optic disc. Away from the 'visual streak' the density of the ganglion cells of the retina diminished progressively. The configuration of the 'visual streak' and the general pattern of the ganglion cell distribution in the rest of the retina coincided with the asymmetry in the magnification of representation of the animal's visual field on the 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.
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.