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The Journal of Neuroscience : the... Apr 2022The mouse primary visual cortex is a model system for understanding the relationship between cortical structure, function, and behavior (Seabrook et al., 2017; Chaplin...
The mouse primary visual cortex is a model system for understanding the relationship between cortical structure, function, and behavior (Seabrook et al., 2017; Chaplin and Margrie, 2020; Hooks and Chen, 2020; Saleem, 2020; Flossmann and Rochefort, 2021). Binocular neurons in V1 are the cellular basis of binocular vision, which is required for predation (Scholl et al., 2013; Hoy et al., 2016; La Chioma et al., 2020; Berson, 2021; Johnson et al., 2021). The normal development of binocular responses, however, has not been systematically measured. Here, we measure tuning properties of neurons to either eye in awake mice of either sex from eye opening to the closure of the critical period. At eye opening, we find an adult-like fraction of neurons responding to the contralateral-eye stimulation, which are selective for orientation and spatial frequency; few neurons respond to ipsilateral eye, and their tuning is immature. Fraction of ipsilateral-eye responses increases rapidly in the first few days after eye opening and more slowly thereafter, reaching adult levels by critical period closure. Tuning of these responses improves with a similar time course. The development and tuning of binocular responses parallel that of ipsilateral-eye responses. Four days after eye opening, monocular neurons respond to a full range of orientations but become more biased to cardinal orientations. Binocular responses, by contrast, lose their cardinal bias with age. Together, these data provide an in-depth accounting of the development of monocular and binocular responses in the binocular region of mouse V1 using a consistent set of visual stimuli and measurements. In this manuscript, we present a full accounting of the emergence and refinement of monocular and binocular receptive field tuning properties of thousands of pyramidal neurons in mouse primary visual cortex. Our data reveal new features of monocular and binocular development that revise current models on the emergence of cortical binocularity. Given the recent interest in visually guided behaviors in mice that require binocular vision (e.g., predation), our measures will provide the basis for studies on the emergence of the neural circuitry guiding these behaviors.
Topics: Animals; Mice; Neurons; Photic Stimulation; Primary Visual Cortex; Vision, Binocular; Visual Cortex
PubMed: 35296547
DOI: 10.1523/JNEUROSCI.1702-21.2022 -
Scientific Reports Jun 2023With the advent of multiplex fluorescence in situ hybridization (FISH) and in situ RNA sequencing technologies, spatial transcriptomics analysis is advancing rapidly,... (Meta-Analysis)
Meta-Analysis
With the advent of multiplex fluorescence in situ hybridization (FISH) and in situ RNA sequencing technologies, spatial transcriptomics analysis is advancing rapidly, providing spatial location and gene expression information about cells in tissue sections at single cell resolution. Cell type classification of these spatially-resolved cells can be inferred by matching the spatial transcriptomics data to reference atlases derived from single cell RNA-sequencing (scRNA-seq) in which cell types are defined by differences in their gene expression profiles. However, robust cell type matching of the spatially-resolved cells to reference scRNA-seq atlases is challenging due to the intrinsic differences in resolution between the spatial and scRNA-seq data. In this study, we systematically evaluated six computational algorithms for cell type matching across four image-based spatial transcriptomics experimental protocols (MERFISH, smFISH, BaristaSeq, and ExSeq) conducted on the same mouse primary visual cortex (VISp) brain region. We find that many cells are assigned as the same type by multiple cell type matching algorithms and are present in spatial patterns previously reported from scRNA-seq studies in VISp. Furthermore, by combining the results of individual matching strategies into consensus cell type assignments, we see even greater alignment with biological expectations. We present two ensemble meta-analysis strategies used in this study and share the consensus cell type matching results in the Cytosplore Viewer ( https://viewer.cytosplore.org ) for interactive visualization and data exploration. The consensus matching can also guide spatial data analysis using SSAM, allowing segmentation-free cell type assignment.
Topics: Animals; Mice; Transcriptome; In Situ Hybridization, Fluorescence; Primary Visual Cortex; Gene Expression Profiling; Algorithms
PubMed: 37311768
DOI: 10.1038/s41598-023-36638-8 -
The Journal of Neuroscience : the... Apr 2023In everyday life, we integrate visual and auditory information in routine tasks such as navigation and communication. While concurrent sound can improve visual...
In everyday life, we integrate visual and auditory information in routine tasks such as navigation and communication. While concurrent sound can improve visual perception, the neuronal correlates of audiovisual integration are not fully understood. Specifically, it remains unclear whether neuronal firing patters in the primary visual cortex (V1) of awake animals demonstrate similar sound-induced improvement in visual discriminability. Furthermore, presentation of sound is associated with movement in the subjects, but little is understood about whether and how sound-associated movement affects audiovisual integration in V1. Here, we investigated how sound and movement interact to modulate V1 visual responses in awake, head-fixed mice and whether this interaction improves neuronal encoding of the visual stimulus. We presented visual drifting gratings with and without simultaneous auditory white noise to awake mice while recording mouse movement and V1 neuronal activity. Sound modulated activity of 80% of light-responsive neurons, with 95% of neurons increasing activity when the auditory stimulus was present. A generalized linear model (GLM) revealed that sound and movement had distinct and complementary effects of the neuronal visual responses. Furthermore, decoding of the visual stimulus from the neuronal activity was improved with sound, an effect that persisted even when controlling for movement. These results demonstrate that sound and movement modulate visual responses in complementary ways, improving neuronal representation of the visual stimulus. This study clarifies the role of movement as a potential confound in neuronal audiovisual responses and expands our knowledge of how multimodal processing is mediated at a neuronal level in the awake brain. Sound and movement are both known to modulate visual responses in the primary visual cortex; however, sound-induced movement has largely remained unaccounted for as a potential confound in audiovisual studies in awake animals. Here, authors found that sound and movement both modulate visual responses in an important visual brain area, the primary visual cortex, in distinct, yet complementary ways. Furthermore, sound improved encoding of the visual stimulus even when accounting for movement. This study reconciles contrasting theories on the mechanism underlying audiovisual integration and asserts the primary visual cortex as a key brain region participating in tripartite sensory interactions.
Topics: Mice; Animals; Primary Visual Cortex; Visual Perception; Sound; Movement; Neurons; Auditory Cortex; Photic Stimulation
PubMed: 36944489
DOI: 10.1523/JNEUROSCI.2444-21.2023 -
The Journal of Neuroscience : the... Jul 2016Visual attention, which improves perception of attended locations or objects, has long been known to affect many aspects of the responses of neuronal populations in...
UNLABELLED
Visual attention, which improves perception of attended locations or objects, has long been known to affect many aspects of the responses of neuronal populations in visual cortex. There are two nonmutually exclusive hypotheses concerning the neuronal mechanisms that underlie these perceptual improvements. The first hypothesis, that attention improves the information encoded by a population of neurons in a particular cortical area, has considerable physiological support. The second hypothesis is that attention improves perception by selectively communicating relevant visual information. This idea has been tested primarily by measuring interactions between neurons on very short timescales, which are mathematically nearly independent of neuronal interactions on longer timescales. We tested the hypothesis that attention changes the way visual information is communicated between cortical areas on longer timescales by recording simultaneously from neurons in primary visual cortex (V1) and the middle temporal area (MT) in rhesus monkeys. We used two independent and complementary approaches. Our correlative experiment showed that attention increases the trial-to-trial response variability that is shared between the two areas. In our causal experiment, we electrically microstimulated V1 and found that attention increased the effect of stimulation on MT responses. Together, our results suggest that attention affects both the way visual stimuli are encoded within a cortical area and the extent to which visual information is communicated between areas on behaviorally relevant timescales.
SIGNIFICANCE STATEMENT
Visual attention dramatically improves the perception of attended stimuli. Attention has long been thought to act by selecting relevant visual information for further processing. It has been hypothesized that this selection is accomplished by increasing communication between neurons that encode attended information in different cortical areas. We recorded simultaneously from neurons in primary visual cortex and the middle temporal area while rhesus monkeys performed an attention task. We found that attention increased shared variability between neurons in the two areas and that attention increased the effect of microstimulation in V1 on the firing rates of MT neurons. Our results provide support for the hypothesis that attention increases communication between neurons in different brain areas on behaviorally relevant timescales.
Topics: Action Potentials; Animals; Attention; Electric Stimulation; Macaca mulatta; Male; Motion Perception; Nerve Net; Photic Stimulation; Reaction Time; Statistics as Topic; Temporal Lobe; Visual Cortex; Visual Pathways; Visual Perception
PubMed: 27413161
DOI: 10.1523/JNEUROSCI.0610-16.2016 -
The Journal of Physiology Jul 2005Parallel processing streams in the primate visual system originate from more than a dozen anatomically and functionally distinct types of retinal ganglion cells (RGCs).... (Review)
Review
Parallel processing streams in the primate visual system originate from more than a dozen anatomically and functionally distinct types of retinal ganglion cells (RGCs). A central problem in determining how visual information is processed is understanding how each of these RGC types connects to more central structures, including the lateral geniculate nucleus (LGN) of the thalamus and (via the LGN) the primary visual cortex. Nevertheless, the available functional and anatomical evidence linking together specific cell types across these structures is surprisingly indirect. This review evaluates the available evidence and assesses the strength of the many inferences that can be made from these observations. There is strong evidence that parasol RGCs are the provenance of the magnocellular (M) visual pathway and that midget RGCs give rise to the parvocellular (P) pathway. Furthermore, the M and P pathways remain segregated up to the input layer of primary visual cortex. The relationships between the numerous other RGC types and cell types in the LGN remain less certain. and there remains ambiguity about how best to define additional pathways, such as the koniocellular (K) pathway, which probably arise from these other, less common, RGC types.
Topics: Action Potentials; Animals; Models, Neurological; Nerve Net; Primates; Retinal Ganglion Cells; Visual Cortex; Visual Pathways; Visual Perception
PubMed: 15905213
DOI: 10.1113/jphysiol.2005.088047 -
The Neuroscientist : a Review Journal... Oct 2016Damage to the primary visual cortex removes the major input from the eyes to the brain, causing significant visual loss as patients are unable to perceive the side of... (Review)
Review
Damage to the primary visual cortex removes the major input from the eyes to the brain, causing significant visual loss as patients are unable to perceive the side of the world contralateral to the damage. Some patients, however, retain the ability to detect visual information within this blind region; this is known as blindsight. By studying the visual pathways that underlie this residual vision in patients, we can uncover additional aspects of the human visual system that likely contribute to normal visual function but cannot be revealed under physiological conditions. In this review, we discuss the residual abilities and neural activity that have been described in blindsight and the implications of these findings for understanding the intact system.
Topics: Awareness; Humans; Vision, Ocular; Visual Pathways
PubMed: 27777337
DOI: 10.1177/1073858416673817 -
Brain Structure & Function May 2022Cetartiodactyls include terrestrial and marine species, all generally endowed with a comparatively lateral position of their eyes and a relatively limited binocular...
Cetartiodactyls include terrestrial and marine species, all generally endowed with a comparatively lateral position of their eyes and a relatively limited binocular field of vision. To this day, our understanding of the visual system in mammals beyond the few studied animal models remains limited. In the present study, we examined the primary visual cortex of Cetartiodactyls that live on land (sheep, Père David deer, giraffe); in the sea (bottlenose dolphin, Risso's dolphin, long-finned pilot whale, Cuvier's beaked whale, sperm whale and fin whale); or in an amphibious environment (hippopotamus). We also sampled and studied the visual cortex of the horse (a closely related perissodactyl) and two primates (chimpanzee and pig-tailed macaque) for comparison. Our histochemical and immunohistochemical results indicate that the visual cortex of Cetartiodactyls is characterized by a peculiar organization, structure, and complexity of the cortical column. We noted a general lesser lamination compared to simians, with diminished density, and an apparent simplification of the intra- and extra-columnar connections. The presence and distribution of calcium-binding proteins indicated a notable absence of parvalbumin in water species and a strong reduction of layer 4, usually enlarged in the striated cortex, seemingly replaced by a more diffuse distribution in neighboring layers. Consequently, thalamo-cortical inputs are apparently directed to the higher layers of the column. Computer analyses and statistical evaluation of the data confirmed the results and indicated a substantial correlation between eye placement and cortical structure, with a markedly segregated pattern in cetaceans compared to other mammals. Furthermore, cetacean species showed several types of cortical lamination which may reflect differences in function, possibly related to depth of foraging and consequent progressive disappearance of light, and increased importance of echolocation.
Topics: Animals; Bottle-Nosed Dolphin; Cetacea; Deer; Horses; Primary Visual Cortex; Primates; Sheep
PubMed: 34604923
DOI: 10.1007/s00429-021-02392-8 -
Nature Communications Nov 2021Sensory data about most natural task-relevant variables are entangled with task-irrelevant nuisance variables. The neurons that encode these relevant signals typically...
Sensory data about most natural task-relevant variables are entangled with task-irrelevant nuisance variables. The neurons that encode these relevant signals typically constitute a nonlinear population code. Here we present a theoretical framework for quantifying how the brain uses or decodes its nonlinear information. Our theory obeys fundamental mathematical limitations on information content inherited from the sensory periphery, describing redundant codes when there are many more cortical neurons than primary sensory neurons. The theory predicts that if the brain uses its nonlinear population codes optimally, then more informative patterns should be more correlated with choices. More specifically, the theory predicts a simple, easily computed quantitative relationship between fluctuating neural activity and behavioral choices that reveals the decoding efficiency. This relationship holds for optimal feedforward networks of modest complexity, when experiments are performed under natural nuisance variation. We analyze recordings from primary visual cortex of monkeys discriminating the distribution from which oriented stimuli were drawn, and find these data are consistent with the hypothesis of near-optimal nonlinear decoding.
Topics: Algorithms; Animals; Brain; Models, Neurological; Models, Theoretical; Neurons; Primary Visual Cortex
PubMed: 34785652
DOI: 10.1038/s41467-021-26793-9 -
Cell Reports Sep 2021Detailing how primate and mouse neurons differ is critical for creating generalized models of how neurons process information. We reconstruct 15,748 synapses in adult...
Detailing how primate and mouse neurons differ is critical for creating generalized models of how neurons process information. We reconstruct 15,748 synapses in adult Rhesus macaques and mice and ask how connectivity differs on identified cell types in layer 2/3 of primary visual cortex. Primate excitatory and inhibitory neurons receive 2-5 times fewer excitatory and inhibitory synapses than similar mouse neurons. Primate excitatory neurons have lower excitatory-to-inhibitory (E/I) ratios than mouse but similar E/I ratios in inhibitory neurons. In both species, properties of inhibitory axons such as synapse size and frequency are unchanged, and inhibitory innervation of excitatory neurons is local and specific. Using artificial recurrent neural networks (RNNs) optimized for different cognitive tasks, we find that penalizing networks for creating and maintaining synapses, as opposed to neuronal firing, reduces the number of connections per node as the number of nodes increases, similar to primate neurons compared with mice.
Topics: Animals; Macaca mulatta; Male; Mice; Microscopy, Electron; Neural Networks, Computer; Neurons; Primary Visual Cortex; Synapses
PubMed: 34525373
DOI: 10.1016/j.celrep.2021.109709 -
PloS One 2023Primary visual cortex (V1) is generally thought of as a low-level sensory area that primarily processes basic visual features. Although there is evidence for...
Primary visual cortex (V1) is generally thought of as a low-level sensory area that primarily processes basic visual features. Although there is evidence for multisensory effects on its activity, these are typically found for the processing of simple sounds and their properties, for example spatially or temporally-congruent simple sounds. However, in congenitally blind individuals, V1 is involved in language processing, with no evidence of major changes in anatomical connectivity that could explain this seemingly drastic functional change. This is at odds with current accounts of neural plasticity, which emphasize the role of connectivity and conserved function in determining a neural tissue's role even after atypical early experiences. To reconcile what appears to be unprecedented functional reorganization with known accounts of plasticity limitations, we tested whether V1's multisensory roles include responses to spoken language in sighted individuals. Using fMRI, we found that V1 in normally sighted individuals was indeed activated by comprehensible spoken sentences as compared to an incomprehensible reversed speech control condition, and more strongly so in the left compared to the right hemisphere. Activation in V1 for language was also significant and comparable for abstract and concrete words, suggesting it was not driven by visual imagery. Last, this activation did not stem from increased attention to the auditory onset of words, nor was it correlated with attentional arousal ratings, making general attention accounts an unlikely explanation. Together these findings suggest that V1 responds to spoken language even in sighted individuals, reflecting the binding of multisensory high-level signals, potentially to predict visual input. This capability might be the basis for the strong V1 language activation observed in people born blind, re-affirming the notion that plasticity is guided by pre-existing connectivity and abilities in the typically developed brain.
Topics: Humans; Primary Visual Cortex; Language; Brain; Brain Mapping; Magnetic Resonance Imaging; Blindness
PubMed: 37566582
DOI: 10.1371/journal.pone.0289671