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Vasoactive intestinal polypeptide immunoreactive neurons in the primary visual cortex of the cat.

When cat visual cortex (area 17) is reacted with an antibody to vasoactive intestinal polypeptide (VIP) a variety of neuronal types is labelled. Many of the labelled neurons are bipolar in form and are most common in layers II and III, although significant numbers of bipolar neurons are also encountered in layer V. Multipolar cells are also labelled. These are most frequent in layer IV and have a variety of shapes. In layer I, the labelled cells are of three varieties, i.e. horizontal bipolar cells, horizontal bitufted cells and multipolar neurons, while in layer VI the few VIP-positive neurons are horizontal bipolar cells. This suggests that all of the VIP-labelled neurons in cat area 17 are non-pyramidal in form, and this has been confirmed by electron microscopy. In these preparations, axon terminals are also labelled and under the light microscope it can be seen that these terminals occur both within the neuropil and around the cell bodies of some neurons, particularly neurons in layers II and III. Electron microscopy has shown that all of the labelled axon terminals form symmetric synapses and that those in the neuropil synapse with the shafts of smooth dendrites. These axodendritic synapses account for about 90% of the synapses formed by the labelled axon terminals. The remainder of the labelled axon terminals synapse with the cell bodies of pyramidal neurons. Parallels are drawn between these results and those previously obtained by examining those neuronal elements labelled with VIP antibodies in rat visual cortex.

Animals

A new heterotopic callosal projection of primary visual cortex in the monkey, Callithrix jacchus.

A callosal projection of area 17 upon the dorsomedial visual area in the marmoset monkey was demonstrated by means of retrograde transport of neuronal tracers. The projection was restricted to those regions representing the vertical meridian in the two areas. This finding, and the data of other authors, indicate that the monkey area 17 projects transcallosally onto homotopic and several heterotopic targets.

Animals

Induction of LTP in rat primary visual cortex: tetanus parameters.

Long-term potentiation (LTP), intensively studied in the hippocampus as a possible mnemonic device, has begun to be studied in the neocortex. In this study the effects of varying tetanic stimulus parameters on LTP of field potentials recorded from layer II/III induced by white matter stimulation in the in vitro rat visual cortical slice were examined. Low intensity tetanus was more effective in producing LTP than high-intensity tetanus, although single pulses of very high intensity reliably resulted in LTP. LTP consistently occurred following 2 Hz-60 min, or 100 Hz-10 min tetanus; whereas, 10 min of 7 and 25 Hz tetanus usually resulted in long-lasting depression. Although no obvious rule related tetanus frequency and duration to the incidence of LTP, an inverted-U relationship was found between tetanus frequency and LTP magnitude.

Animals

Lamina-selective A68 immunoreactivity in primary visual cortex of Alzheimer's disease patients.

Sections of area 17 from 9 Alzheimer's disease (AD) and 13 control cases were stained using the monoclonal antibody, Alz-50, which identifies pathologically-involved neuronal systems in AD patients. Strong positive staining was seen only in AD cases. The pattern of staining was highly lamina-selective; laminae I-IVa and V were intensely stained and lamina VI staining was moderately intense, while laminae IVb and IVc were relatively unstained. The results support the growing consensus that cortical pathology in AD is not generalized, but affects specific neuronal populations. The specific anatomical distribution of degenerative change suggests that there may be a specific set of visual deficits in AD patients.

Adolescent

The cytoarchitectonic boundaries of the monocular and binocular areas of the rat primary visual cortex.

We describe the cytoarchitectonic characteristics of the monocular (Oc1M) and the binocular (Oc1B) areas of the rat visual cortex and their boundaries in Nissl-stained sections. This formulation, which draws upon the computer image analysis of these areas by Zilles et al. (J. Comp. Neurol., 226 (1984) 391-402), can aid in the delineation of Oc1M from Oc1B in quantitative studies requiring a volumetric analysis of both subfields.

Animals

Excitatory inputs to layer V pyramidal cells of rat primary visual cortex revealed by acetylcholine activation.

Cells in layers II-III or VI were activated by microdrop application of acetylcholine (ACh), while monitoring the intracellular response of layer V pyramidal cells. This enabled the tracing of functional connections between the cells of layers II-III or VI with those of layer V. ACh activation of layer II-III or VI cells resulted in a small depolarization of these cells, accompanied by a burst of excitatory postsynaptic potentials (EPSPs) from layer V pyramidal cells. These effects of ACh were blocked by tetrodotoxin (TTX), suggesting the involvement of action potentials in their production. The input resistance of layer V pyramidal cells during and after the EPSP burst was not significantly different from control values, further suggesting an indirect effect of ACh on layer V pyramidal cells. Isolation of the supragranular layer, by horizontal cutting, did not prevent the EPSP burst evoked by ACh application to the lower layer VI, suggesting a direct input from layer VI to layer V pyramidal cells. ACh applied near pyramidal cells in layers II-III, V or VI caused transient hyperpolarization associated with a decrease in input resistance followed by a large depolarization, an increase in input resistance, and action potential discharges. The ACh-mediated hyperpolarization and the train of action potentials of layer II-III pyramidal cells were blocked by TTX. Thus the ACh-activated cells in layers II-III and VI make an excitatory synaptic contact with layer V pyramidal cells, producing the EPSP burst observed in layer V.

Acetylcholine

The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat.

Perception of a visual attribute, such as orientation, is strongly dependent on the context within which a feature is presented, such as that seen in the tilt illusion. The possibility that the neurophysiological basis for this phenomenon may be manifest at the level of cells in striate cortex is suggested by anatomical and physiological observations of orientation dependent long range horizontal connections which relate disparate points in the visual field. This study explores the dependency of the functional properties of single cells on visual context. We observed several influences of the visual field area surrounding cells' receptive field on the properties of the receptive field center: inhibition or facilitation dependent on the orientation of the surround, shifts in orientation preference and changes in the bandwidth of orientation tuning. To relate these changes to perceptual changes in orientation we modeled a neuronal ensemble encoding orientation. Our results show that the filter characteristics of striate cortical cells are not necessarily fixed, but can be dynamic, changing according to context.

Animals

The postnatal development of the rat primary visual cortex during optic nerve impulse blockade by intraocular tetrodotoxin: a quantitative electron microscopic analysis.

The effect of tetrodotoxin (TTX)-induced monocular impulse blockade on various parameters of synaptogenesis during the first 3 postnatal weeks of the developing rat visual cortex was investigated by quantitative electron microscopy. During the injection period, beyond 14 days postnatal (dpn), the effectiveness of TTX in blocking optic nerve impulses was monitored by loss of the pupillary light reflex. Between 5 and 21 dpn, TTX treatment reduced the number of type I axodendritic synapses by approximately 23%, when compared to sham-injected controls. These reductions were found in layers III, IV, and the superficial region of layer V. Layer IV exhibited the greatest decrease (24%) while layers III and V showed reductions of 20% and 18%, respectively. At 21 dpn, the number of type II axodendritic synapses decreased by 19% in the same layers, but no reductions were found at earlier ages. TTX also reduced the mean number of synaptic vesicles within type I and type II terminals by 27% and 15%, respectively. At 9 dpn, reductions were first found in layers IV and V, but by 21 dpn significant decreases were found in layers II/III, IV and V. TTX had no effect on the length of the postsynaptic density of both synaptic types or on cortical thickness at any age. These data indicate that optic impluses are important mediators of synaptogenesis in the developing visual cortex, the loss of which induces localized and specific synaptic alterations, possibly due to a change in cortical circuitry.

Animals

Blindsight in rodents: the use of a 'high-level' distance cue in gerbils with lesions of primary visual cortex.

Two experiments examined the possibility that Mongolian gerbils with bilateral lesions of the striate cortex could use retinal image size as a distance cue on a jumping task. Systematically wider or narrower 'probe' landing platforms were inserted amongst regular training trials with a standard-sized landing platform. In both sham-operated and destriate animals, narrower platforms tended to produce overjumps of the leading edge of the landing platforms, while the wider probes tended to produce underjumps. The size of this effect did not differ between the two groups in either study. Differences between this type of task and traditional size discrimination experiments are discussed.

Animals

Receptive field dynamics in adult primary visual cortex.

The adult brain has a remarkable ability to adjust to changes in sensory input. Removal of afferent input to the somatosensory, auditory, motor or visual cortex results in a marked change of cortical topography. Changes in sensory activity can, over a period of months, alter receptive field size and cortical topography. Here we remove visual input by focal binocular retinal lesions and record from the same cortical sites before and within minutes after making the lesion and find immediate striking increases in receptive field size for cortical cells with receptive fields near the edge of the retinal scotoma. After a few months even the cortical areas that were initially silenced by the lesion recover visual activity, representing retinotopic loci surrounding the lesion. At the level of the lateral geniculate nucleus, which provides the visual input to the striate cortex, a large silent region remains. Furthermore, anatomical studies show that the spread of geniculocortical afferents is insufficient to account for the cortical recovery. The results indicate that the topographic reorganization within the cortex was largely due to synaptic changes intrinsic to the cortex, perhaps through the plexus of long-range horizontal connections.

Afferent Pathways

Layer IVA of rhesus monkey primary visual cortex.

Layer IVA of rhesus monkey striate cortex contains pyramidal cells arranged in distinct groups. Their cell bodies are in a configuration of flat cones, each with an average diameter of 60 microns, and their apical dendrites aggregate into bundles that ascend toward the pial surface. Nissl-stained sections suggest that these pyramidal cell cones have their bases in layer IVB, with their tops extending into layer IVA. The neurons in the cones are readily apparent in MAP2 antibody-stained material, and in cytochrome oxidase-reacted tissue it is evident that the pyramidal cell cones occupy the pale spaces that are surrounded by the darkly reactive honeycomb lattice. This lattice of neuropil around the cones contains some axons and boutons that are immunoreactive for parvalbumin, and it is within the lattice that other investigators have shown afferents from the parvocellular (P)-layers of the dLGN to terminate. Because of this input, it is likely that the pyramidal cell cones of layer IVA are involved with color and form perception. The relationship between the layer IVA cones of neurons and the underlying system of previously described pyramidal cell modules (Peters and Sethares, 1991) is discussed, as well as the possibility that the pyramidal cell cones might represent aggregations of neurons, which receive input from basic sets of P-like afferents originating from color-responsive ganglion cells of the retina, as described by Schein and de Monasterio (1987).

Animals

Development of cortical afferents and cortico-tectal efferents of the mammalian (rat) primary visual cortex.

At the time when the fibres from the striate cortex (area 17) begin to innervate the superficial layers of the superior colliculus of the young rat (postnatal days 4 and 5) a high degree of specificity in the organization of this newly formed cortico-tectal projection is already apparent. Thus, in young rats, as in adult mammals of virtually all species studied so far, the somata of cortico-tectal neurones are confined to lamina V of the ipsilateral cortex. However, this high degree of laminar (radial) specificity in young animals is accompanied by a substantial degree of exuberance as indicated by a tangential distribution of the cortico-tectal cells which is wider than that in the adult. The exuberant projections are pruned during the second postnatal week. The cortico-cortical associational and commissural fibres start to enter the grey matter of the rat striate cortex after postnatal day 7. Again a high degree of specificity in the laminar distribution of those newly established projections is apparent. However, the cortico-cortical projection, at the time when cortico-cortical fibres enter the cortical laminae, is clearly exuberant since the tangential spread of cortical cells projecting to the striate cortex is wider than that in the adult. Pruning of these excessive projections takes place some time after postnatal day 14. It is believed that understanding the mechanism(s) underlying the development of connections of the rat visual cortex might be of general importance in understanding developmental abnormalities in the pattern of interconnections of the visual cortices of other mammalian orders.

Afferent Pathways

Laminar differences in receptive field properties of cells in cat primary visual cortex.

1. Cells in area 17 of the cat visual cortex were studied with a view towards correlating receptive field properties with layering. A number of receptive field parameters were measured for all units, and nearly every unit was marked with a microlesion to determine accurately the layer in which it was found.2. Cells were defined as simple or complex by mapping with stationary stimuli, using the criteria of Hubel & Wiesel (1962). Complex cells fell into two groups: those that showed summation for increased slit length (standard complex) and those that did not (special complex).3. The simple cells were located in the deep part of layer 3, in layer 4, and in layer 6. This corresponds to the distribution of afferents from the dorsal layers of the lateral geniculate nucleus. In these cortical layers the simple cells differed primarily with respect to their receptive field size, cells in layer 4 having the smallest, layer 3 intermediate, and layer 6 the largest fields. Layer 4 was the only layer in which simple cells showed end-inhibition (a reduction in response to slits extending beyond the excitatory portion of the receptive field).4. The standard complex cells were found in all layers, but were quite scarce in layer 4. As with the simple cells, field size varied with layer: in layer 2+3 they had small to intermediate field sizes, in layer 5 intermediate, and in layer 6 very large. Layer 6 cells showed summation for slits of increased length up to very large values, and responded best when the slits were centred in the receptive field. The only standard complex cells that showed end-inhibition were those in layer 2+3, and these were similar to the layer 4 simple cells in terms of proportion of end-inhibited units and degree of end-inhibition.5. The special complex cells, originally described by Palmer & Rosenquist (1974), were found in two tiers: the upper one at the layer 3/layer 4 border and the lower one in layer 5. They were different from the standard complex cells in having a high spontaneous activity, high velocity preference, and large fields which were similar in size (at a given eccentricity) from one cell to the next. Many showed reduced response to slits of increasing length, even for slits that did not extend beyond the borders of the responsive region.6. Cells in layer 6 (the origin of the corticogeniculate projection) were antidromically activated from the lateral geniculate nucleus. The antidromically activated units included both simple and complex cells, and they had the long receptive fields characteristic of the overall population of cells in layer 6.7. The results showed that there are different types of simple and complex cells, and that cells in different layers have different properties. Taken together with their differences in site of projection, this demonstrates that the anatomical lamination pattern is reflected in functional differences between cells in different layers.

Action Potentials

Continuity of orientation columns between superficial and deep laminae of the cat primary visual cortex.

1. Recent reports of a marked and consistent dislocation between orientation columns in the superficial and deep layers of cat striate cortex (Bauer, 1982, 1983) directly contradict the traditional view of the system (Hubel & Wiesel, 1962). This has considerable implications for our current understanding of cortical organization, and in order to clarify the issue we have carried out experiments to test the continuity of the columnar system with depth, in central regions of area 17. 2. In twenty-four penetrations, eighteen of which were placed as perpendicular as possible to the surface of the cortex, orientation preference was assessed at regular intervals both qualitatively and using a randomly interleaved quantitative technique. The distribution of preferred orientations was analysed with reference to a detailed histological reconstruction of the electrode track, including the location of laminar boundaries and the course of radial tiers of cells and capillaries. 3. From a further series of eighteen near-perpendicular penetrations, the change in average orientation between one superficial and one deep layer recording site was compared with the deviation of the track from perpendicular to the surface and hence parallel to the orientation columns. 4. In penetrations perpendicular to the surface of the cortex, orientation preference showed little variation between superficial and deep laminae. In oblique penetrations, preferred orientation generally changed according to a single, smooth trend. Those irregularities that were encountered were confined to oblique penetrations, and were distributed throughout the cortical laminae. 5. In conclusion, our evidence does not support the presence of a systematic discontinuity with depth within the orientation columnar system. It is therefore entirely consistent with earlier evidence on the subject.

Animals