Dynamic detection of light intensity by cat visual cortex neurons

Dynamics of intensity functions of neurons in area 17 of the visual cortex was studied by the method of time slices on unanesthetized cats. The intensity functions of the neurons were estimated from successive fragments of responses. In 70% of cases during 40-200 ms after beginning of the stimulus action the preferred intensity changed from lesser to greater brightness. The possible role of this effect in the intensity of time coding by the visual cortex neurons is discussed.     

Interrelation among properties of visual cortex neurons in the cat

In acute experiments on immobilized cats 13 functional characteristics of 96 visual cortex neurons were investigated. Regressional and cluster analyses were used to divide these neurons into two subgroups with different density and degree of connections between characteristics. The receptive fields of cells of the first subgroup were localized relatively centrally in the visual field, those of the second subgroup were localized more often on the periphery. A valuable correlation was found in the half of the studied characteristics. In each subgroup the more centrally localized cells with small receptive fields had relatively shorter latencies, lower thresholds, shorter temporal summation, wider intensity range and greater differential sensitivity; their responses were phasic, with high-frequency discharges. The density of valuable correlation of the characteristics varied from 0.21 to 0.99. The amount of these correlations in the first subgroup was two times higher than in the second one. The possible mechanisms of the correlation between the properties of the visual cortex neurons are discussed, as well as their differences in two subgroups and in the cortex and LGB.     

Intracortical microstimulation of neurons in the visual cortex of the cat

The response of visual cortex neurons to local intracortical microstimulation was measured in the anesthetized cat. When the recording microelectrode was very close (about 20 micrometers) to the tip of the stimulating electrode, threshold currents as low as 10 micro A were capable of firing neurons. Over a 20-fold range in distance from the site of stimulation, an 80-fold increase in threshold current was observed. The mean latency of activation for 30 neurons tested with intracortical stimulation was 2.88 +/- 0.45 msec. The majority of these cells were probably synaptically activated. The mean threshold current for these neurons was 0.55 +/- 0.12 mA (N = 30). These values were significantly smaller than the thresholds found previously when stimulating electrodes were located on the pia-arachnoid surface of the visual cortex.     

The effect of sombrevin on the orientation adjustment of the visual cortex neurons in the cat

Change in the orientation tuning of 58 visual cortex neurons, evoked by light sombrevine anaesthesia were studied in acute experiments on immobilized cats. After the sombrevine injection a reliable change of the preferable orientation by 47.6 +/- 5.6 degrees took place in 60% of cells, while in the remaining cells it was stable in all stages of anaesthesia. Stable neurons preferred the horizontal and vertical orientations, in the unstable ones this preference was less expressed. The stable neurons possessed higher qualities of orientation detection than the unstable ones. The width of the orientation tuning changed reliably by 65.2 +/- 6.7 degrees on the average in 55% of neurons, while in 31% of neurons the tuning acuteness was worse, but in 24% it was sharper. The frequency of background discharges under anaesthesia in 2/3 of investigated neurons was reduced by 58% and that of the evoked discharges by 35%. The preferable orientation, the width of the tuning and the frequency of the neuron discharge as a rule recovered in 30 min after the beginning of the anaesthesia.     

Role of burst activity in attribute detection by visual neurons of the cat cortex

The temporal structure of neuronal responses has been investigated in the Clare-Bishop area of the cat cortex. Stationary and moving slit and moving spot have been used for stimulation. It was found that orientational and directional selectivity was determined mainly by the number of clustered impulses and the number of clusters. A closed-loop model for features detection which is able to interpret clustered activity is presented.     

Polyneuronal innervation of spiny stellate neurons in cat visual cortex

Our hypothesis was that spiny stellate neurons in layer 4 of cat visual cortex receive polyneuronal innervation. We characterised the synapses of four likely sources of innervation by three simple criteria: the type of synapse, the target (spine, dendritic shaft), and the area of the presynaptic bouton. The layer 6 pyramids had the smallest boutons and formed asymmetric synapses mainly with the dendritic shaft. The thalamic afferents had the largest boutons and formed asymmetric synapses mainly with spines. The spiny stellates had medium-sized boutons and formed asymmetric synapses mainly with spines. We used these to make a “template” to match against the boutons forming synapses with the spiny stellate dendrite. Of the asymmetric synapses, 45% could have come from layer 6 pyramidal neurons, 28% from spiny stellate neurons, and 6% from thalamic afferents. The remaining 21% of asymmetric synapses could not be accounted for without assuming some additional selectivity of the presynaptic axons. Additional asymmetric synapses may come from a variety of sources, including other cortical neurons and subcortical nuclei such as the claustrum. Of the symmetric synapses, 84% could have been provided by clutch cells, which form large boutons. The remainder, formed by small boutons, probably come from other smooth neurons in layer 4, e.g., neurogliaform and bitufted neurons. Our analysis supports the hypothesis that the spiny stellate receives polyneuronal innervation, perhaps from all the sources of boutons in layer 4. Although layer 4 is the major recipient of thalamic afferents, our results show that they form only a few percent of the synapses of layer 4 spiny stellate neurons.     

Postnatal maturation of nonpyramidal neurons in the visual cortex of the cat

A Golgi study of nonpyramidal neurons in the visual cortex of kittens aged from 1 to 80 days revealed that different neuronal types undergo a differential sequence of maturation. The earliest nonpyramidal cells to differentiate are large multipolar cells of layers 3-5, which appear around birth and whose axons gradually establish long lateral, intracortical connections. They are followed by spiny stellate cells of layer 4, which appear in the first postnatal, week, and by neuroglioform cells in layers 4 and 5, a cell type which at 10 days displays a highly differentiated axonal plexus. In general, most classes of local axon cells can be identified by the end of the second week, though still possessing a very immature morphology, the axonal-tuft cells of layer 2 maturing later, in the third week. With some exceptions, most neurons exhibit an adultlike axonal arborization by the end of the first month; however, immature chandelier terminals are observed until the 40th day, and in kittens aged from 30 to 80 days, the vertical terminal segments of chandelier cells are larger than in the adult. Some neuronal types seem to present an exuberant growth of axonal fibers in the late postnatal period and a subsequent reduction up to the adult stage.     

Selective staining of a subset of GABAergic neurons in cat visual cortex by monoclonal antibody VC1.1

VC1.1 is a monoclonal antibody generated against cat area 17, which selectively outlines subsets of cortical neurons (Arimatsu et al., 1987). This study was conducted to determine the ultrastructural distribution of the VC1.1 antigen and to identify the particular subclasses of cortical neurons that were labeled. In the light microscope, VC1.1 delineated the surfaces of neurons located mainly in layer IV but also in other layers. The staining surrounded neuronal cell bodies and dendrites in a periodic or meshwork pattern but did not label axons. VC1.1-labeled neurons were morphologically heterogeneous and included multipolar, bipolar, and bitufted classes. In the electron microscope, VC1.1 immunoreactivity surrounded presynaptic membranes of terminal boutons and intersynaptic sections of postsynaptic membranes, but was not present within terminal boutons or synaptic clefts. Both asymmetric and symmetric synapses were immunoreactive. Labeling was also observed intracellularly on VC1.1-outlined neurons, associated with perisynaptic portions of plasma membranes. Tract-tracing methods were used in conjunction with immunocytochemistry to determine whether VC1.1 identified projection neurons, local circuit neurons, or a combination of both types. Layer V and VI corticogeniculate and corticotectal projection neurons were retrogradely labeled with rhodamine fluorescent latex microspheres. In a large sample of retrogradely labeled neurons, none were VC1.1-positive, suggesting that VC1.1 stained a population of local circuit neurons. Additional immunocytochemical double-labeling studies with an antiserum to GABA and VC1.1, revealed that VC1.1-positive neurons were immunoreactive to GABA. These were a major subset of the GABAergic neurons in area 17 and tended to have medium to large cell bodies. It is concluded that VC1.1 identifies a new, immunologically distinct subset of GABAergic neurons in area 17. The restricted distribution of this antigen on perisynaptic portions of GABA-containing cells and surrounding terminal boutons onto these cells suggests that this antigen may play an important role in inhibitory cortical circuits.     

Orientational tuning of visual cortex neurons to different stimulus intensities in the cat

The orientation tuning of field 17 neurons of the visual cortex was studied in immobilized and unanesthetized cats under different intensities of test light slits and constant light background. Orientation tuning of five neurons was invariant to stimulus intensity: their preferential orientation did not change. Thirteen cells were variable as during the change of the contrast they showed a statistically significant displacement of orientation tuning from 22 degrees to 90 degrees. Changes in other neurons were not significant. Invariant neurons differed from variable ones in several characteristics. The mechanisms of orientation tuning changes during contrast variations are discussed.     

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.     

Morphological types of projection neurons in layer 5 of cat visual cortex

Pyramidal cells in layer 5 of the visual cortex have multiple cortical and subcortical projection sites. Previous studies found that many cells possess bifurcating axons and innervate more than one cortical or subcortical target, but cells projecting to both cortical and subcortical targets were not observed. The present study examines the morphology of cells in cat visual cortex projecting to the superior colliculus, the main subcortical target of layer 5, and cells in layer 5 projecting to cortical areas 18 and 19. The neurons that give rise to these different projections were retrogradely labelled and intracellularly stained in living brain slices. Our results show that cells within each projection group have several morphological features in common. All corticotectal cells have a long apical dendrite forming a large terminal tuft in layer 1. Their cell bodies are medium sized to large, and their basal dendrites form a dense and symmetrical dendritic field. Corticocortical cells in layer 5 have a very different morphology: their apical dendrites are short and they never reach higher than layers 2/3. Their cells bodies are small to medium sized and they have fewer basal dendrites than corticotectal cells. Thus there are two morphologically distinct projection systems in layer 5, one projecting to cortical and the other one to subcortical targets, suggesting that these two systems transmit different information from the visual cortex. Among the corticotectal cells with the largest cell bodies we found some cells whose basal and apical dendrites were almost devoid of spines. Spiny and spinefree corticotectal cells also have different intrinsic axon collaterals and therefore play different roles in the cortical circuitry. While many spiny corticotectal cells have axon collaterals that project to layer 6, spinefree corticotectal cells have fewer axon collaterals and these do not arborize in layer 6. We suggest that the two morphological types of corticotectal cells might be related to functional differences known to exist among these cells. We discuss how the presence or absence of spines affects the integration of the synaptic input and how this might be related to the cells' functional properties.     

Local circuitry of identified projection neurons in cat visual cortex brain slices

The relationship between pyramidal cell morphology and efferent target was investigated in layer 6 of cat primary visual cortex (area 17). Layer 6 has 2 projections, one to the lateral geniculate nucleus (LGN) and another to the visual claustrum. The cells of origin of each projection were identified by retrograde transport of fluorescent latex microspheres. The labeled cells were visualized in brain slices prepared from area 17, using an epifluorescence compound microscope modified for intracellular recording. Individual retrogradely labeled cells were penetrated and intracellularly stained with Lucifer yellow to visualize the patterns of axons and dendrites associated with each projection. The neurons that give rise to the 2 projections had very different patterns of dendrites and local axonal collaterals, but the patterns within each group were highly stereotyped. The differences between their axonal collaterals were particularly dramatic. Claustrum projecting cells had fine, horizontally directed collaterals that arborized exclusively in layer 6 and lower layer 5. Most LGN projecting cells had virtually no horizontal arborization in layer 6. Instead, they sent widespread collaterals vertically, which arborized extensively in layer 4. The apical dendrites of the 2 groups also differed markedly. Claustrum projecting cells had apical dendrites reaching to layer 1, with branches in layer 5 only, while LGN projecting cells never had an apical dendrite reaching higher than layer 3, with side branches in layers 5 and 4. Therefore, each efferent target must receive inputs from neurons whose synaptic connections within area 17 are significantly different from those of neurons projecting to other targets. This further suggests that distinct visual response properties should be associated with each projection. In addition to the claustrum and LGN projecting cells, about 20% of layer 6 pyramidal neurons lacked an efferent axon. Morphologically, most resembled LGN projecting neurons, but a few had characteristics of claustrum projecting cells. These neurons may represent cells that either failed to make an efferent connection or cells that lost an efferent axon during development. Their frequency suggests that such intrinsic, presumably excitatory, neurons may play a significant role in cortical processing.     

Effects of claustral stimulation on the properties of visual cortex neurons in the cat

To assess the possible role of the claustrum in visual processing, extracellular unit recordings were made in the striate cortex of cats during claustral stimulation. The results showed that electrical stimulation of the dorsocaudal portion of the claustrum produced a decrease in the spontaneous activity and optimal firing characteristics of visual cortical cells.     

Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex

Spiny stellate neurons of area 17 of the cat's visual cortex were physiologically characterised and injected intracellularly with horseradish peroxidase. Six neurons from sublamina 4A were selected. Five had the S-type of simple receptive fields; one had a complex receptive field. Their axons formed boutons mainly in layers 3 and 4. An electron microscopic examination of 45 boutons showed that each bouton formed one asymmetric synapse on average. Spines were the most frequent synaptic target (74%); dendritic shafts formed the remainder (26%). On the basis of ultrastructural characteristics, 8% of the target dendrites were characterised as originating from smooth γ-aminobutyrate-ergic (GABAergic) neurons. Thus the major output of spiny stellate neurons is to other spiny neurons, probably pyramidal neurons in layer 3 and spiny stellates in layer 4.     

Plasticity of cat visual cortex

Monocular eyelid closure in kittens mimics certain visual deficits in humans that result in amblyopia ex anopsia. I have now studied the effects of monocular eyelid closure in cat upon the slow-wave response recorded from visul cortex. The pattern of changes in the response closely paralleled the changes in visual function of the amblyopic eye, in particular the suppression during binocular vision.     

Distribution and morphological characterization of phosphate-activated glutaminase-immunoreactive neurons in cat visual cortex

Phosphate-activated glutaminase (PAG) is the major enzyme involved in the synthesis of the excitatory neurotransmitter glutamate in cortical neurons of the mammalian cerebral cortex. In this study, the distribution and morphology of glutamatergic neurons in cat visual cortex was monitored through immunocytochemistry for PAG. We first determined the specificity of the anti-rat brain PAG polyclonal antibody for cat brain PAG. We then examined the laminar expression profile and the phenotype of PAG-immunopositive neurons in area 17 and 18 of cat visual cortex. Neuronal cell bodies with moderate to intense PAG immunoreactivity were distributed throughout cortical layers II-VI and near the border with the white matter of both visual areas. The largest and most intensely labeled cells were mainly restricted to cortical layers III and V. Careful examination of the typology of PAG-immunoreactive cells based on the size and shape of the cell body together with the dendritic pattern indicated that the vast majority of these cells were pyramidal neurons. However, PAG immunoreactivity was also observed in a paucity of non-pyramidal neurons in cortical layers IV and VI of both visual areas. To further characterize the PAG-immunopositive neuronal population we performed double-stainings between PAG and three calcium-binding proteins, parvalbumin, calbindin and calretinin, to determine whether GABAergic non-pyramidal cells can express PAG, and neurofilament protein, a marker for a subset of pyramidal neurons in mammalian neocortex. We here present PAG as a neurochemical marker to map excitatory cortical neurons that use the amino acid glutamate as their neurotransmitter in cat visual cortex.     

Activation of the mechanism of orientation selectivity of neurons of the visual cortex of the cat by a moving noise field

Directional tuning of the striate cortex complex cells for motion of slit stimuli and visual noise field was investigated on unanesthetized cats. The investigated cells demonstrated different degree of orientational and directional sensitivity. Shifts of preferred direction for visual noise stimuli with respect to preferred direction for slit were found in orientational selective cells only. It is concluded that in spite of the fact that a visual noise field has no inherent orientation it activates orientational mechanism in the visual cortex.     

Characteristics of the coding of light stimulus intensity by visual cortex neurons during light adaptation in the cat

Response of 70 neurons in area 17 of the visual cortex to optimal stimuli of different intensity in the receptive field under conditions of photopic adaptation were analyzed in unanesthetized cats. The reaction threshold, differential sensitivity, optimal intensity and the width of the brightness range were estimated. No intensity detectors were found in this area. 70% of neurons studied had inhibitory distortion in the range of their intensity functions. The neurons differed in their threshold reactions by 5-6 orders, in dynamic range--by 3-4 orders, and in differential sensitivity--by 2-3 orders. The visual cortex neurons with receptive fields in central and periphery parts of the visual field had different intensity functions.     

A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex

The nonpyramidal neurons in area 17 of cat visual cortex have been examined in Golgi preparations. From their dendritic patterns, neurons are classified as being multipolar, bitufted, or bipolar, and on the basis of the abundance of dendritic spines as spinous, sparsely spinous, or smooth. When neurons are so classified seven different types of nonpyramidal neurons are encountered in layers II through V. Three of the types of multipolar neurons in layers II through V have spherical dendritic trees. The small multipolar cells have smooth dendrites and are the smallest neurons in the cortex. They have short dendrites and dense local axonal plexuses and occur throughout layers II to V The sparsely spinous stellate cells have longer dendrites, are confined to layer II/III, and have local axonal arborizations, whereas the spinous stellate cells are limited to layer IV. A fourth type of multipolar neuron in layers II through V is the basket cell. Such neurons have elongate dendritic trees and either smooth or sparsely spinous dendrites. Depending upon the orientation of the neurons in the sections, their axons appear to form arcades or long, horizontally extended branches, or a mixture of these two axonal patterns. The terminal portions of the axons of these basket cells pass around the cell bodies of adjacent neurons. The two types of bitufted neurons in layers II through V have vertically oriented dendritic trees. One type, the chandelier cell, has smooth dendrites and a characteristic axon forming vertical strings of terminals. The other sparsely spinous bitufted neurons have axons producing vertically oriented plexuses. The remaining type of neuron encountered in layers II through V is a bipolar cell. The bipolar cell has a single major dendritic trunk arising from each pole of the cell body, and each of these gives rise to a very narrow, long, and vertically oriented dendritic tree. The axon usually takes origin from one of the primary dendrites. In layer I are horizontally oriented, bitufted cells with smooth dendrites. The axons of these horizontal cells of layer I arise from one of the primary dendritic trunks and appear to form a plexus confined to layer I. Horizontally oriented neurons are also present in deep layer VI, but the horizontal cells of layer VI are bipolar. The other two neuronal types in layer VI are multipolar cells with sparsely spinous dendrites. The larger of these two types resembles the basket cells in layers II through V, the only important difference between them being that in addition to the long horizontal branches, the axons of the basket cells of layer VI have a long ascending branch which reaches at least as far as layer IV. The other sparsely spinous cells of layer VI are medium sized. Their axons take a descending and oblique course before elaborating a locally distributed plexus. The various types of neurons defined in this study are compared with neurons described by previous authors who have examined the populations of nonpyramidal cells in area 17 of cat visual cortex and in other visual and nonvisual cortical areas of cats, monkeys, and rodents. In some cases it has been possible to postulate the functional roles that particular types of neurons might play within cat visual cortex.