Abstract

Studies of human and rodent navigation often reveal a remarkable cross-species similarity between the cognitive and neural mechanisms of navigation. Such cross-species resemblance often overshadows some critical differences between how humans and nonhuman animals navigate. In this review, I propose that a navigation system requires both a storage system (i.e., representing spatial information) and a positioning system (i.e., sensing spatial information) to operate. I then argue that the way humans represent spatial information is different from that inferred from the cellular activity observed during rodent navigation. Such difference spans the whole hierarchy of spatial representation, from representing the structure of an environment to the representation of subregions of an environment, routes and paths, and the distance and direction relative to a goal location. These cross-species inconsistencies suggest that what we learn from rodent navigation does not always transfer to human navigation. Finally, I argue for closing the loop for the dominant, unidirectional animal-to-human approach in navigation research so that insights from behavioral studies of human navigation may also flow back to shed light on the cellular mechanisms of navigation for both humans and other mammals (i.e., a human-to-animal approach).

Highlights

  • Since Tolman’s (1948) original concept of a “cognitive map,” research on nonhuman animal navigation has long inspired studies of how the human navigation system functions (Lee 2017; Wang and Spelke 2002)

  • How we sense the distance affects how we represent and reproduce it (Arnold et al 2016; Brunec et al 2017; Chrastil and Warren 2014a; Waller et al 2004). These results indicate that human distance representation does not always correspond to the extrinsic physical metrics

  • Howard et al (2014) demonstrated that human hippocampal activity is related to the route and the Euclidean distance to a goal, it is hard to discern whether such distance representation was based on sensory odometer or visuospatial memory of a map

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Summary

Introduction

Since Tolman’s (1948) original concept of a “cognitive map,” research on nonhuman animal navigation has long inspired studies of how the human navigation system functions (Lee 2017; Wang and Spelke 2002). Human estimation of distance and direction is often biased and inconsistent (Ishikawa and Montello 2006; Loomis et al 1993; McNamara and Diwadkar 1997). Humans show significant errors in representing the relative direction of geographic places (e.g., cities in North America)—spatial knowledge obtained from map learning (Friedman 2009; Zhang et al 2014a).

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