Orientation Tuning Depends on Spatial Frequency in Mouse Visual Cortex.
ABSTRACT: The response properties of neurons to sensory stimuli have been used to identify their receptive fields and to functionally map sensory systems. In primary visual cortex, most neurons are selective to a particular orientation and spatial frequency of the visual stimulus. Using two-photon calcium imaging of neuronal populations from the primary visual cortex of mice, we have characterized the response properties of neurons to various orientations and spatial frequencies. Surprisingly, we found that the orientation selectivity of neurons actually depends on the spatial frequency of the stimulus. This dependence can be easily explained if one assumed spatially asymmetric Gabor-type receptive fields. We propose that receptive fields of neurons in layer 2/3 of visual cortex are indeed spatially asymmetric, and that this asymmetry could be used effectively by the visual system to encode natural scenes.
Project description:Maps representing the preference of neurons for the location and orientation of a stimulus on the visual field are a hallmark of primary visual cortex. It is not yet known how these maps develop and what function they play in visual processing. One hypothesis postulates that orientation maps are initially seeded by the spatial interference of ON- and OFF-center retinal receptive field mosaics. Here we show that such a mechanism predicts a link between the layout of orientation preferences around singularities of different signs and the cardinal axes of the retinotopic map. Moreover, we confirm the predicted relationship holds in tree shrew primary visual cortex. These findings provide additional support for the notion that spatially structured input from the retina may provide a blueprint for the early development of cortical maps and receptive fields. More broadly, it raises the possibility that spatially structured input from the periphery may shape the organization of primary sensory cortex of other modalities as well.
Project description:Circuits in the visual cortex integrate the information derived from separate ON (light-responsive) and OFF (dark-responsive) pathways to construct orderly columnar representations of stimulus orientation and visual space. How this transformation is achieved to meet the specific topographic constraints of each representation remains unclear. Here we report several novel features of ON-OFF convergence visualized by mapping the receptive fields of layer 2/3 neurons in the tree shrew (Tupaia belangeri) visual cortex using two-photon imaging of GCaMP6 calcium signals. We show that the spatially separate ON and OFF subfields of simple cells in layer 2/3 exhibit topologically distinct relationships with the maps of visual space and orientation preference. The centres of OFF subfields for neurons in a given region of cortex are confined to a compact region of visual space and display a smooth visuotopic progression. By contrast, the centres of the ON subfields are distributed over a wider region of visual space, display substantial visuotopic scatter, and have an orientation-specific displacement consistent with orientation preference map structure. As a result, cortical columns exhibit an invariant aggregate receptive field structure: an OFF-dominated central region flanked by ON-dominated subfields. This distinct arrangement of ON and OFF inputs enables continuity in the mapping of both orientation and visual space and the generation of a columnar map of absolute spatial phase.
Project description:Cortical neurons in thalamic recipient layers receive excitation from the thalamus and the cortex. The relative contribution of these two sources of excitation to sensory tuning is poorly understood. We optogenetically silenced the visual cortex of mice to isolate thalamic excitation onto layer 4 neurons during visual stimulation. Thalamic excitation contributed to a third of the total excitation and was organized in spatially offset, yet overlapping, ON and OFF receptive fields. This receptive field structure predicted the orientation tuning of thalamic excitation. Finally, both thalamic and total excitation were similarly tuned to orientation and direction and had the same temporal phase relationship to the visual stimulus. Our results indicate that tuning of thalamic excitation is unlikely to be imparted by direction- or orientation-selective thalamic neurons and that a principal role of cortical circuits is to amplify tuned thalamic excitation.
Project description:Genetic methods available in mice are likely to be powerful tools in dissecting cortical circuits. However, the visual cortex, in which sensory coding has been most thoroughly studied in other species, has essentially been neglected in mice perhaps because of their poor spatial acuity and the lack of columnar organization such as orientation maps. We have now applied quantitative methods to characterize visual receptive fields in mouse primary visual cortex V1 by making extracellular recordings with silicon electrode arrays in anesthetized mice. We used current source density analysis to determine laminar location and spike waveforms to discriminate putative excitatory and inhibitory units. We find that, although the spatial scale of mouse receptive fields is up to one or two orders of magnitude larger, neurons show selectivity for stimulus parameters such as orientation and spatial frequency that is near to that found in other species. Furthermore, typical response properties such as linear versus nonlinear spatial summation (i.e., simple and complex cells) and contrast-invariant tuning are also present in mouse V1 and correlate with laminar position and cell type. Interestingly, we find that putative inhibitory neurons generally have less selective, and nonlinear, responses. This quantitative description of receptive field properties should facilitate the use of mouse visual cortex as a system to address longstanding questions of visual neuroscience and cortical processing.
Project description:The mouse is a promising model in the study of visual system function and development because of available genetic tools. However, a quantitative analysis of visual receptive field properties had not been performed in the mouse superior colliculus (SC) despite its importance in mouse vision and its usefulness in developmental studies. We have made single-unit extracellular recordings from superficial layers of the SC in urethane-anesthetized C57BL/6 mice. We first map receptive fields with flashing spot stimuli and show that most SC neurons have spatially overlapped ON and OFF subfields. With drifting sinusoidal gratings, we then determine the tuning properties of individual SC neurons, including selectivity for stimulus direction and orientation, spatial frequency tuning, temporal frequency tuning, response linearity, and size preference. A wide range of receptive field sizes and selectivity are observed across the population and in various subtypes of SC neurons identified morphologically. In particular, orientation-selective responses are discovered in the mouse SC, and they are not affected by cortical lesion or long-term visual deprivation. However, ON/OFF characteristics and spatial frequency tuning of SC neurons are influenced by cortical inputs and require visual experience during development. Together, our results provide essential information for future investigations on the functional development of the superior colliculus.
Project description:The primary visual cortex of higher mammals is organized into two-dimensional maps, where the preference of cells for stimulus parameters is arranged regularly on the cortical surface. In contrast, the preference of neurons in the rodent appears to be arranged randomly, in what is termed a salt-and-pepper map. Here we revisited the spatial organization of receptive fields in mouse primary visual cortex by measuring the tuning of pyramidal neurons in the joint orientation and spatial frequency domain. We found that the similarity of tuning decreases as a function of cortical distance, revealing a weak but statistically significant spatial clustering. Clustering was also observed across different cortical depths, consistent with a columnar organization. Thus, the mouse visual cortex is not strictly a salt-and-pepper map. At least on a local scale, it resembles a degraded version of the organization seen in higher mammals, hinting at a possible common origin.
Project description:The concept of receptive field is a linear, feed-forward view of visual signal processing. Frequently used models of V1 neurons, like the dynamic Linear filter--static nonlinearity--Poisson [corrected] spike encoder model, predict that receptive fields measured with different stimulus ensembles should be similar. Here, we tested this concept by comparing spatiotemporal maps of V1 neurons derived from two very different, but commonly used, stimulus ensembles: sparse noise and Hartley subspace stimuli. We found maps from the two methods agreed for neurons in input layer 4C but were very different for neurons in superficial layers of V1. Many layer 2/3 cells have receptive fields with multiple elongated subregions when mapped with Hartley stimuli, but their spatial maps collapse to only a single, less-elongated subregion when mapped with sparse noise. Moreover, for upper layer V1 neurons, the preferred orientation for Hartley maps is much closer to the preferred orientation measured with drifting gratings than is the orientation preference of sparse-noise maps. These results challenge the concept of a stimulus-invariant receptive field and imply that intracortical interactions shape fundamental properties of layer 2/3 neurons.
Project description:Here we report the first quantitative analysis of spiking activity in human early visual cortex. We recorded multi-unit activity from two electrodes in area V2/V3 of a human patient implanted with depth electrodes as part of her treatment for epilepsy. We observed well-localized multi-unit receptive fields with tunings for contrast, orientation, spatial frequency, and size, similar to those reported in the macaque. We also observed pronounced gamma oscillations in the local-field potential that could be used to estimate the underlying spiking response properties. Spiking responses were modulated by visual context and attention. We observed orientation-tuned surround suppression: responses were suppressed by image regions with a uniform orientation and enhanced by orientation contrast. Additionally, responses were enhanced on regions that perceptually segregated from the background, indicating that neurons in the human visual cortex are sensitive to figure-ground structure. Spiking responses were also modulated by object-based attention. When the patient mentally traced a curve through the neurons' receptive fields, the accompanying shift of attention enhanced neuronal activity. These results demonstrate that the tuning properties of cells in the human early visual cortex are similar to those in the macaque and that responses can be modulated by both contextual factors and behavioral relevance. Our results, therefore, imply that the macaque visual system is an excellent model for the human visual cortex.
Project description:Directing attention to the spatial location or the distinguishing feature of a visual object modulates neuronal responses in the visual cortex and the stimulus discriminability of subjects. However, the spatial and feature-based modes of attention differently influence visual processing by changing the tuning properties of neurons. Intriguingly, neurons' tuning curves are modulated similarly across different visual areas under both these modes of attention. Here, we explored the mechanism underlying the effects of these two modes of visual attention on the orientation selectivity of visual cortical neurons. To do this, we developed a layered microcircuit model. This model describes multiple orientation-specific microcircuits sharing their receptive fields and consisting of layers 2/3, 4, 5, and 6. These microcircuits represent a functional grouping of cortical neurons and mutually interact via lateral inhibition and excitatory connections between groups with similar selectivity. The individual microcircuits receive bottom-up visual stimuli and top-down attention in different layers. A crucial assumption of the model is that feature-based attention activates orientation-specific microcircuits for the relevant feature selectively, whereas spatial attention activates all microcircuits homogeneously, irrespective of their orientation selectivity. Consequently, our model simultaneously accounts for the multiplicative scaling of neuronal responses in spatial attention and the additive modulations of orientation tuning curves in feature-based attention, which have been observed widely in various visual cortical areas. Simulations of the model predict contrasting differences between excitatory and inhibitory neurons in the two modes of attentional modulations. Furthermore, the model replicates the modulation of the psychophysical discriminability of visual stimuli in the presence of external noise. Our layered model with a biologically suggested laminar structure describes the basic circuit mechanism underlying the attention-mode specific modulations of neuronal responses and visual perception.
Project description:The integration of synaptic inputs onto dendrites provides the basis for neuronal computation. Whereas recent studies have begun to outline the spatial organization of synaptic inputs on individual neurons, the underlying principles related to the specific neural functions are not well understood. Here we perform two-photon dendritic imaging with a genetically-encoded glutamate sensor in awake monkeys, and map the excitatory synaptic inputs on dendrites of individual V1 superficial layer neurons with high spatial and temporal resolution. We find a functional integration and trade-off between orientation-selective and color-selective inputs in basal dendrites of individual V1 neurons. Synaptic inputs on dendrites are spatially clustered by stimulus feature, but functionally scattered in multidimensional feature space, providing a potential substrate of local feature integration on dendritic branches. Furthermore, apical dendrite inputs have larger receptive fields and longer response latencies than basal dendrite inputs, suggesting a dominant role for apical dendrites in integrating feedback in visual information processing.