Model Constrained by Visual Hierarchy Improves Prediction of Neural Responses to Natural Scenes.
ABSTRACT: Accurate estimation of neuronal receptive fields is essential for understanding sensory processing in the early visual system. Yet a full characterization of receptive fields is still incomplete, especially with regard to natural visual stimuli and in complete populations of cortical neurons. While previous work has incorporated known structural properties of the early visual system, such as lateral connectivity, or imposing simple-cell-like receptive field structure, no study has exploited the fact that nearby V1 neurons share common feed-forward input from thalamus and other upstream cortical neurons. We introduce a new method for estimating receptive fields simultaneously for a population of V1 neurons, using a model-based analysis incorporating knowledge of the feed-forward visual hierarchy. We assume that a population of V1 neurons shares a common pool of thalamic inputs, and consists of two layers of simple and complex-like V1 neurons. When fit to recordings of a local population of mouse layer 2/3 V1 neurons, our model offers an accurate description of their response to natural images and significant improvement of prediction power over the current state-of-the-art methods. We show that the responses of a large local population of V1 neurons with locally diverse receptive fields can be described with surprisingly limited number of thalamic inputs, consistent with recent experimental findings. Our structural model not only offers an improved functional characterization of V1 neurons, but also provides a framework for studying the relationship between connectivity and function in visual cortical areas.
Project description:Understanding the functions of a brain region requires knowing the neural representations of its myriad inputs, local neurons and outputs. Primary visual cortex (V1) has long been thought to compute visual orientation from untuned thalamic inputs, but very few thalamic inputs have been measured in any mammal. We determined the response properties of ? 28,000 thalamic boutons and ? 4,000 cortical neurons in layers 1-5 of awake mouse V1. Using adaptive optics that allows accurate measurement of bouton activity deep in cortex, we found that around half of the boutons in the main thalamorecipient L4 carried orientation-tuned information and that their orientation and direction biases were also dominant in the L4 neuron population, suggesting that these neurons may inherit their selectivity from tuned thalamic inputs. Cortical neurons in all layers exhibited sharper tuning than thalamic boutons and a greater diversity of preferred orientations. Our results provide data-rich constraints for refining mechanistic models of cortical computation.
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:Inhibition modulates receptive field properties and integrative responses of neurons in cortical circuits. The contribution of specific interneuron classes to cortical circuits and emergent responses is unknown. Here, we examined neuronal responses in primary visual cortex (V1) of adult Dlx1(-/-) mice, which have a selective reduction in cortical dendrite-targeting interneurons (DTIs) that express calretinin, neuropeptide Y, and somatostatin. The V1 neurons examined in Dlx1(-/-) mice have reduced orientation selectivity and altered firing rates, with elevated late responses, suggesting that local inhibition at dendrites has a specific role in modulating neuronal computations. We did not detect overt changes in the physiological properties of thalamic relay neurons and features of thalamocortical projections, such as retinotopic maps and eye-specific inputs, in the mutant mice, suggesting that the defects are cortical in origin. These experimental results are well explained by a computational model that integrates broad tuning from dendrite-targeting and narrower tuning from soma-targeting interneuron subclasses. Our findings suggest a key role for DTIs in the fine-tuning of stimulus-specific cortical responses.
Project description:The mapping of the topographic representation of the visual field onto cortical areas changes throughout the hierarchy of cortical visual areas. The changes are believed to reflect the establishment of modules with different spatial processing emphasis. The receptive fields (RFs) of neurons within these modules, however, may not be governed by the same spatial topographic map parameters. Here it is shown that the RFs of area V4 neurons (centered 1-12 degrees in eccentricity) are based on a circularly symmetric sampling of the primary visual cortical retinotopic map. No eccentricity dependent magnification beyond that observed in V1 is apparent in the V4 neurons. The size and shape of V4 RFs can be explained by a simple, constant sized, two-dimensional Gaussian sample of visual input from the retinotopic map laid out across the surface of V1. Inferences about the spatial scale of interactions within the receptive fields of neurons cannot be based on a visual area's apparent cortical magnification derived from topographic mapping.
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:Sensory processing is an active process involving the interaction of ongoing cortical activity with incoming stimulus information. However, the modulators and circuits involved in this interaction are incompletely understood. One potential candidate is the cannabinoid-signaling system, which is known to modulate the dynamics of cortical networks. Here, we show that in the primate primary and secondary visual cortices, the cannabinoid CP55940 modulates not only population dynamics but also influences the dynamics of the stimulus-response relationship of individual neurons. At the population level, CP55940 decreases EEG power, LFP power, and LFP coherence. At the single-neuron level, intrinsic spike train dynamics appear relatively unchanged, but visual receptive fields are altered: CP55940 induced an overall delay and broadening of the temporal component of V1 and V2 spatiotemporal receptive fields. Our findings provide neurophysiologic evidence for a link between cannabinoid-signaling, network dynamics and the function of a canonical cortical circuit.
Project description:The primary visual cortex (V1) receives its driving input from the eyes via the lateral geniculate nucleus (LGN) of the thalamus. The lateral pulvinar nucleus of the thalamus also projects to V1, but this input is not well understood. We manipulated lateral pulvinar neural activity in prosimian primates and assessed the effect on supra-granular layers of V1 that project to higher visual cortex. Reversibly inactivating lateral pulvinar prevented supra-granular V1 neurons from responding to visual stimulation. Reversible, focal excitation of lateral pulvinar receptive fields increased the visual responses in coincident V1 receptive fields fourfold and shifted partially overlapping V1 receptive fields toward the center of excitation. V1 responses to regions surrounding the excited lateral pulvinar receptive fields were suppressed. LGN responses were unaffected by these lateral pulvinar manipulations. Excitation of lateral pulvinar after LGN lesion activated supra-granular layer V1 neurons. Thus, lateral pulvinar is able to powerfully control and gate information outflow from V1.
Project description:Even within the early sensory areas, the majority of the input to any given cortical neuron comes from other cortical neurons. To extend our knowledge of the contextual information that is transmitted by such lateral and feedback connections, we investigated how visually nonstimulated regions in primary visual cortex (V1) and visual area V2 are influenced by the surrounding context. We used functional magnetic resonance imaging (fMRI) and pattern-classification methods to show that the cortical representation of a nonstimulated quarter-field carries information that can discriminate the surrounding visual context. We show further that the activity patterns in these regions are significantly related to those observed with feed-forward stimulation and that these effects are driven primarily by V1. These results thus demonstrate that visual context strongly influences early visual areas even in the absence of differential feed-forward thalamic stimulation.
Project description:Layer 1 (L1) of primary visual cortex (V1) is the target of projections from many brain regions outside of V1. We found that inputs to the non-columnar mouse V1 from the dorsal lateral geniculate nucleus and feedback projections from multiple higher cortical areas to L1 are patchy. The patches are matched to a pattern of M2 muscarinic acetylcholine receptor expression at fixed locations of mouse, rat, and monkey V1. Neurons in L2/3 aligned with M2-rich patches have high spatial acuity, whereas cells in M2-poor zones exhibited high temporal acuity. Together M2+ and M2- zones form constant-size domains that are repeated across V1. Domains map subregions of the receptive field, such that multiple copies are contained within the point image. The results suggest that the modular network in mouse V1 selects spatiotemporally distinct clusters of neurons within the point image for top-down control and differential routing of inputs to cortical streams.
Project description:Visual stimulation produces oscillatory gamma responses in human primary visual cortex (V1) that also relate to visual perception. We have shown previously that peak gamma frequency positively correlates with central V1 cortical surface area. We hypothesized that people with larger V1 would have smaller receptive fields and that receptive field size, not V1 area, might explain this relationship. Here we set out to test this hypothesis directly by investigating the relationship between fMRI estimated population receptive field (pRF) size and gamma frequency in V1. We stimulated both the near-center and periphery of the visual field using both large and small stimuli in each location and replicated our previous finding of a positive correlation between V1 surface area and peak gamma frequency. Counter to our expectation, we found that between participants V1 size (and not PRF size) accounted for most of the variability in gamma frequency. Within-participants we found that gamma frequency increased, rather than decreased, with stimulus eccentricity directly contradicting our initial hypothesis.