Spatial cognition in a virtual reality home-cage extension for freely moving rodents

Abstract

Virtual reality (VR) environments are a powerful tool to investigate brain mechanisms involved in the behavior of animals. With this technique, animals are usually head fixed or secured in a harness, and training for cognitively more complex VR paradigms is time consuming. A VR apparatus allowing free animal movement and the constant operator-independent training of tasks would enable many new applications. Key prospective usages include brain imaging of animal behavior when carrying a miniaturized mobile device such as a fluorescence microscope or an optetrode. Here, we introduce the Servoball, a spherical VR treadmill based on the closed-loop tracking of a freely moving animal and feedback counterrotation of the ball. Furthermore, we present the complete integration of this experimental system with the animals' group home cage, from which single individuals can voluntarily enter through a tunnel with radio-frequency identification (RFID)-automated access control and commence experiments. This automated animal sorter functions as a mechanical replacement of the experimenter. We automatically trained rats using visual or acoustic cues to solve spatial cognitive tasks and recorded spatially modulated entorhinal cells. When electrophysiological extracellular recordings from awake behaving rats were performed, head fixation can dramatically alter results, so that any complex behavior that requires head movement is impossible to achieve. We circumvented this problem with the use of the Servoball in open-field scenarios, as it allows the combination of open-field behavior with the recording of nerve cells, along with all the flexibility that a virtual environment brings. This integrated home cage with a VR arena experimental system permits highly efficient experimentation for complex cognitive experiments. Virtual reality (VR) environments are a powerful tool for the investigation of brain mechanisms. We introduce the Servoball, a VR treadmill for freely moving rodents. The Servoball is integrated with the animals' group home cage. Single individuals voluntarily enter using automated access control. Training is highly time-efficient, even for cognitively complex VR paradigms.

Cholinergic modulation of spatial learning, memory and navigation

“…While this was a constraint when animals had to be trained manually, the emergence of the rodent cognition field operating with high throughput automated assays (Brunton, Botvinick, & Brody, ; Dhawale et al., ; O'Connor et al., ) with psychometric training that allows controlling cognitive demand and testing well defined hypotheses will likely transform our understanding of spatial cognition. One example is the emergence and spread of rodent VR navigation systems in recent years (Aronov & Tank, ; Kaupert et al., ; Leinweber, Ward, Sobczak, Attinger, & Keller, ) allowing complicated navigation tasks. This also provides a segue to another important issue: mechanistic insight often emerges from probing the activity of neurons under different conditions (Sviatkó & Hangya, ), which type of studies have been scarce with respect to cholinergic control of spatial learning, memory and navigation.…”

Habit learning in hierarchical cortex–basal ganglia loops

“…Although this setup is physically impossible as turning to the same side will always lead to the same arm (given the same starting point), it can be implemented by virtual reality technologies for freely moving rats (Thurley & Ayaz, 2017). New technologies, as the apparatus used by Kaupert et al (2017), include a spherical treadmill controlled through a closed loop which allows to adapt the scenario according to the animals' decisions.…”

Visually Guided Behavior and Optogenetically Induced Learning in Head-Fixed Flies Exploring a Virtual Landscape

“…This shortcoming is addressed by the complementary approach of studying behavior in virtual reality (VR) [10]. VR approaches enable the creation of environments with customized rules for how the virtual sensory surroundings change in response to an animal's actions and have found wide application in neuroscience across species [11][12][13][14][15][16][17][18][19]. Here we use VR to study the role of visual landmarks for navigation in Drosophila melanogaster.…”