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Restivo, K.

Publications and source records attributed to Restivo, K..

4 recordsLinked to original sources

Dual-feature selectivity enables bidirectional coding in visual cortical neurons

Sensory neurons are traditionally viewed as feature detectors that respond with an increase in firing rate to preferred stimuli while remaining unresponsive to others. Here, we identify a dual-feature encoding strategy in macaque visual cortex, wherein many neurons in areas V1 and V4 are selectively tuned to two distinct visual features--one that enhances and one that suppresses activity--around an elevated baseline firing rate. By combining neuronal recordings with functional digital twin models--deep learning-based predictive models of biological neurons--we were able to systematically identify each neurons preferred and non-preferred features. These feature pairs served as anchors for a continuous, low-dimensional axis in natural image similarity space, along which neuronal activity varied approximately linearly. Within a single visual area, visual features that strongly or weakly activated individual neurons also had a high probability of modulating the activity of other neurons, suggesting a shared feature selectivity across the population that structures stimulus encoding. We show that this encoding strategy is conserved across species, present in both primary and lateral visual areas of mouse cortex. Dual-feature selectivity is consistent with recent anatomical evidence for feature-specific inhibitory connectivity, complementing the feature-detector principle through circuit mechanisms in which selective excitation and inhibition may together enhance the representational capacity of the neuronal population.

neuroscience↗

Energy Guided Diffusion for Generating Neurally Exciting Images

In recent years, most exciting inputs (MEIs) synthesized from encoding models of neuronal activity have become an established method to study tuning properties of biological and artificial visual systems. However, as we move up the visual hierarchy, the complexity of neuronal computations increases. Consequently, it becomes more challenging to model neuronal activity, requiring more complex models. In this study, we introduce a new attention readout for a convolutional data-driven core for neurons in macaque V4 that outperforms the state-of-the-art task-driven ResNet model in predicting neuronal responses. However, as the predictive network becomes deeper and more complex, synthesizing MEIs via straightforward gradient ascent (GA) can struggle to produce qualitatively good results and overfit to idiosyncrasies of a more complex model, potentially decreasing the MEIs model-to-brain transferability. To solve this problem, we propose a diffusion-based method for generating MEIs via Energy Guidance (EGG). We show that for models of macaque V4, EGG generates single neuron MEIs that generalize better across architectures than the state-of-the-art GA while preserving the within-architectures activation and requiring 4.7x less compute time. Furthermore, EGG diffusion can be used to generate other neurally exciting images, like most exciting natural images that are on par with a selection of highly activating natural images, or image reconstructions that generalize better across architectures. Finally, EGG is simple to implement, requires no retraining of the diffusion model, and can easily be generalized to provide other characterizations of the visual system, such as invariances. Thus EGG provides a general and flexible framework to study coding properties of the visual system in the context of natural images.1

neuroscience↗

Deep learning-driven characterization of single cell tuning in primate visual area V4 unveils topological organization

Deciphering the brains structure-function relationship is key to understanding the neuronal mechanisms underlying perception and cognition. The cortical column, a vertical organization of neurons with similar functions, is a classic example of primate neocortex structure-function organization. While columns have been identified in primary sensory areas using parametric stimuli, their prevalence across higher-level cortex is debated, particularly regarding complex tuning in natural image space. However, a key hurdle in identifying columns is characterizing the complex, nonlinear tuning of neurons to high-dimensional sensory inputs. Building on prior findings of topological organization for features like color and orientation, we investigate functional clustering in macaque visual area V4 in non-parametric natural image space, using large-scale recordings and deep learning-based analysis. We combined linear probe recordings with deep learning methods to systematically characterize the tuning of >1,200 V4 neurons using in silico synthesis of most exciting images (MEIs), followed by in vivo verification. Single V4 neurons exhibited MEIs containing complex features, including textures and shapes, and even high-level attributes with eye-like appearance. Neurons recorded on the same silicon probe, inserted orthogonal to the cortical surface, often exhibited similarities in their spatial feature selectivity, suggesting a degree of functional organization along the cortical depth. We quantified MEI similarity using human psychophysics and distances in a contrastive learning-derived embedding space. Moreover, the selectivity of the V4 neuronal population showed evidence of clustering into functional groups of shared feature selectivity. These functional groups showed parallels with the feature maps of units in artificial vision systems, suggesting potential shared encoding strategies. These results demonstrate the feasibility and scalability of deep learning-based functional characterization of neuronal selectivity in naturalistic visual contexts, offering a framework for quantitatively mapping cortical organization across multiple levels of the visual hierarchy.

neuroscience↗

Diverse task-driven modeling of macaque V4 reveals functional specialization towards semantic tasks

Responses to natural stimuli in area V4 - a mid-level area of the visual ventral stream - are well predicted by features from convolutional neural networks (CNNs) trained on image classification. This result has been taken as evidence for the functional role of V4 in object classification. However, we currently do not know if and to what extent V4 plays a role in solving other computational objectives. Here, we investigated normative accounts of V4 (and V1 for comparison) by predicting macaque single-neuron responses to natural images from the representations extracted by 23 CNNs trained on different computer vision tasks including semantic, geometric, 2D, and 3D types of tasks. We found that V4 was best predicted by semantic classification features and exhibited high task selectivity, while the choice of task was less consequential to V1 performance. Consistent with traditional characterizations of V4 function that show its high-dimensional tuning to various 2D and 3D stimulus directions, we found that diverse non-semantic tasks explained aspects of V4 function beyond those captured by individual semantic tasks. Nevertheless, jointly considering the features of a pair of semantic classification tasks was sufficient to yield one of our top V4 models, solidifying V4s main functional role in semantic processing and suggesting that V4s affinity to 2D or 3D stimulus properties found by electrophysiologists can result from semantic functional goals.

neuroscience↗