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Spatial transitions in color can aid any visual perception task, and its neural representation, the "integration of color and form," is thought to begin at primary visual cortex (V1). Integration of color and form is untested in mouse V1, yet studies show that the ventral retina provides the necessary substrate from green-sensitive rods and ultraviolet-sensitive cones. Here, we used two-photon imaging in V1 to measure spatial frequency (SF) tuning along four axes of rod and cone contrast space, including luminance and color. We first reveal that V1's sensitivity to color is similar to luminance, yet average SF tuning is significantly shifted lowpass for color. Next, guided by linear models, we used SF tuning along all four color axes to estimate the proportion of neurons that fall into classic models of color opponency, i.e., "single-," "double-," and "non-opponent." Few neurons (~6%) fit the criteria for double opponency, which are uniquely tuned for chromatic borders. Most of the population can be described as a unimodal distribution ranging from strongly single-opponent to non-opponent. Consistent with recent studies of the rodent and primate retina, our V1 data are well-described by a simple model in which ON and OFF channels to V1 sample the photoreceptor mosaic randomly. Finally, an analysis comparing color opponency to preferred orientation and retinotopy further validates rods, and not cone M-opsin, as opponent with cone S-opsin in the upper visual field. [ABSTRACT FROM AUTHOR]

The visual system adapts to maintain sensitivity and selectivity over a large range of luminance intensities. One way that the retina maintains sensitivity across night and day is by switching between rod and cone photoreceptors, which alters the receptive fields and interneuronal correlations of retinal ganglion cells (RGCs). While these adaptations allow the retina to transmit visual information to the brain across environmental conditions, the code used for that transmission varies. To determine how downstream targets encode visual scenes across light levels, we measured the effects of luminance adaptation on thalamic and cortical population activity. While changes in the retinal output are evident in the lateral geniculate nucleus (LGN), selectivity in the primary visual cortex (V1) is largely invariant to the changes in luminance. We show that the visual system could maintain sensitivity across environmental conditions without altering cortical selectivity through the convergence of parallel functional pathways from the thalamus to the cortex. [Display omitted] • Adaptation alters the thalamic neural code between scotopic and photopic luminance • Visual cortex exhibits largely luminance-invariant selectivity and noise correlations • The convergence of parallel pathways can generate a luminance-invariant code O'Shea et al. investigates how the transition between cone- and rod-mediated vision affects neural representations in central visual areas of the mouse. Whereas the thalamus inherits luminance-dependent functional properties from the retina, visual cortex exhibits a luminance-invariant code. The convergence of parallel afferent pathways can generate a luminance-invariant code. [ABSTRACT FROM AUTHOR]

Studies in the mouse retina have characterized the spatial distribution of an anisotropic ganglion cell and photoreceptor mosaic, which provides a solid foundation to study how the cortex pools from afferent parallel color channels. In particular, the mouse’s retinal mosaic exhibits a gradient of wavelength sensitivity along its dorsoventral axis. Cones at the ventral extreme mainly express S opsin, which is sensitive to ultraviolet (UV) wavelengths. Then, moving toward the retina’s dorsal extreme, there is a transition to M-opsin dominance. Here, we tested the hypothesis that the retina’s opsin gradient is recapitulated in cortical visual areas as a functional map of wavelength sensitivity. We first identified visual areas in each mouse by mapping retinotopy with intrinsic signal imaging (ISI). Next, we measured ISI responses to stimuli along different directions of the S- and M-color plane to quantify the magnitude of S and M input to each location of the retinotopic maps in five visual cortical areas (V1, AL, LM, PM, and RL). The results illustrate a significant change in the S:M-opsin input ratio along the axis of vertical retinotopy that is consistent with the gradient along the dorsoventral axis of the retina. In particular, V1 populations encoding the upper visual field responded to S-opsin contrast with 6.1-fold greater amplitude than to M-opsin contrast. V1 neurons encoding lower fields responded with 4.6-fold greater amplitude to M- than S-opsin contrast. The maps in V1 and higher visual areas (HVAs) underscore the significance of a wavelength sensitivity gradient for guiding the mouse’s behavior. [ABSTRACT FROM AUTHOR]

To guide future experiments aimed at understanding the mouse visual system, it is essential that we have a solid handle on the global topography of visual cortical areas. Ideally, the method used to measure cortical topography is objective, robust, and simple enough to guide subsequent targeting of visual areas in each subject. We developed an automated method that uses retinotopic maps of mouse visual cortex obtained with intrinsic signal imaging (Schuett et al., 2002; Kalatsky and Stryker, 2003; Marshel et al., 2011) and applies an algorithm to automatically identify cortical regions that satisfy a set of quantifiable criteria for what constitutes a visual area. This approach facilitated detailed parcellation of mouse visual cortex, delineating nine known areas (primary visual cortex, lateromedial area, anterolateral area, rostrolateral area, anteromedial area, posteromedial area, laterointermediate area, posterior area, and postrhinal area), and revealing two additional areas that have not been previously described as visuotopically mapped in mice (laterolateral anterior area and medial area). Using the topographic maps and defined area boundaries from each animal, we characterized several features of map organization, including variability in area position, area size, visual field coverage, and cortical magnification. We demonstrate that higher areas in mice often have representations that are incomplete or biased toward particular regions of visual space, suggestive of specializations for processing specific types of information about the environment. This work provides a comprehensive description of mouse visuotopic organization and describes essential tools for accurate functional localization of visual areas. [ABSTRACT FROM AUTHOR]

A characteristic feature in the primary visual cortex is that visual responses are suppressed as a stimulus extends beyond the classical receptive field. Here, we examined the role of inhibitory neurons expressing somatostatin (SOM+) or parvalbumin (PV+) on surround suppression and preferred receptive field size. We recorded multichannel extracellular activity in VI of transgenic mice expressing channelrhodopsin in SOM 1 neurons or PV + neurons. Preferred size and surround suppression were measured using drifting square-wave gratings of varying radii and at two contrasts. Consistent with findings in primates, we found that the preferred size was larger for lower contrasts across all cortical depths, whereas the suppression index (SI) showed a trend to decrease with contrast. We then examined the effect of these metrics on units that were suppressed by photoactivation of either SOM+ or PV+ neurons. When activating SOM + neurons, we found a significant increase in SI at cortical depths >400 /nm, whereas activating PV ' neurons caused a trend toward lower Sis regardless of cortical depth. Conversely, activating PV neurons significantly increased preferred size across all cortical depths, similar to lowering contrast, whereas activating SOM+ neurons had no systematic effect on preferred size across all depths. These data suggest that SOM ' and PV+ neurons contribute differently to spatial integration. Our findings are compatible with the notion that SOM+ neurons mediate surround suppression, particularly in deeper cortex, whereas PV+ activation decreases the drive of the input to cortex and therefore resembles the effects on spatial integration of lowering contrast. [ABSTRACT FROM AUTHOR]

Orientation and spatial frequency tuning are highly salient properties of neurons in primary visual cortex (V1). The combined organization of these particular tuning properties in the cortical space will strongly shape the V1 population response to different visual inputs, yet it is poorly understood. In this study, we used two-photon imaging in macaque monkey V1 to demonstrate the three-dimensional cell-by-cell layout of both spatial frequency and orientation tuning. We first found that spatial frequency tuning was organized into highly structured maps that remained consistent across the depth of layer II/III, similarly to orientation tuning. Next, we found that orientation and spatial frequency maps were intimately related at the fine spatial scale observed with two-photon imaging. Not only did the map gradients tend notably toward orthogonality, but they also co-varied negatively from cell to cell at the spatial scale of cortical columns. [ABSTRACT FROM AUTHOR]

Numerous studies have revealed traveling waves of activity in sensory cortex, both following sensory stimulation and during ongoing activity. We contributed to this body of work by measuring the spike-triggered average of the local field potential (stLFP) at multiple concurrent locations (Nauhaus et al., 2009) in the visual cortex of anesthetized cats and macaques.Wefound the stLFP to be progressively delayed at increasing distances from the site of the triggering spikes, and interpreted this as a traveling wave of depolarization originating from that site. Our results were criticized, however, on two grounds. First, a study using the same recording techniques in the visual cortex of awake macaques reported an apparent lack of traveling waves, and proposed that traveling waves could arise artifactually from excessive filtering of the field potentials (Ray and Maunsell, 2011). Second, the interpretability of the stLFP was questioned (Kenneth Miller, personal communication), as the stLFP must reflect not only interactions between spike trains and field potentials, but also correlations within and across the spike trains. Here, we show that our data and interpretation are not imperiled by these criticisms. We reanalyzed our field potentials to remove any possible artifact due to filtering and to discount the effects of correlations within and across the triggering spike trains. In both cases, we found that the traveling waves were still present. In fact, closer inspection of Ray and Maunsell's (2011) data from awake cortex shows that they do agree with ours, as they contain clear evidence for traveling waves. [ABSTRACT FROM AUTHOR]

Summary: The local field potential (LFP) is increasingly used to measure the combined activity of neurons within a region of tissue. Yet, available estimates of the size of this region are highly disparate, ranging from several hundred microns to a few millimeters. To measure the size of this region directly, we used a combination of multielectrode recordings and optical imaging. We determined the orientation selectivity of stimulus-evoked LFP signals in primary visual cortex and were able to predict it on the basis of the surrounding map of orientation preference. The results show that >95% of the LFP signal originates within 250 μm of the recording electrode. This quantitative estimate indicates that LFPs are more local than often recognized and provides a guide to the interpretation of the increasing number of studies that rest on LFP recordings. [Copyright &y& Elsevier]

Neurons in visual cortex are linked by an extensive network of lateral connections. To study the effect of these connections on neural responses, we recorded spikes and local field potentials (LFPs) from multi-electrode arrays that were implanted in monkey and cat primary visual cortex. Spikes at each location generated outward traveling LFP waves. When the visual stimulus was absent or had low contrast, these LFP waves had large amplitudes and traveled over long distances. Their effect was strong: LFP traces at any site could be predicted by the superposition of waves that were evoked by spiking in a ∼1.5-mm radius. As stimulus contrast increased, both the magnitude and the distance traveled by the waves progressively decreased. We conclude that the relative weight of feedforward and lateral inputs in visual cortex is not fixed, but rather depends on stimulus contrast. Lateral connections dominate at low contrast, when spatial integration of signals is perhaps most beneficial. [ABSTRACT FROM AUTHOR]

Summary: The organization of primary visual cortex (V1) into functional maps makes individual cells operate in a variety of contexts. For instance, some neurons lie in regions of fairly homogeneous orientation preference (iso-orientation domains), while others lie in regions with a variety of preferences (e.g., pinwheel centers). We asked whether this diversity in local map structure correlates with the degree of selectivity of spike responses. We used a combination of imaging and electrophysiology to reveal that neurons in regions of homogeneous orientation preference have much sharper tuning. Moreover, in both monkeys and cats, a common principle links the structure of the orientation map, on the spatial scale of dendritic integration, to the degree of selectivity of individual cells. We conclude that neural computation is not invariant across the cortical surface. This finding must factor into future theories of receptive field wiring and map development. [Copyright &y& Elsevier]

A correction to the article "Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex" in the November 2012 issue is presented which mentions the misstated scale bar length for the figure.

A correction to the article "Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex" in the November 2012 issue is presented which mentions the incorrect computation performed to yield the values in the text and on the axis label.

Summary: We show functional-anatomical organization of motion direction in mouse dorsal lateral geniculate nucleus (dLGN) using two-photon calcium imaging of dense populations in thalamus. Surprisingly, the superficial 75 μm region contains anterior and posterior direction-selective neurons (DSLGNs) intermingled with nondirection-selective neurons, while upward- and downward-selective neurons are nearly absent. Unexpectedly, the remaining neurons encode both anterior and posterior directions, forming horizontal motion-axis selectivity. A model of random wiring consistent with these results makes quantitative predictions about the connectivity of direction-selective retinal ganglion cell (DSRGC) inputs to the superficial dLGN. DSLGNs are more sharply tuned than DSRGCs. These results suggest that dLGN maintains and sharpens retinal direction selectivity and integrates opposing DSRGC subtypes in a functional-anatomical region, perhaps forming a feature representation for horizontal-axis motion, contrary to dLGN being a simple relay. Furthermore, they support recent conjecture that cortical direction and orientation selectivity emerge in part from a previously undescribed motion-selective retinogeniculate pathway. [ABSTRACT FROM AUTHOR]