At any given instant, multiple potential targets for saccades are present in the visual world, implying that a "selection process" within the brain determines the target of the next eye movement. Some superior colliculus (SC) neurons begin discharging seconds before saccade initiation, suggesting involvement in target selection or, alternatively, in postselectional saccade preparation. SC neurons were recorded in monkeys who selected saccade targets on the basis of motion direction in a visual display. Some neurons carried a direction-selective visual signal, consistent with a role in target selection in this task, whereas other SC neurons appeared to be more involved in postselection specification of saccade parameters.
Color has become a premier model system for understanding how information is processed by neural circuits, and for investigating the relationships among genes, neural circuits, and perception. Both the physical stimulus for color and the perceptual output experienced as color are quite well characterized, but the neural mechanisms that underlie the transformation from stimulus to perception are incompletely understood. The past several years have seen important scientific and technical advances that are changing our understanding of these mechanisms. Here, and in the accompanying minisymposium, we review the latest findings and hypotheses regarding color computations in the retina, primary visual cortex, and higher-order visual areas, focusing on non-human primates, a model of human color vision.In trichromatic primates, including humans and Old World monkeys, there are three types of cone photoreceptors that are responsible for color vision ( Fig. 1 A, B). The cone classes are called L, M, and S because of their spectral-sensitivity peaks, which lie in the long-, middle-, and short-wavelength regions of the visible spectrum. These labels replace the misleading terms "red," "green," and "blue." Two physically distinct stimuli appear as different colors only if they produce different relative activations in at least two cone types; conversely, any pair of physically distinct stimuli that activate the cone types in the same relative amount appear the same, like the two yellows shown in Figure 1C. While photoreceptor responses are easily computed from the spectral distribution of the stimulus, there is no straightforward relationship between photoreceptor response and color (Hofer et al., 2005a;Shevell and Kingdom, 2008). The multitude of color phenomena, including color afterimages, color assimilation, neon-color spreading, color constancy, and colored shadows, is compelling because in many cases two physically identical stimuli are made to appear different colors, or two physically different stimuli are made to appear the same simply by changing the spatial or temporal context (Fig. 2). A full description of the neural machinery for color should account for these observations, as well as more cognitive phenomena involving the relationship between experience, language, memory, emotion and color. The neural basis of color has been reviewed previously from a range of perspectives (Gegenfurtner, 2003;Gegenfurtner and Kiper, 2003;Lennie and Movshon, 2005;Sincich and Horton, 2005;Solomon and Lennie, 2007;Conway, 2009;Dobkins, 2009;Jacobs and Nathans, 2009;Stockman and Brainard, 2010). Here we focus on advances and pressing questions regarding the mechanisms of color in retina, striate cortex, and extrastriate cortex of non-human primates, although we note that other species are emerging as excellent model systems of color processing (Lotto and Chittka, 2005;Van Hooser and Nelson, 2006;Osorio and Vorobyev, 2008;Borst, 2009;Johnson et al., 2010;Srinivasan, 2010). Retinal mechanismsA single cone by itself is color blind b...
Optogenetics has advanced our understanding of the neural basis of simple behaviors in rodents and small animals. In primates, however, for which more sophisticated behavioral assays exist, optogenetic manipulations of behavior have been unsuccessful. Here, we report that monkeys reliably shift their gaze toward the receptive field of optically driven channelrhodopsin–2–expressing V1 neurons. This result establishes optogenetics as a viable tool for the causal analysis of behavior in primate brain.
Genetic strategies for perturbing activity of selected neurons hold great promise for understanding circuitry and behavior. Several such strategies exist, but there has been no direct demonstration of reversible inactivation of mammalian neurons in vivo. We previously reported quickly reversible inactivation of neurons in vitro using expression of the Drosophila allatostatin receptor (AlstR). Here, adeno-associated viral vectors are used to express AlstR in vivo in cortical and thalamic neurons of rats, ferrets, and monkeys. Application of the receptor's ligand, allatostatin (AL), leads to a dramatic reduction in neural activity, including responses of visual neurons to optimized visual stimuli. Additionally, AL eliminates activity in spinal cords of transgenic mice conditionally expressing AlstR. This reduction occurs selectively in AlstR-expressing neurons. Inactivation can be reversed within minutes upon washout of the ligand and is repeatable, demonstrating that the AlstR/AL system is effective for selective, quick, and reversible silencing of mammalian neurons in vivo.
Understanding color vision requires knowing how signals from the three classes of cone photoreceptor are combined in the cortex. We recorded from single V1 neurons in awake monkeys while an automated, closed-loop system identified stimuli that differed in cone contrast but evoked the same response. We found that isoresponse surfaces for about half the neurons were planar, consistent with linear processing. The remaining isoresponse surfaces were nonplanar. Some were cup-shaped, indicating sensitivity to a narrow region of color space. Others were ellipsoidal, indicating sensitivity to all color directions. The major and minor axes of these nonlinear surfaces were often aligned to a set of three color directions that were previously identified in perceptual experiments. These results demonstrate that many V1 neurons combine cone signals nonlinearly and provide a new framework within which to decipher color processing in V1.
23The primary motor cortex (M1) is essential for voluntary fine motor control and is functionally conserved 24 across mammals. Using high-throughput transcriptomic and epigenomic profiling of over 450,000 single 25 nuclei in human, marmoset monkey, and mouse, we demonstrate a broadly conserved cellular makeup 26 of this region, whose similarity mirrors evolutionary distance and is consistent between the 27 transcriptome and epigenome. The core conserved molecular identity of neuronal and non-neuronal 28 types allowed the generation of a cross-species consensus cell type classification and inference of 29 conserved cell type properties across species. Despite overall conservation, many species 30 specializations were apparent, including differences in cell type proportions, gene expression, DNA 31 methylation, and chromatin state. Few cell type marker genes were conserved across species, 32 providing a short list of candidate genes and regulatory mechanisms responsible for conserved features 33 of homologous cell types, such as the GABAergic chandelier cells. This consensus transcriptomic 34 classification allowed the Patch-seq identification of layer 5 (L5) corticospinal Betz cells in non-human 35 primate and human and characterization of their highly specialized physiology and anatomy. These 36 findings highlight the robust molecular underpinnings of cell type diversity in M1 across mammals and 37 point to the genes and regulatory pathways responsible for the functional identity of cell types and their 38 species-specific adaptations. 39 40 distinguished on the basis of regions of open chromatin or DNA methylation 5,9,10 . Furthermore, several 48 recent studies have shown that transcriptomically-defined cell types can be aligned across species 2,11-49 13 , indicating that these methods provide a path to quantitatively study evolutionary conservation and 50 divergence at the level of cell types. However, application of these methods has been highly 51 fragmented to date. Human and mouse comparisons have been performed in different cortical regions, 52 using single-cell (with biases in cell proportions) versus single-nucleus (with biases in transcript 53 makeup) analysis, and most single-cell transcriptomic and epigenomic studies have been performed 54 independently. 55 56The primary motor cortex (MOp in mouse, M1 in human and non-human primates, all referred to as M1 57 herein) provides an ideal cortical region to address questions about cellular evolution in rodents and 58 primates by integrating these approaches. Unlike the primary visual cortex (V1), which is highly 59 specialized in primates, or frontal and temporal association areas, whose homologues in rodents 60 remain poorly defined, M1 is essential for fine motor control and is functionally conserved across 61 placental mammals. M1 is an agranular cortex, lacking a defined L4, although neurons with L4-like 62properties have been described 14 . L5 of carnivore and primate M1 contains exceptionally large 63 "giganto-cellular" corticospinal neurons (Betz c...
. We recorded from neurons in the intermediate and deep layers of the superior colliculus (SC) while monkeys performed a novel direction discrimination task. In contrast to the task we used previously, the new version required the monkey to dissociate perceptual judgments from preparation to execute specific operant saccades. The monkey discriminated between 2 opposed directions of motion in a random-dot motion stimulus and was required to maintain the decision in memory throughout a delay period before the target of the required operant saccade was revealed. We hypothesized that perceptual decisions made in this paradigm would be represented in an "abstract" or "categorical" form within the brain, probably in the frontal cortex, and that decision-related neural activity would be eliminated from spatially organized preoculomotor structures such as the SC. To our surprise, however, a small population of neurons in the intermediate and deep layers of the SC fired in a choice-specific manner early in the trial well before the monkey could plan the operant saccade. Furthermore, the representation of the decision during the delay period appeared to be spatial: the active region in the SC map corresponded to the region of space toward which the perceptually discriminated stimulus motion flowed. Electrical microstimulation experiments suggested that these decisionrelated SC signals were not merely related to covert saccade planning. We conclude that monkeys may employ, in part, a spatially referenced mnemonic strategy for representing perceptual decisions, even when an abstract, categorical representation might appear more likely a priori.
Rules by which V1 neurons combine signals originating in the cone photoreceptors are poorly understood. We measured cone inputs to V1 neurons in awake, fixating monkeys with white-noise analysis techniques that reveal properties of light responses not revealed by purely linear models used in previous studies. Simple cells were studied by spike-triggered averaging that is robust to static nonlinearities in spike generation. This analysis revealed, among heterogeneously tuned neurons, two relatively discrete categories: one with opponent L- and M-cone weights and another with nonopponent cone weights. Complex cells were studied by spike-triggered covariance, which identifies features in the stimulus sequence that trigger spikes in neurons with receptive fields containing multiple linear subunits that combine nonlinearly. All complex cells responded to nonopponent stimulus modulations. Although some complex cells responded to cone-opponent stimulus modulations too, none exhibited the pure opponent sensitivity observed in many simple cells. These results extend the findings on distinctions between simple and complex cell chromatic tuning observed in previous studies in anesthetized monkeys.
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