Activity in brain system that controls eye movements highlights importance of spatial thinking

In the new study, published in Nature Neuroscience, scientists measured the information contained in patterns of brain cell activity across multiple brain regions involved in visual category decisions. The researchers monitored activity in the superior colliculus (SC) and part of the posterior parietal cortex (PPC), a region of the cerebral cortex that is important for visual categorical decisions. To their surprise, they saw that activity in the SC was even more involved than the PPC in guiding the subjects' category decisions, suggesting that it helps coordinate higher-order cognitive processes traditionally thought to take place in the neocortex.

"This is a really surprising place to find these kinds of cognitive signals because this area of the brain is traditionally associated with simpler spatial orienting behaviors and even reflexive functions," said David Freedman, PhD, Professor of Neurobiology and the Neuroscience Institute at UChicago and senior author of the new study. "We have this evolutionarily ancient brain structure that seems to be even more involved in complex cognitive decisions than the cortical areas we studied in our experiments."

An ancient brain region with surprising powers

All animals, from fish and reptiles to mammals like primates and humans, need to quickly distinguish and categorize objects in their field of vision. Is the object moving toward them an obstacle or a threat? Is that thing darting by a predator or prey?

The SC is a region in the brain that is evolutionarily conserved across all vertebrates, even those without a more sophisticated neocortex. It helps orient movements of the head and eyes toward visual stimuli, and it was traditionally believed to kick off reflexive motor actions by relaying inputs from upstream brain regions. However, recent research has shown that it is also involved in complex tasks like selecting an orientation point and paying attention to stimuli at different spatial locations.

Freedman and his team have been studying other cortical areas with strong anatomical connections to the SC for years. These adjacent areas are involved in flexible and cognitively demanding decision-making tasks, and the researchers wanted to see if the SC is involved in more abstract thinking too. For the latest study, they trained monkeys to perform a visual decision-making task in which they viewed images on a computer screen. The animals received fruit juice rewards for pushing a button at the right times to assign images to the correct categories.

While the subjects performed the task, the researchers recorded brain cell activity in the SC and the lateral intraparietal area (LIP), part of the PPC that Freedman's lab previously showed is involved in category decisions during these kinds of tasks. Since the task required the subjects to maintain their gaze in one spot and indicate their choices by a hand movement, the experimental design singled out brain activity needed for categorization -- not the eye or head movements usually thought to be the SC's job.

The researchers saw lots of activity in the SC that encoded the categories of the images the animals were looking at, and this activity took place more strongly than in the PPC. They also performed an experiment in which they injected a drug to temporarily numb the SC during the same task. While this didn't impair most of the subjects' motor and visual functions, it dramatically affected their ability to correctly categorize the images until the effects of the drug wore off.

"Our results show us that this area is really important for the task," Freedman said. "Even in tasks where the animals don't need to move their eyes or direct their attention to different places, the superior colliculus is involved in these more complex cognitive behaviors."

That special "oomph" for problem-solving

Freedman said it's not just surprising to find this activity in the SC; it could mean something about why this brain region is being recruited to solve such complex tasks. Since it is present across all vertebrates, from primitive sharks to modern humans, it was one of the earliest brain regions that evolved to help process visual inputs and generate corresponding movements. But in this new study, it's also involved in decidedly non-spatial functions. Could this be a sign that spatial processing provides a special "oomph" to problem-solving?

Freedman pointed out the kind of eye movements and hand gestures that humans make when we're asked to recall something or make decisions. If someone asks what you had for dinner last night, for example, your eyes often drift upward, as if the answer were written on the ceiling. Or when weighing a decision between two choices, you might move your hands up and down like two sides of a balance scale.

"Some of this data might be telling us is that the reason we're making these kinds of spatial gestures and eye movements is because the spatial parts of the brain are getting recruited into helping us perform these non-spatial cognitive functions," said first author Barbara Peysakhovich, PhD, a former graduate student in Freedman's lab now a postdoctoral researcher at Harvard.

Or, we've all had the experience of struggling to understand something written in text -- like a long press release about a neuroscience study -- but having it instantly click into place when the same information is presented in a graphic.

"They say a picture is worth 1,000 words -- even a very simple spatial diagram can rapidly convey so much more information than you can possibly describe," Freedman said. "It's like the brain has created this beautiful mental graph paper which it can use to solve both spatial and non-spatial problems."

The study, "Primate superior colliculus is causally engaged in abstract higher-order cognition," was supported by funding from National Institutes of Health (grants R01EY019041, U19NS107609, 1F31MH124395, F30EY033648, F31 EY029155) and the Department of Defense Vannevar Bush Faculty Fellowship (N000141912001). Additional authors include Barbara Peysakhovich, Ou Zhu, Stephanie M. Tetrick, Vinay Shirhatti, Alessandra A. Silva, Sihai Li, Matthew C. Rosen, and W. Jeffrey Johnston from UChicago and Guilhem Ibos from UChicago and Institut de Neurosciences de la Timone, Aix-Marseille Université, France.