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A new framework for measuring densities of immunolabeled neurons across cortical layers was implemented that combines a confocal microscopy sampling strategy with automated analysis of 3D image stacks. Its utility was demonstrated by quantifying neuronal density in macaque cortical areas V1 and V2. A series of overlapping confocal image stacks were acquired, each spanning from the pial surface to the white matter. DAPI channel images were automatically thresholded, and contiguous regions that included multiple clumped nuclear profiles were split using k -means clustering of image pixels for a set of candidate k values determined based on the clump’s area; the most likely candidate segmentation was selected based on criteria that capture expected nuclear profile shape and size. The centroids of putative nuclear profiles estimated from 2D images were then grouped across z planes in an image stack to identify the positions of nuclei in x – y – z . 3D centroids falling outside user-specified exclusion boundaries were deleted, nuclei were classified by the presence or absence of signal in a channel corresponding to an immunolabeled antigen (e.g., the pan-neuronal marker NeuN) at the nuclear centroid location, and the set of classified cells was combined across image stacks to estimate density across cortical depth. The method was validated by comparison with conventional stereological methods. The average neuronal density across cortical layers was 230 × 10 3 neurons per mm 3 in V1 and 130 × 10 3 neurons per mm 3 in V2. The method is accurate, flexible, and general enough to measure densities of neurons of various molecularly identified types.

Complex scene perception depends upon the interaction between signals from the classical receptive field (CRF) and the extra-classical receptive field (eCRF) in primary visual cortex (V1) neurons. Although much is known about V1 eCRF properties, we do not yet know how the underlying mechanisms map onto the cortical microcircuit. We probed the spatio-temporal dynamics of eCRF modulation using a reverse correlation paradigm, and found three principal eCRF mechanisms: tuned-facilitation, untuned-suppression, and tuned-suppression. Each mechanism had a distinct timing and spatial profile. Laminar analysis showed that the timing, orientation-tuning, and strength of eCRF mechanisms had distinct signatures within magnocellular and parvocellular processing streams in the V1 microcircuit. The existence of multiple eCRF mechanisms provides new insights into how V1 responds to spatial context. Modeling revealed that the differences in timing and scale of these mechanisms predicted distinct patterns of net modulation, reconciling many previous disparate physiological and psychophysical findings.

The Kv3.1b potassium channel subunit, which facilitates the fast-spiking phenotype characteristic of parvalbumin (PV)-expressing inhibitory interneurons, is also expressed by subpopulations of excitatory neurons in macaque cortex. We have previously shown that V1 neurons expressing Kv3.1b but not PV or GABA were largely concentrated within layers 4Cα and 4B of V1, suggesting laminar or pathway specificity. In the current study, the distribution and pattern of co-immunoreactivity of GABA, PV, and Kv3.1b across layers in extrastriate cortical areas V2 and MT of the macaque monkey were measured using the same triple immunofluorescence labeling, confocal microscopy, and partially automated cell-counting strategies used in V1. For comparison, densities of the overall cell and neuronal populations were also measured for each layer of V2 and MT using tissue sections immunofluorescence labeled for the pan-neuronal marker NeuN. GABAergic neurons accounted for 14% of the total neuronal population in V2 and 25% in MT. Neurons expressing Kv3.1b but neither GABA nor PV were present in both areas. This subpopulation was most prevalent in the lowest subcompartment of layer 3, comprising 5% of the total neuronal population in layer 3C of both areas, and 41% and 36% of all Kv3.1b+ neurons in this layer in V2 and MT, respectively. The prevalence and laminar distribution of this subpopulation were remarkably consistent between V2 and MT and showed a striking similarity to the patterns observed previously in V1, suggesting a common contribution to the cortical circuit across areas.

Perceptually, color is used to discriminate objects by hue and to identify color boundaries. The primate retina and the lateral geniculate nucleus (LGN) have cell populations sensitive to color modulation, but the role of the primary visual cortex (V1) in color signal processing is uncertain. We re-evaluated color processing in V1 by studying single-neuron responses to luminance and to equiluminant color patterns equated for cone contrast. Many neurons respond robustly to both equiluminant color and luminance modulation (color-luminance cells). Also, there are neurons that prefer luminance (luminance cells), and a few neurons that prefer color (color cells). Surprisingly, most color-luminance cells are spatial-frequency tuned, with approximately equal selectivity for chromatic and achromatic patterns. Therefore, V1 retains the color sensitivity provided by the LGN, and adds spatial selectivity for color boundaries.

Orientation tuning of neurons is one of the chief emergent characteristics of the primary visual cortex, VI (refs 1,2). Neurons of the lateral geniculate nucleus, which comprise the thalamic input to VI, are not orientation-tuned, but the majority of VI neurons are quite selective. How orientation tuning arises within VI is still controversial 1,3–17 . To study this problem, we measured how the orientation tuning of neurons evolves with time 18–20 using a new method: reverse correlation in the orientation domain. Orientation tuning develops after a delay of 30–45 milliseconds and persists for 40–85 ms. Neurons in layers 4Cα or 4Cβ, which receive direct input from the thalamus, show a single orientation preference which remains unchanged throughout the response period. In contrast, the preferred orientations of output layer neurons (in layers 2,3,4B, 5 or 6) usually change with time, and in many cases the orientation tuning may have more than one peak. This difference in dynamics is accompanied by a change in the sharpness of orientation tuning; cells in the input layers are more broadly tuned than cells in the output layers. Many of these observed properties of output layer neurons cannot be explained by simple feedforward models 1,3–6 , whereas they arise naturally in feedback networks 7–17 . Our results indicate that VI is more than a bank of static oriented filters; the dynamics of output layer cells appear to be shaped by intracortical feedback.

The S-cone system is closely linked to the perception of blue/yellow. The trichromatic system of Old-World monkeys and humans has relatively few S-cones in the fovea. In this study, we investigated the distribution of putative S-cone afferents in macaques primary visual cortex (V1) which form a characteristic honeycomb arrangement in layer 4A. It was hypothesized that if there were a low number of S-cone opponent projecting neurons in central vision then this would be seen as a reduction in afferents in foveal layer 4A. Recent studies have shown that the vesicular glutamate transporter 2 (VGlut2) is a marker for thalamic afferent terminals in cortex. The distribution of VGlut2-immunoreactive (-ir) terminals was studied in the foveal and perifoveal representation of V1. It was found that there was a substantial reduction in the terminal density in the foveal representation: the density was 5–6 times lower in the foveal V1 than in regions representing perifoveal eccentricities of 1°–2° and beyond. These findings may provide the cortical substrate of foveal tritanopia, the reduced blue perceptual ability for small fields in the center of gaze.

Stimulation outside the receptive field of a primary visual cortical (V1) neuron reveals intracortical neural interactions 1 , 2 , 3 , 4 , 5 , 6 . However, previous investigators implicitly or explicitly considered the extent of cortical spatial summation and, therefore, the size of the classical receptive field to be fixed and independent of stimulus characteristics or of surrounding context. On the contrary, we found that the extent of spatial summation in macaque V1 neurons depended on contrast, and was on average 2.3-fold greater at low contrast. This adaptive increase in spatial summation at low contrast was seen in cells throughout V1 and was independent of surround inhibition.

This paper offers a theory for the origin of direction selectivity (DS) in the macaque primary visual cortex, V1. DS is essential for the perception of motion and control of pursuit eye movements. In the macaque visual pathway, neurons with DS first appear in V1, in the Simple cell population of the Magnocellular input layer 4Cα. The lateral geniculate nucleus (LGN) cells that project to these cortical neurons, however, are not direction selective. We hypothesize that DS is initiated in feed-forward LGN input, in the summed responses of LGN cells afferent to a cortical cell, and it is achieved through the interplay of 1) different visual response dynamics of ON and OFF LGN cells and 2) the wiring of ON and OFF LGN neurons to cortex. We identify specific temporal differences in the ON/OFF pathways that, together with item 2, produce distinct response time courses in separated subregions; analysis and simulations confirm the efficacy of the mechanisms proposed. To constrain the theory, we present data on Simple cells in layer 4Cα in response to drifting gratings. About half of the cells were found to have high DS, and the DS was broadband in spatial and temporal frequency (SF and TF). The proposed theory includes a complete analysis of how stimulus features such as SF and TF interact with ON/OFF dynamics and LGN-to-cortex wiring to determine the preferred direction and magnitude of DS.

Understanding the synaptic characteristics of each cortical layer is essential for elucidating the functional architecture of each brain region. In the current study, we made a detailed quantitative comparison of the synaptic structure in the predominantly input layers of primate primary visual cortex (layer 4C) and in the predominant output layer (layer 3B) using focused ion beam scanning electron microscopy (FIB/SEM). We quantified the synaptic density in each layer, classified synaptic boutons according to their number of synapses and mitochondrial content, and quantified key morphometric parameters, including bouton volume, postsynaptic density (PSD) area and morphology, volume occupied by mitochondria, and postsynaptic targets. Our results revealed that for all the layers there is a higher proportion of single-synapse boutons without mitochondria. Multisynaptic boutons containing mitochondria (MSBm+)- which likely correspond to TC terminals -were significantly more abundant in the thalamocortical recipient layers 4Cα and 4Cβ. These MSBm+ boutons were also larger, more likely to contact dendritic spines, and contained more mitochondria than other bouton categories. In contrast, layer 3B, displayed a lower prevalence of MSBm+ boutons, these boutons were smaller than those in layer 4C and made fewer synapses. These findings highlight laminar differences in bouton architecture and support the idea that TC synapses are structurally adapted to support high synaptic efficacy. Together, our data provide a detailed quantitative framework for understanding the synaptic organization of primate V1, with implications for sensory processing and cortical circuit function.