The target article by Jeffery et al. reviews the literature on three-dimensional spatial navigation and highlights important considerations for interpreting both behavioral and neurobiological data on this topic. In their review, they lay the foundation for the hypothesis that three-dimensional spatial navigation is “bicoded” – that is, based on different encoding mechanisms for horizontal and vertical space. Furthermore, they argue that a fully three-dimensional map has never evolved in any species.
The “bicoded” model is based on studies of animals that move along surfaces to navigate, which constrains the design of experiments and the data used to build theory. For a complete theory of three-dimensional spatial navigation, a wider range of animals must be studied. In particular, data from animals that freely navigate three-dimensional volumetric space will help determine whether a single model can account for three-dimensional spatial navigation in terrestrial, aerial, and aquatic species. Counter to the model proposed by the authors of the target article, I hypothesize that a fully three-dimensional volumetric map has evolved in species that are not limited to navigating along surfaces. More broadly, I hypothesize that three-dimensional spatial representation depends upon an animal's mode of locomotion and the navigational tasks it encounters in the natural environment.
Another point I would like to make is that models of three-dimensional spatial navigation must be grounded in behavioral and neurobiological studies of animals engaged in biologically relevant and natural tasks. For example, rodents have conveniently served as animal models for a wide range of studies, including spatial navigation. Many rodent maze studies are, however, highly artificial, requiring that animals perform tasks they are unlikely to encounter in a natural setting, and in spaces far more restricted than they would navigate in the wild. The study of inbred rodents that have not navigated the natural environment for many generations raises additional concerns.
Research traditions have limited the study of spatial navigation, and advances in the field require a comparative approach. The importance of choosing the right animals for the questions under study, first articulated by Nobel Laureate August Krogh (Reference Krogh1929), is widely recognized in the field of Neuroethology, but is less influential in the broad field of Systems Neuroscience. It is important that the spatial navigation research community interested in problems of three-dimensional spatial navigation turn to the study of animals that have evolved to solve this problem.
Echolocating bats present an excellent model system to pursue questions about three-dimensional spatial navigation. Bats belong to the order Chiroptera, many species of which use biological sonar systems to represent the spatial location of targets and obstacles. In turn, this spatial information is used to build a cognitive map that can guide navigation in the absence of sensory cues. Anecdotal reports and laboratory studies of echolocating bats provide evidence that bats rely strongly on spatial memory (Griffin Reference Griffin1958; Jensen et al. Reference Jensen, Moss and Surlykke2005), and field studies show that bats use memory on many different spatial scales (Schnitzler et al. Reference Schnitzler, Moss and Denzinger2003; Tsoar et al. Reference Tsoar, Nathan, Bartan, Vyssotski, Dell'Omo and Ulanovsky2011). Importantly, bats use an absolute-space–based (allocentric) navigational strategy that is hippocampus-dependent, and place cells have been identified and characterized in the bat hippocampus (Ulanovsky & Moss Reference Ulanovsky and Moss2007; Yartsev & Ulanovsky Reference Yartsev and Ulanovsky2013). Furthermore, grid cells have been recently described in the medial entorhinal cortex (MEC) of the Egyptian fruit bat (Yartsev et al. Reference Yartsev, Witter and Ulanovsky2011). Therefore, echolocating bats are particularly well suited for researchers to use in behavioral, neurobiological, and computational studies of three-dimensional spatial navigation.
Neural recording data from the MEC and hippocampus of bats have raised questions about the generality of the rodent model in spatial representation. Although neural recordings from awake, behaving rats and bats show that neurons in the hippocampus and MEC represent two-dimensional space in a similar way (Ulanovsky & Moss Reference Ulanovsky and Moss2007; Yartsev et al. Reference Yartsev, Witter and Ulanovsky2011), there is one noteworthy difference, namely an absence of continuous theta oscillations in hippocampal recordings from the big brown bat (Ulanovsky & Moss Reference Ulanovsky and Moss2007) and the MEC and hippocampus in the Egyptian fruit bat (Yartsev et al. Reference Yartsev, Witter and Ulanovsky2011; Yartsev & Ulanovsky Reference Yartsev and Ulanovsky2013). Whole cell patch clamp studies of the MEC of the big brown also demonstrate differences in subthreshold membrane potential resonance between bats and rats (Heys et al. Reference Heys, MacLeod, Moss and Hasselmo2013). These reported species differences challenge a fundamental assumption of the oscillatory interference model of spatial coding (e.g., Burgess et al. Reference Burgess, Barry and O'Keefe2007; Hasselmo et al. Reference Hasselmo, Giocomo and Zilli2007). By extension, comparative data could raise questions about the generality of three-dimensional spatial coding mechanisms in the brains of animals that have evolved to navigate along surfaces, compared with those that move freely through three-dimensional volumetric spaces, such as air and water.
In summary, I propose that it is premature to assert that a fully three-dimensional map has never evolved in any species, as empirical data are lacking to support the notion that three-dimensional space coding in all animals is the same. Recent findings from Yartsev & Ulanovsky (Reference Yartsev and Ulanovsky2013), demonstrating three-dimensional space representation in the hippocampus of the free-flying Egyptian Fruit bat, are consistent with the hypothesis that space representation is tied to an animal's mode of locomotion. To fully test this hypothesis requires a large body of comparative data.
The target article by Jeffery et al. reviews the literature on three-dimensional spatial navigation and highlights important considerations for interpreting both behavioral and neurobiological data on this topic. In their review, they lay the foundation for the hypothesis that three-dimensional spatial navigation is “bicoded” – that is, based on different encoding mechanisms for horizontal and vertical space. Furthermore, they argue that a fully three-dimensional map has never evolved in any species.
The “bicoded” model is based on studies of animals that move along surfaces to navigate, which constrains the design of experiments and the data used to build theory. For a complete theory of three-dimensional spatial navigation, a wider range of animals must be studied. In particular, data from animals that freely navigate three-dimensional volumetric space will help determine whether a single model can account for three-dimensional spatial navigation in terrestrial, aerial, and aquatic species. Counter to the model proposed by the authors of the target article, I hypothesize that a fully three-dimensional volumetric map has evolved in species that are not limited to navigating along surfaces. More broadly, I hypothesize that three-dimensional spatial representation depends upon an animal's mode of locomotion and the navigational tasks it encounters in the natural environment.
Another point I would like to make is that models of three-dimensional spatial navigation must be grounded in behavioral and neurobiological studies of animals engaged in biologically relevant and natural tasks. For example, rodents have conveniently served as animal models for a wide range of studies, including spatial navigation. Many rodent maze studies are, however, highly artificial, requiring that animals perform tasks they are unlikely to encounter in a natural setting, and in spaces far more restricted than they would navigate in the wild. The study of inbred rodents that have not navigated the natural environment for many generations raises additional concerns.
Research traditions have limited the study of spatial navigation, and advances in the field require a comparative approach. The importance of choosing the right animals for the questions under study, first articulated by Nobel Laureate August Krogh (Reference Krogh1929), is widely recognized in the field of Neuroethology, but is less influential in the broad field of Systems Neuroscience. It is important that the spatial navigation research community interested in problems of three-dimensional spatial navigation turn to the study of animals that have evolved to solve this problem.
Echolocating bats present an excellent model system to pursue questions about three-dimensional spatial navigation. Bats belong to the order Chiroptera, many species of which use biological sonar systems to represent the spatial location of targets and obstacles. In turn, this spatial information is used to build a cognitive map that can guide navigation in the absence of sensory cues. Anecdotal reports and laboratory studies of echolocating bats provide evidence that bats rely strongly on spatial memory (Griffin Reference Griffin1958; Jensen et al. Reference Jensen, Moss and Surlykke2005), and field studies show that bats use memory on many different spatial scales (Schnitzler et al. Reference Schnitzler, Moss and Denzinger2003; Tsoar et al. Reference Tsoar, Nathan, Bartan, Vyssotski, Dell'Omo and Ulanovsky2011). Importantly, bats use an absolute-space–based (allocentric) navigational strategy that is hippocampus-dependent, and place cells have been identified and characterized in the bat hippocampus (Ulanovsky & Moss Reference Ulanovsky and Moss2007; Yartsev & Ulanovsky Reference Yartsev and Ulanovsky2013). Furthermore, grid cells have been recently described in the medial entorhinal cortex (MEC) of the Egyptian fruit bat (Yartsev et al. Reference Yartsev, Witter and Ulanovsky2011). Therefore, echolocating bats are particularly well suited for researchers to use in behavioral, neurobiological, and computational studies of three-dimensional spatial navigation.
Neural recording data from the MEC and hippocampus of bats have raised questions about the generality of the rodent model in spatial representation. Although neural recordings from awake, behaving rats and bats show that neurons in the hippocampus and MEC represent two-dimensional space in a similar way (Ulanovsky & Moss Reference Ulanovsky and Moss2007; Yartsev et al. Reference Yartsev, Witter and Ulanovsky2011), there is one noteworthy difference, namely an absence of continuous theta oscillations in hippocampal recordings from the big brown bat (Ulanovsky & Moss Reference Ulanovsky and Moss2007) and the MEC and hippocampus in the Egyptian fruit bat (Yartsev et al. Reference Yartsev, Witter and Ulanovsky2011; Yartsev & Ulanovsky Reference Yartsev and Ulanovsky2013). Whole cell patch clamp studies of the MEC of the big brown also demonstrate differences in subthreshold membrane potential resonance between bats and rats (Heys et al. Reference Heys, MacLeod, Moss and Hasselmo2013). These reported species differences challenge a fundamental assumption of the oscillatory interference model of spatial coding (e.g., Burgess et al. Reference Burgess, Barry and O'Keefe2007; Hasselmo et al. Reference Hasselmo, Giocomo and Zilli2007). By extension, comparative data could raise questions about the generality of three-dimensional spatial coding mechanisms in the brains of animals that have evolved to navigate along surfaces, compared with those that move freely through three-dimensional volumetric spaces, such as air and water.
In summary, I propose that it is premature to assert that a fully three-dimensional map has never evolved in any species, as empirical data are lacking to support the notion that three-dimensional space coding in all animals is the same. Recent findings from Yartsev & Ulanovsky (Reference Yartsev and Ulanovsky2013), demonstrating three-dimensional space representation in the hippocampus of the free-flying Egyptian Fruit bat, are consistent with the hypothesis that space representation is tied to an animal's mode of locomotion. To fully test this hypothesis requires a large body of comparative data.
ACKNOWLEDGMENT
Supported by ONR Grant (N00014-12-1-0339), Three-dimensional Spatial Navigation, to Cynthia F. Moss and Timothy Horiuchi.