Abstract
The process by which visual information is incorporated into the brain's spatial framework to represent landmarks is poorly understood. Studies in humans and rodents suggest that retrosplenial cortex (RSC) plays a key role in these computations. We developed an RSC-dependent behavioral task in which head-fixed mice learned the spatial relationship between visual landmark cues and hidden reward locations. Two-photon imaging revealed that these cues served as dominant reference points for most task-active neurons and anchored the spatial code in RSC. This encoding was more robust after task acquisition. Decoupling the virtual environment from mouse behavior degraded spatial representations and provided evidence that supralinear integration of visual and motor inputs contributes to landmark encoding. V1 axons recorded in RSC were less modulated by task engagement but showed surprisingly similar spatial tuning. Our data indicate that landmark representations in RSC are the result of local integration of visual, motor, and spatial information.
Highlights
Spatial navigation requires the constant integration of sensory information, motor feedback, and prior knowledge of the environment (Hardcastle et al, 2015; McNaughton et al, 2006; Taube, 2007; Valerio and Taube, 2012)
We developed a behavioral task that required mice to learn the spatial relationships between visual cues and hidden rewards along a virtual linear corridor (Figure 1A and B)
Trial onset neurons and reward neurons did not show trial type selectivity (Figure 3—figure supplement 1E). These results indicate that neurons in retrosplenial cortex (RSC) encode a mix of task variables with a strong preference for visual cues informing the animal about goal locations
Summary
Spatial navigation requires the constant integration of sensory information, motor feedback, and prior knowledge of the environment (Hardcastle et al, 2015; McNaughton et al, 2006; Taube, 2007; Valerio and Taube, 2012). Even in situations where the immediate surroundings may not be informative, distal landmarks can provide critical orientation cues to find goal locations (Morris, 1981; Tolman, 1948) Their importance is further underlined by the fact that salient visuo-spatial cues anchor almost every type of spatially-tuned cells observed in the mammalian brain to date, including head-direction cells (Jacob et al, 2017; Taube et al, 1990; Yoder et al, 2011), hippocampal place cells (Buzsaki, 2005; Jeffery, 1998), and grid cells in the medial entorhinal cortex (Hafting et al, 2005; Perez-Escobar et al, 2016). A number of theoretical studies have shown the importance of landmarks for error correction during spatial computations (Burgess et al, 2007; Fuhs and Touretzky, 2006; Monaco et al, 2011; Sreenivasan and Fiete, 2011) It remains poorly understood how visual information is integrated into spatial code for goal-directed behavior
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