A Multispecies Perspective on the Evolution of Form Vision

Citation

Lanfranchi, Francesco (Frank) (2025) A Multispecies Perspective on the Evolution of Form Vision. Dissertation (Ph.D.), California Institute of Technology. doi:10.7907/154t-x703. https://resolver.caltech.edu/CaltechTHESIS:01282025-190331921

Abstract

In the mammalian visual system, photons captured by the retina are transformed into meaningful internal percepts of surroundings through a hierarchy of interconnected visual areas. Understanding the representation of visual information at each node of the hierarchy has been a central quest of visual systems neuroscience over the past 50 years. The primate visual system, with its over two dozen distinct areas broadly organized into a dorsal stream for visuo-motor transformations and a ventral stream for object recognition, has served as the gold standard for studying the organization of the visual system. Recent advances in artificial neural networks modeled on the primate visual system for object recognition have prompted the question, is hierarchical representation necessary, and if so, can we observe it across all highly visual mammalian species? Hierarchical organization appears to be a key architectural principle of both artificial and biological networks, enabling stepwise construction of a structured and compact representation from raw sensory input. Here we present a series of efforts to determine the cortical organization and connectivity of the tree shrew visual system and directly compare to that of the primate. This cross-species study sheds light on the evolution and mechanisms of vision in a close relative of primates. Using high-density Neuropixels recordings, we demonstrate that the tree shrew ventral visual pathway exhibits primate-like hierarchical processing, with progressively larger receptive fields, increasing response latencies, and enhanced selectivity for complex stimuli along the visual pathway. Area V2 in the tree shrew performs key functions similar to those of the primate inferotemporal (IT) cortex. Specifically, V2 contains strongly face-selective cells, supports a complete representation of high-level object space, and achieves the most accurate object identity decoding and reconstruction among all tree shrew visual areas. Yet we also found significant differences from the canonical template for hierarchical organization observed in the primate, including maintenance of relatively small, focal receptive fields throughout the hierarchy, and better decoding of latent variables in late deep neural network (DNN) layers by area V2 compared to other areas.

The hierarchical organization of the visual system describes the arrangement of areas but does not reveal how information flows between them. Understanding the type of processing carried out at each node raised the next question of whether information that is transmitted across nodes is differentiated between feedforward and feedback connections. To explore this, we combined electrical microstimulation and extracellular recordings to identify the directionality of projections which is applicable in various species. We used this technique to first study the connections between the first two nodes of the tree shrew cortical hierarchy, V1 and V2. We found that V2 feedback neurons carry a full visual representation on par to other V2 cells. These feedback neurons were distinct with regards to their spatial features, including distinct locations and sizes of their receptive fields. We also found that both feedforward and feedback V2 neurons were modulated by perceptual conflict arising when distinct textures were presented to each eye, suggesting they could refine V1 processing to perceptual inconsistencies.

These studies provide insights into how the tree shrew visual system generates object representations through a hierarchy of interconnected nodes, employing strategies adapted to its cortical constraints. In addition, by combining electrical microstimulation with electrophysiology we set the foundation for cross-species studies to determine the role of feedforward and feedback processing along the visual hierarchy. Together, this work reveals conserved principles of visual processing across species while showcasing unique adaptations in the tree shrew, offering insights into the evolutionary origins and functional organization of the primate visual system.

Thesis Files