Mental Disengagement From Navigation Degrades Spatial Codes for the Environment

Post by Lani Cupo

The takeaway

When animals navigate an environment, the hippocampus forms a spatial code based on sensory cues and motion. Mentally disengaging from navigation leads to the degradation of place codes, even when physical motion through the environment is still occurring, suggesting that internal state, not just external information, is critical to forming a spatial code.

What's the science?

Previous research in rodent navigation has established the existence of “place cells” — neurons in the hippocampus that respond to specific positions or directions in the external environment that allow animals to navigate. Specific patterns of activity among these neurons can be viewed as a spatial code, however, it is yet unknown how mental engagement impacts the activation of these spatial codes. This week in Nature Neuroscience, Pettit, Yuan, and colleagues investigated the role of mental engagement in activating spatial codes in mice by examining their behavior and neuronal activity during reward-based navigation tasks in a virtual environment. 

How did they do it?

The authors constructed a virtual environment for male adult mice, with each mouse placed on top of a spherical treadmill. The heads of the mice were restrained to allow for concurrent cellular imaging, however the mice could freely rotate the treadmill. Motion was captured with optical sensors and the information was relayed to a projection on a screen in front of the mouse’s head displaying an environment with visual cues that the mice were trained to recognize. Mice could achieve water rewards in certain “reward zones” of the virtual environment by licking a spout in front of them. Cell imaging was achieved with a method known as two-photon microscopy: lasers are shined on cells, and, because the mouse strains express fluorescent calcium indicators in neurons, light is emitted back upon neuronal activation and can be recorded during waking behavior. This allows the researchers to examine when neurons fire, linking neuronal activation with mouse behavior. In this study, the authors quantified the degree to which mice were engaged or disengaged via lick-based metrics, based on how spatially selective and abundant mouse licks were.

What did they find?

While some sessions included almost only engaged trials, other sessions included larger proportions of disengaged trials, and these usually occurred together at the end of sessions, indicating that mice switched from engaged to disengaged behavior. This could indicate satiety as they received about 1 mL of water. During engaged sessions, neural activity formed specific sequences or place codes. However, the activity of the population of cells differed during disengaged trials. Regardless of whether the trial was engaged or disengaged, the mouse was moving through the environment, indicating that the change in neural activity was not due to placement in the environment, but was instead associated with the mouse’s altered behavior reflecting mental disengagement, even when matching trials on variables such as running speed. Furthermore, when considering the activity of all neurons at a population level, there was no difference between engaged and disengaged trials, suggesting a degradation of the spatial code, not just a general alteration in neural activity. Finally, by examining neuronal activity in streaks of engaged and disengaged trials, the authors found that the shift in activity happened in less than a minute.

What's the impact?

This study found that the hippocampal place codes that are associated with rodent navigation of the environment degrade when mice mentally disengage from a goal-directed task. The authors’ findings suggest that beyond sensory cues and motion information, mental engagement is required to establish hippocampal spatial maps of the surrounding environment. These findings challenge the established idea that spatial maps form automatically in rodent hippocampi and demonstrate that internal state impacts neural encoding of the external environment.