Biology subjects

Livingstone, M. S.

Publications and source records attributed to Livingstone, M. S..

8 recordsLinked to original sources

bioRxiv2026

Parametric neural control differentiates top neural network models of primate visual cortex

Leading deep neural network encoding models predict visual cortical responses with nearly indistinguishable accuracy, raising the strong inference that these models have converged on the same underlying brain-aligned parameterization of natural image space. Here we demonstrate that this is not the case. We introduce axis-aligned feature accentuation, which converts each model's fitted encoding axis into graded stimulus perturbations that are predicted to parametrically control neural firing within and beyond the natural-image range. We generated over 27,500 controller stimuli from ten leading vision models and presented them to five macaques in closed-loop experiments targeting early, mid-, and high-level visual areas. Despite matched natural image predictivity, models diverged strongly in their ability to control neural firing using accentuated stimuli, revealing that most model encoding axes failed to capture the precise tuning of their corresponding neurons. The two adversarially trained models showed a consistent advantage, though adversarial robustness was only weakly predictive of neural control across other models. Instead, control was better predicted by the spatial frequency structure of the input gradient: the distribution of pixels influencing each encoding axis. Overall, these results establish neural control via axis-aligned feature accentuation as a causal method to assess the alignment between how neurons and models parameterize the visual world.

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bioRxiv2025

Response dynamics in macaque ventral stream recapitulate the visual hierarchy

Chronic recording in macaque inferotemporal cortex (IT) revealed a progression of feature selectivity over the duration of the response, with different images evoking strongest responses in different time bins. Neurons responded briskly and transiently to early best images and gave slower and more sustained responses to later best images. Correlations between IT selectivity and deep neural network (DNN) activations in early layers were faster and more transient than correlations with deeper DNN layers, suggesting a hierarchical representation unfolding. Analysis of best images in different time bins showed that early best images were simpler, or made up of fewer parts, than later best images. This simple-to-complex selectivity dynamic is consistent with, but more universal than, previously reported dynamics of global-to-local or category-to-exemplar selectivity. In parallel with the simple-to-complex selectivity progression, the image selectivity and the population activity became sparser during the response, consistent with the hypothesis of a canonical cortical microcircuit that pools inputs and incorporates neighboring-neuron inhibition. We propose that this temporal cascade in IT recapitulates the multiple antecedent stages in the visual hierarchy, which also show a simple-to-complex progression of feature selectivity.

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bioRxiv2025

Metabolic organization of macaque visual cortex reflects retinotopic eccentricity and category selectivity

Neural activity requires energy metabolism, and the brains metabolic architecture varies across regions. Yet, it remains unclear whether these variations are meaningfully related to the functional and perceptual demands of cortical processing. In high-level visual cortex, category-selective regions, such as those preferentially responding to faces and scenes, are consistently distributed along a topographic axis that varies in sensitivity to spatial scale, a feature dimension that imposes differing metabolic demands at the level of the retina. This axis reflects a broader organizing principle of the visual system: retinotopic eccentricity, the topographic mapping of visual space relative to gaze. Here, we tested whether cortical metabolic architecture reflects this principle by aligning in vivo fMRI maps of eccentricity and visual category selectivity with ex vivo cytochrome oxidase (CO) histology, a marker of oxidative metabolism, in macaque visual cortex. We found that face-selective region ML, which is biased toward central vision, exhibits higher CO intensity than the peripherally-biased scene-selective region LPP. More broadly, CO intensity covaries with eccentricity across the entire occipitotemporal cortex, though this gradient only partially accounts for the elevated CO in ML. These findings reveal a close correspondence between cortical energy consumption and retinotopic representation, suggesting that metabolic resources are shaped by the processing demands of visual perception.

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bioRxiv2024

Brain Feature Maps Reveal Progressive Animal-Feature Representations in the Ventral Stream.

What are the fundamental units of representation in the primate visual brain? While objects have become an intuitive framework for studying neurons in many parts of cortex, it is possible that neurons follow a more expressive organizational principle, such as encoding generic features present across textures, places, and objects. In this study, we used multi-electrode arrays to record from neurons in early (V1/V2), middle (V4), and late (posterior inferotemporal cortex (PIT)) areas across the visual hierarchy, estimating the local operation of each neuron over the entire visual scene. These estimates, called "heatmaps," approximate the weight sharing operation of convolutional neural networks. We found that while populations of neurons across V1, V4, and PIT responded over the full scene, they focused on salient sub-regions within object outlines. The best captured object feature class belonged to animals, not general objects, as a trend that increased over the visual hierarchy. These results show that the monkey ventral stream is partially organized to encode local animal features over objects, even as early as primary visual cortex.

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bioRxiv2023

When the whole is only the parts: non-holistic object parts predominate face-cell responses to illusory faces.

Humans are inclined to perceive faces in everyday objects with a face-like configuration. This illusion, known as face pareidolia, is often attributed to a specialized network of face cells in primates. We found that face cells in macaque inferotemporal cortex responded selectively to pareidolia images, but this selectivity did not require a holistic, face-like configuration, nor did it encode human faceness ratings. Instead, it was driven mostly by isolated object parts that are perceived as eyes only within a face-like context. These object parts lack usual characteristics of primate eyes, pointing to the role of lower-level features. Our results suggest that face-cell responses are dominated by local, generic features, unlike primate visual perception, which requires holistic information. These findings caution against interpreting neural activity through the lens of human perception. Doing so could impose human perceptual biases, like seeing faces where none exist, onto our understanding of neural activity.

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bioRxiv2019

Body-map proto-organization in newborn macaques

Topographic sensory maps are a prominent feature of the adult primate brain. Here, we asked whether topographic representations of the environment are fundamental to early development. Using fMRI, we find that the newborn somato-motor system, spanning frontoparietal cortex and subcortex, comprises multiple topographic body representations. The organization of these large-scale body maps was indistinguishable from those in adults and already exhibited features stereotypical of adult maps. Finer-scale differentiation of individual fingers increased over the first two years, suggesting that topographic representations are refined during early development. Last, we found that somato-motor representations were unchanged in two visually impaired monkeys who relied entirely on touch for interacting with their environment, demonstrating that massive shifts in early sensory experience in an otherwise anatomically intact brain are not sufficient for driving cross-modal plasticity. We propose that a topographic scaffolding is present at birth that both directs and constrains experience-driven modifications throughout sensory systems.

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bioRxiv2019

Evolving super stimuli for real neurons using deep generative networks

Finding the best stimulus for a neuron is challenging because it is impossible to test all possible stimuli. Here we used a vast, unbiased, and diverse hypothesis space encoded by a generative deep neural network model to investigate neuronal selectivity in inferotemporal cortex without making any assumptions about natural features or categories. A genetic algorithm, guided by neuronal responses, searched this space for optimal stimuli. Evolved synthetic images evoked higher firing rates than even the best natural images and revealed diagnostic features, independently of category or feature selection. This approach provides a way to investigate neural selectivity in any modality that can be represented by a neural network and challenges our understanding of neural coding in visual cortex.\n\nHighlightsO_LIA generative deep neural network interacted with a genetic algorithm to evolve stimuli that maximized the firing of neurons in alert macaque inferotemporal and primary visual cortex.\nC_LIO_LIThe evolved images activated neurons more strongly than did thousands of natural images.\nC_LIO_LIDistance in image space from the evolved images predicted responses of neurons to novel images.\nC_LI

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bioRxiv2017

Retinotopic Organization of Scene Areas in Macaque Inferior Temporal Cortex

Primates have specialized domains in inferior temporal (IT) cortex that are responsive to particular image categories. Though IT traditionally has been regarded as lacking retinotopy, several recent studies in monkeys have shown that retinotopic maps extend to face patches along the lower bank of the superior temporal sulcus (STS) in IT cortex. Here, we confirm the presence of visual field maps within and around the lower bank of the STS and extend these prior findings to scene-selective cortex in the ventral-most regions of IT. Within the occipito-temporal sulcus (OTS), we identified two retinotopic areas, OTS1 and OTS2. The polar angle representation of OTS2 was a mirror reversal of the OTS1 representation. These regions contained representations of the contralateral periphery and were selectively active for scene vs. face, body, or object images. The extent of this retinotopy parallels that in humans and shows that the organization of the scene network is preserved across primate species. In addition retinotopic maps were identified in dorsal extrastriate, posterior parietal, and frontal cortex as well as the thalamus, including both the LGN and pulvinar. Taken together, it appears that most, if not all, of the macaque visual system contains organized representations of visual space.\n\nSIGNIFICANCE STATEMENTPrimates have specialized domains in inferior temporal (IT) cortex that are responsive to particular image categories. Though retinotopic maps are considered a fundamental organizing principle of posterior visual cortex, IT traditionally has been regarded as lacking retinotopy. Recent imaging studies have demonstrated the presence of several visual field maps within lateral IT. Using neuroimaging, we found multiple representations of visual space within ventral IT cortex of macaques that included scene-selective IT cortex. The scene domains were biased towards the peripheral visual field. These data demonstrate the prevalence of visual field maps throughout the primate visual system, including late stages in the ventral visual hierarchy, and support the idea that domains representing different categories are biased towards different parts of the visual field.

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