Simply put, the goal of my research is to describe the neuronal circuitry of the retina. The organization of the mammalian retina is certainly complex but it is not chaotic. Although there are many cell types, most adhere to a relatively constant morphology and they are distributed in non-random mosaics. Furthermore, each cell type ramifies at a characteristic depth in the retina and makes a stereotyped set of synaptic connections. In other words, these neurons form a series of local circuits across the retina. The next step is to identify the simplest and commonest of these repeating neural circuits. They are the building blocks of retinal function. If we think of it in this way, the retina is a fabulous model for the rest of the CNS. We are interested in identifying specific circuits and cell types that support the different functions of the retina. For example, there appear to be specific pathways for rod and cone mediated vision. Rods are used under low light conditions and rod circuitry is specialized for high sensitivity when photons are scarce (when you’re out camping, starlight). The hallmark of the rod-mediated system is monochromatic vision. In contrast, the cone circuits are specialized for high acuity and color vision under relatively bright or daylight conditions. Individual neurons may be filled with fluorescent dyes under visual control. This is achieved by impaling the cell with a glass microelectrode using a 3D micromanipulator. We are also interested in the diffusion of dye through coupled neuronal networks in the retina. The dye filled cells are also combined with antibody labeling to reveal neuronal connections and circuits. This triple-labeled material may be viewed and reconstructed in 3 dimensions by multi-channel confocal microscopy. We have our own confocal microscope facility in the department and timeslots are available to students in my lab.

Each spring, billions of Bogong moths escape hot conditions in different regions of southeast Australia by migrating over 1000 km to a limited number of cool caves in the Australian Alps, historically used for aestivating over the summer. At the beginning of autumn the same individuals make a return migration to their breeding grounds to reproduce and die. To steer migration Bogong moths sense the Earth’s magnetic field and correlate its directional information with visual cues. In this presentation, we will show that a critically important visual cue is the distribution of starlight within the austral night sky. By tethering spring and autumn migratory moths in a flight simulator, we found that under natural dorsally-projected night skies, and in a nulled magnetic field (disabling the magnetic sense), moths flew in their seasonally appropriate migratory directions, turning in the opposite direction when the night sky was rotated 180°. Visual interneurons in the moth’s optic lobe and central brain responded vigorously to identical sky rotations. Migrating Bogong moths thus use the starry night sky as a true compass to distinguish geographic cardinal directions, the first invertebrate known to do so. These stellar cues are likely reinforced by the Earth’s magnetic field to create a robust compass mechanism for long-distance nocturnal navigation.

All sensory information – like what we see, hear and smell – gets encoded in spike trains by sensory neurons and gets sent to the brain. Due to the complexity of neural circuits and the difficulty of quantifying complex animal behavior, it has been exceedingly hard to resolve how the brain decodes these spike trains to drive behavior. We now measure quantal signals originating from sparse photons through the most sensitive neural circuits of the mammalian retina and correlate the retinal output spike trains with precisely quantified behavioral decisions. We utilize a combination of electrophysiological measurements on the most sensitive ON and OFF retinal ganglion cell types and a novel deep-learning based tracking technology of the head and body positions of freely-moving mice. We show that visually-guided behavior relies on information from the retinal ON pathway for the dimmest light increments and on information from the retinal OFF pathway for the dimmest light decrements (“quantal shadows”). Our results show that the distribution of labor between ON and OFF pathways starts already at starlight supporting distinct pathway-specific visual computations to drive visually-guided behavior. These results have several fundamental consequences for understanding how the brain integrates information across parallel information streams as well as for understanding the limits of sensory signal processing. In my talk, I will discuss some of the most eminent consequences including the extension of this “Quantum Behavior” paradigm from mouse vision to monkey and human visual systems.