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PubMed2000

Membrane potential and firing rate in cat primary visual cortex.

We have investigated the relationship between membrane potential and firing rate in cat visual cortex and found that the spike threshold contributes substantially to the sharpness of orientation tuning. The half-width at half-height of the tuning of the spike responses was 23 +/- 8 degrees, compared with 38 +/- 15 degrees for the membrane potential responses. Direction selectivity was also greater in spike responses (direction index, 0.61 +/- 0.35) than in membrane potential responses (0.28 +/- 0.21). Threshold also increased the distinction between simple and complex cells, which is commonly based on the linearity of the spike responses to drifting sinusoidal gratings. In many simple cells, such stimuli evoked substantial elevations in the mean potential, which are nonlinear. Being subthreshold, these elevations would be hard to detect in the firing rate responses. Moreover, just as simple cells displayed various degrees of nonlinearity, complex cells displayed various degrees of linearity. We fitted the firing rates with a classic rectification model in which firing rate is zero at potentials below a threshold and grows linearly with the potential above threshold. When the model was applied to a low-pass-filtered version of the membrane potential (with spikes removed), the estimated values of threshold (-54.4 +/- 1.4 mV) and linear gain (7.2 +/- 0.6 spikes. sec(-1). mV(-1)) were similar across the population. The predicted firing rates matched the observed firing rates well and accounted for the sharpening of orientation tuning of the spike responses relative to that of the membrane potential. As it was for stimulus orientation, threshold was also independent of stimulus contrast. The rectification model accounted for the dependence of spike responses on contrast and, because of a stimulus-induced tonic hyperpolarization, for the response adaptation induced by prolonged stimulation. Because gain and threshold are unaffected by visual stimulation and by adaptation, we suggest that they are constant under all conditions.

Action Potentials↗
PubMed2001

Contextual modulation in primary visual cortex of macaques.

Recent studies have suggested that V1 neurons extract figures from their backgrounds, in that they respond better to interior features of figures than to equivalent features of background stimuli. This is reportedly true even when the figure boundaries are distant from the borders of the classical receptive field (RF). To test the role of V1 neurons in figure-ground segregation, we recorded their responses to texture figures on texture backgrounds, centered on the RF. The texture elements of the figures remained identical across trials, and figure boundaries were defined by orientation differences between the elements in the background texture relative to elements in the figure. For nearly all neurons (98/102), responses to a large texture figure did not differ from the responses to a uniform-texture background. Although many neurons gave enhanced responses to texture boundaries, this occurred only when the boundaries were within or close to the RF borders. Similar effects were found in V2. For neurons in V1, the limited spatial extent of the contextual modulation was not increased either at low stimulus contrast or when the animal was rewarded for detecting an orientation-defined figure. Thus, V1 neurons appear to signal texture boundaries rather than figures per se. Unexpectedly, many V1 neurons gave significant long-latency responses to texture stimuli located entirely outside the classical RF, up to 5 degrees from the RF border in some cases. However, these responses did not depend on the stimulus forming a figure that contained the RF. Although V1 neurons are influenced by stimuli outside the classical RF, they do not appear to segregate figures from ground.

Animals↗
PubMed2001

Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1).

The spatial structure of color cell receptive fields is controversial. Here, spots of light that selectively modulate one class of cones (L, M, or S, or loosely red, green, or blue) were flashed in and around the receptive fields of V-1 color cells to map the spatial structure of the cone inputs. The maps generated using these cone-isolating stimuli and an eye-position-corrected reverse correlation technique produced four findings. First, the receptive fields were Double-Opponent, an organization of spatial and chromatic opponency critical for color constancy and color contrast. Optimally stimulating both center and surround subregions with adjacent red and green spots excited the cells more than stimulating a single subregion. Second, red-green cells responded in a luminance-invariant way. For example, red-on-center cells were excited equally by a stimulus that increased L-cone activity (appearing bright red) and by a stimulus that decreased M-cone activity (appearing dark red). This implies that the opponency between L and M is balanced and argues that these cells are encoding a single chromatic axis. Third, most color cells responded to stimuli of all orientations and had circularly symmetric receptive fields. Some cells, however, showed a coarse orientation preference. This was reflected in the receptive fields as oriented Double-Opponent subregions. Fourth, red-green cells often responded to S-cone stimuli. Responses to M- and S-cone stimuli usually aligned, suggesting that these cells might be red-cyan. In summary, red-green (or red-cyan) cells, along with blue-yellow and black-white cells, establish three chromatic axes that are sufficient to describe all of color space.

Animals↗
PubMed2001

Layer-specific input to distinct cell types in layer 6 of monkey primary visual cortex.

Layer 6 of monkey V1 contains a physiologically and anatomically diverse population of excitatory pyramidal neurons. Distinctive arborization patterns of axons and dendrites within the functionally specialized cortical layers define eight types of layer 6 pyramidal neurons and suggest unique information processing roles for each cell type. To address how input sources contribute to cellular function, we examined the laminar sources of functional excitatory input onto individual layer 6 pyramidal neurons using scanning laser photostimulation. We find that excitatory input sources correlate with cell type. Class I neurons with axonal arbors selectively targeting magnocellular (M) recipient layer 4Calpha receive input from M-dominated layer 4B, whereas class I neurons whose axonal arbors target parvocellular (P) recipient layer 4Cbeta receive input from P-dominated layer 2/3. Surprisingly, these neuronal types do not differ significantly in the inputs they receive directly from layers 4Calpha or 4Cbeta. Class II cells, which lack dense axonal arbors within layer 4C, receive excitatory input from layers targeted by their local axons. Specifically, type IIA cells project axons to and receive input from the deep but not superficial layers. Type IIB neurons project to and receive input from the deepest and most superficial, but not middle layers. Type IIC neurons arborize throughout the cortical layers and tend to receive inputs from all cortical layers. These observations have implications for the functional roles of different layer 6 cell types in visual information processing.

Animals↗
PubMed2001

Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex.

Hundreds of thalamic axons ramify within a column of cat visual cortex; yet each layer 4 neuron receives input from only a fraction of them. We have examined the specificity of these connections by recording simultaneously from layer 4 simple cells and cells in the lateral geniculate nucleus with spatially overlapping receptive fields (n = 221 cell pairs). Because of the precise retinotopic organization of visual cortex, the geniculate axons and simple-cell dendrites of these cell pairs should have overlapped within layer 4. Nevertheless, monosynaptic connections were identified in only 33% of all cases, as estimated by cross-correlation analysis. The visual responses of monosynaptically connected geniculate cells and simple cells were closely related. The probability of connection was greatest when a geniculate center overlapped a strong simple-cell subregion of the same sign (ON or OFF) near the center of the subregion. This probability was further increased when the time courses of the visual responses were similar. In addition, the connections were strongest when the simple-cell subregion and the geniculate center were matched in position, sign, and size. The rules of connectivity between geniculate afferents and simple cells resemble those found for retinal afferents to geniculate cells. The connections along the retinogeniculocortical pathway, therefore, show a precision that goes beyond simple retinotopy to include many other response properties, such as receptive-field sign, timing, subregion strength, and size. This specificity in wiring emphasizes the need for developmental mechanisms (presumably correlation-based) that can select among afferents that differ only slightly in their response properties.

Action Potentials↗
PubMed1990

Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey.

We tested color and contrast sensitivity in the magnocellular and parvocellular subdivisions of the lateral geniculate body and in layers 2, 3, 4B, and 4C alpha of visual area 1 to obtain physiological data on the degree of segregation of the 2 pathways and on the fate of the color and contrast information as it is transmitted from the geniculate to the cortex. On average, magnocellular geniculate cells were much less responsive than parvocellular cells to shifts between 2 equiluminant colors. Nevertheless, many magnocellular cells (though not all) continued to give some response at equiluminance. As expected from previous studies, luminance contrast sensitivity differed markedly between magnocellular and parvocellular layers. In V-1, the properties of cells in the magnorecipient layers 4C alpha and 4B faithfully reflected the properties of magnocellular geniculate cells, showing no evidence of any parvocellular input. Like magnocellular geniculate cells, they showed high contrast sensitivity, and with color contrast stimuli they showed large response decrements at equiluminance. In the interblob regions of cortical layers 2 and 3, which anatomically appear to receive most of their inputs from parvorecipient layer 4C beta, contrast sensitivities of some of the cells were compatible with a predominantly parvocellular input. Other interblob cells had sensitivities intermediate between magno- and parvocellular geniculate cells, suggesting a possible contribution from the magnocellular system. Many cells in cortical layers 2 and 3 responded to color-contrast borders equally well at all relative brightnesses of the 2 colors, including equiluminance. We recorded from many direction- and disparity-selective cells in V-1: most of the direction-selective and all of the clearly stereo-selective cells were located in layer 4B.

Animals↗
PubMed1986

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↗
PubMed1984

Specificity of intrinsic connections in primate primary visual cortex.

Several recent studies have suggested a patchy system of intrinsic lateral connections in area 17 of the macaque monkey. To see whether this pattern bore any relationship to the cytochrome oxidase blobs we made multiple tiny injections of horseradish peroxidase into layers 2 and 3 of area 17, small enough so that some of the injections (or their cores) were entirely inside a single blob, or entirely outside. When the injection centers were entirely in blobs, the label in layers 2 and 3 was transported preferentially to nearby blobs, avoiding nonblob areas. When the injections were in nonblob areas, the label was found predominantly in surrounding nonblob areas, avoiding the blobs. Besides this lateral transport, label was also present in the layers below 2 and 3: the label in layers 4 and 6 was very restricted, occupying roughly the diameter of the injection core and presumably representing axons of cell bodies at the injection site; in layer 5 diffusely labeled patches observed the same blob/nonblob segregation seen above layer 4.

Animals↗
PubMed1984

[Demonstration of an effect of (3H)-L-proline on the number of dendritic spines on stellate cells of the primary visual cortex in Macaca during the critical period].

A morphometric study in cortical layer IVC of Macaca area 17 was performed during the critical period. A 20% increase in the number of dendritic spines was observed in neurons with horizontal dendritic tree in the cortical sublayer IVC alpha after an intraocular injection of (3H)-L-proline. A neuroactive role of this amino acid is discussed.

Animals↗
PubMed1995

Differential properties of cells in the feline primary visual cortex providing the corticofugal feedback to the lateral geniculate nucleus and visual claustrum.

We have examined the responses of 141 layer VI cells in the feline visual cortex. Within this group we compared the responses of a subpopulation of cells checked for connectivity by electrical stimulation in the dLGN and the visual claustrum. The antidromically identified corticogeniculate projecting cells had relatively short receptive fields, as judged from length response curves, measured quantitatively, and were located at the "short" end of the receptive field length spectrum seen in the general population. Of the 17 corticogeniculate projecting cells, 71% were S type cells, which were typically monocular and directionally selective, with relatively long latencies following electrical stimulation. The remaining 29% were C type cells, also directionally selective, but with a wider spread of ocular dominance preferences and shorter latencies following electrical stimulation. S and C type subpopulations did not differ in their receptive field lengths. The mean receptive field length for this subpopulation was 2.2 degrees +/- 0.27, the shortest field being 1 degrees and the longest 5 degrees. The five layer VI cells activated by electrical stimulation from electrodes within the dorsocaudal (visual) claustrum all had much longer receptive field lengths than the corticogeniculate population, often 10 degrees or longer and were monocular and directionally selective S type cells. These data indicate that the information carried in the corticogeniculate stream (and that from layer VI directly to layer IV carried by axon collaterals) is relatively tightly focused in spatial terms whilst the less spatially focused, long receptive field output from layer VI projects to the claustrum.

Animals↗
PubMed1995

Cytochrome-oxidase blobs in cat primary visual cortex.

Cytochrome-oxidase blobs are central to two of the most influential ideas in contemporary visual neuroscience--cortical modularity and parallel processing pathways. In particular, the regular 2D array of cytochrome-oxidase-rich blobs in primate visual cortex is arguably the most compelling evidence for cortical modularity and has been hypothesized to mark a separate processing stream through the visual cortex. Although previously a variety of mammals have been studied, blobs have only been demonstrated in the visual cortex of primates, which has led to the conclusion that blobs represent a primate-specific feature of visual cortical organization. Here we demonstrate the presence of cytochrome-oxidase blobs in a nonprimate species. Throughout the full tangential extent of layers II-III in cat visual cortex the cytochrome-oxidase staining pattern is distinctly patchy, with the darkly stained blobs forming a regular 2D array. In addition, the blobs in cat visual cortex are functionally related to the underlying ocular dominance columns. The presence of cytochrome-oxidase blobs in the cat clearly demonstrates that they no longer can be considered a primate-specific feature of visual cortical organization.

Animals↗
PubMed1996

Contextual modulation in primary visual cortex.

We studied extra-receptive field contextual modulation in area V1 of awake, behaving macaque monkeys. Contextual modulation was studied using texture displays in which texture covering the receptive field (RF) was the same in all trials, but the perceptual context of this texture could vary depending on the configuration of extra-RF texture elements. We found robust contextual modulation when disparity, color, luminance, and orientation cues variously defined a textured figure centered on the RF of V1 neurons. We found contextual modulation to have a spatial extent of approximately 8 to 10 degrees diameter parafoveally. Contextual modulation correlated with perceptual experience of both binocularly rivalrous texture displays and of displays with a simple example of surface occlusion. We found contextual modulation in V1 to have a characteristic latency of 80-100 msec after stimulus onset, potentially allowing feedback from extrastriate areas to underlie to this effect.

Animals↗
PubMed1998

Functional streams and local connections of layer 4C neurons in primary visual cortex of the macaque monkey.

The primate visual system is composed of multiple, functionally specialized cortical areas. The functional diversity among areas is thought to reflect different contributions from early parallel visual pathways to the area V1 neurons providing input to "higher" cortical areas. The M pathway is believed to provide information about motion and contrast, via layer 4B of V1, to dorsal visual areas. The P pathway is believed to provide information about shape and color, via layer 2/3 of V1, to ventral visual areas, with specialized contributions from cytochrome-oxidase (CO) blob versus interblob neurons. However, the detailed anatomical relationships between the M and P pathways and the neurons in V1 that provide input to higher extrastriate cortical areas are poorly understood. To study these relationships, spiny stellate neurons in the M- and P-recipient layers of V1, 4Calpha and 4Cbeta, respectively, were intracellularly labeled, and their axonal and dendritic arbors were reconstructed. We find that neurons with dendrites in upper layer 4Calpha project axons to layer 4B and CO blobs in layer 2/3, thus relaying M input to these regions. Other neurons in lower layer 4Calpha provide M input to interblobs. These cells have either (1) dendrites restricted to lower layer 4Calpha and axons specifically targeting layer 2/3 interblobs, or (2) dendrites in lower 4Calpha and 4Cbeta and axons targeting blobs and interblobs. P-recipient layer 4Cbeta neurons have dense axonal arbors in both blobs and interblobs but not layer 4B. Quantitative analyses reveal that 4Calpha cells provide approximately five times more synapses than 4Cbeta cells to layer 4B, whereas 4Cbeta cells provide five times more synapses than 4Calpha cells to layer 2/3. These observations imply that M input is dominant in layer 4B. In layer 2/3, both blobs and interblobs receive M and P input, but the P input is dominant, and M input to interblobs derives exclusively from a subpopulation of M afferents that targets lower 4Calpha, not from afferents targeting only upper 4Calpha (cf. Blasdel and Lund, 1983). We speculate that the M and P pathways to interblobs are "X-like" linear systems, whereas blobs also receive nonlinear "Y-like" M input.

Animals↗
PubMed1998

Synaptic and neurochemical characterization of parallel pathways to the cytochrome oxidase blobs of primate visual cortex.

The primary visual cortex (V1) of primates is unique in that it is both the recipient of visual signals, arriving via parallel pathways (magnocellular [M], parvocellular [P], and koniocellular [K]) from the thalamus, and the source of several output streams to higher order visual areas. Within this scheme, output compartments of V1, such as the cytochrome oxidase (CO) rich blobs in cortical layer III, synthesize new output pathways appropriate for the next steps in visual analysis. Our chief aim in this study was to examine and compare the synaptic arrangements and neurochemistry of elements involving direct lateral geniculate nucleus (LGN) input from the K pathway with those involving indirect LGN input from the M and P pathways arriving from cortical layer IV. Geniculocortical K axons were labeled via iontophoretic injections of wheat germ agglutinin-horseradish peroxidase into the LGN and intracortical layer IV axons (indirect P and M pathways to the CO-blobs) were labeled by iontophoretic injections of Phaseolus vulgaris leucoagglutinin into layer IV. The neurochemical content of both pre- and postsynaptic profiles was identified by postembedding immunocytochemistry for gamma-amino butyric acid (GABA) and glutamate. Sizes of pre- and postsynaptic elements were quantified by using an image analysis system, BioQuant IV. Our chief finding is that K LGN axons and layer IV axons (indirect input from M and P pathways) exhibit different synaptic relationships to CO blob cells. Specifically, our results show that within the CO blobs: 1) all K cell axons contain glutamate, and the vast majority of layer IV axons contain glutamate with only 5% containing GABA; 2) K axons terminate mainly on dendritic spines of glutamatergic cells, while layer IV axons terminate mainly on dendritic shafts of glutamatergic cells; 3) K axons have larger boutons and contact larger postsynaptic dendrites, which suggests that they synapse closer to the cell body within the CO blobs than do layer IV axons. Taken together, these results suggest that each input pathway to the CO blobs uses a different strategy to contribute to the processing of visual information within these compartments.

Animals↗