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Topography and Functional Specialization of Mouse Higher Visual Areas

Abstract

The senses are the interface between an organism and its environment. To interact with the world, animals must detect external stimuli, interpret sensory signals to encode relevant information, and make appropriate decisions based on previous experience and behavioral goals. All of these abilities depend on the organization and activity of neural circuits. To piece together the puzzle of how circuits produce perception and behavior, it is necessary to label, monitor and manipulate specific network components to assess their role in information processing. The recent development of molecular, genetic, and optical techniques enables this type of circuit dissection with unprecedented precision in the mouse model. While the mouse uses sensory information to navigate its environment and make decisions, as in other mammals, relatively little is known about processing beyond primary sensory areas in this species. Anatomical studies have predicted the existence of multiple higher visual areas in the mouse (Wang & Burkhalter 2007), yet their functional and behavioral roles remain unknown. The aim of this dissertation is to begin adding pieces to the puzzle by examining the information represented by higher visual areas, in terms of visual field topography and encoding for basic visual features. First, the representation of the visual field across the cortical surface was mapped using intrinsic signal imaging. As each distinct area contains its own independent map of visual space, analysis of visual field gradients allowed precise identification of 11 distinct higher areas and their boundaries, including two previously undescribed regions in mice. Characterization of visual coverage across areas demonstrated that higher areas often have incomplete or biased representations of visual space, suggesting an emphasis on processing particular types of visual information. Next, areas identified using intrinsic imaging were selectively targeted for higher resolution imaging using two-photon microscopy to measure the sensory evoked response properties across large populations from seven different visual areas. We found that neurons in higher visual areas respond selectively to basic visual features including orientation, direction, spatial frequency and temporal frequency, and that different areas could be distinguished based on encoding for specific combinations of spatiotemporal features. These results demonstrate the unique functional specializations of different mouse higher visual areas, and suggest specific hypothesis about their behavioral roles. Together, this work establishes the basic topographic and functional organization of nearly a dozen distinct visual areas across the mouse cortex, providing a foundation for future studies examining the circuit and cellular mechanisms of information processing in this system. Future work examining more complex functional properties, the circuitry that links areas across the network, and the relationships between specific circuit components and behavior, will be essential to create a more complete picture of sensory processing in the mouse

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