By Liang Liang, Mark Andermann and Chinfei Chen

Our perception of the outside world can vary greatly depending on the state of our brain. If we are interested in a picture, even grainy details will not escape our eyes. When we doze off in a boring lecture, we may lose track of what is shown on the whiteboard, yet we can be quickly woken up by a sudden movement in front of us. The ability to flexibly filter visual information has long been thought to largely occur at late stages of processing, at the level of sensory cortex. However, earlier stages of visual processing such as the thalamus receive a variety of projections from the cortex and from neuromodulatory systems which can carry information of the brain states. Any potential modulation of processing at these earlier stages would efficiently streamline relevant information flow to downstream brain areas. We therefore set out to ask whether modulation of visual responses to certain visual stimuli might already take place as visual signals first enter the brain.

We examined the activity of neurons that relay retina information to the thalamus in awake mice. To achieve this goal, we expressed a sensitive calcium indicator in mouse retinal ganglion cells and developed a means of tracking the activity of hundreds of individual retinal axonal terminals in the thalamus, a region historically considered to be a sensory relay between the retina and the cortex. To evoke visual responses and to assess visual tuning properties of these axon terminals, we delivered a battery of visual stimuli including drifting gratings of different spatial frequencies, directions or axes of motion, as well as full-screen changes in luminance. The mouse was head-restrained but could otherwise freely run on a running wheel. During this time, the mouse’s arousal level (measured via the instantaneous pupil area) fluctuated spontaneously on a time scale of seconds to tens of seconds.

A diverse set of retinal ganglion cell types project to the thalamus, and each type carries specific kinds of visual information, such as direction of motion, orientation, brightness changes, or object’s size. Surprisingly, larger pupil diameter was found to be associated with an overall reduction of visual response magnitude in retinal axons, while the axons’ preferences for motion directions or axes remained unchanged. Remarkably, the degree of modulation of retinal axon responses by arousal varied across stimuli and across functionally distinct subsets of axons. At low and intermediate spatial frequencies, the majority of retinal boutons were suppressed by arousal. In contrast, at high spatial frequencies, boutons tuned to regions of visual space ahead of the mouse showed enhancement of responses. Arousal-related modulation also varied with a bouton’s preference for luminance changes and direction or axis of motion. In particular, greater response suppression was observed for boutons tuned to luminance decrements versus increments, and for boutons preferring motion along directions or axes of optic flow.

Together, our results suggest that selective modulation of distinct visual information channels by arousal state occurs at very early stages of visual processing, before the information is transmitted to neurons in visual thalamus. Such early filtering may provide an efficient means of optimizing central visual processing and perception across behavioral contexts.

Liang Liang is Assistant Professor of Neuroscience at Yale University. In January 2020, she launched a new lab on neural computation in visual thalamus.  

Liang completed her postdoctoral training with Mark Andermann, Associate Professor of Medicine at Beth Israel Deaconess Medical Center and Chinfei Chen, Professor of Neurology at Boston Children’s Hospital.

Learn more in the original research articles:
Retinal inputs to the thalamus are selectively gated by arousal. Liang Liang, Alex Fratzl, Jasmine D.S. Reggiani, Omar El Mansour, Chinfei Chen, Mark L. Andermann. Current Biology. 2020 October 19.

A fine-scale functional logic to convergence from retina to thalamus. Liang Liang, Alex Fratzl, Glenn Goldey, Rohan N. Ramesh, Arthur U. Sugden, Josh L. Morgan, Chinfei Chen, Mark L. Andermann. Cell. 2018 May 31.