Jeffery et al.'s target article is a fascinating synthesis of the relatively scarce but expanding research on three-dimensional navigation, in addition to proposing an engaging hypothesis on the neural representation of vertical space. As recognized by Jeffery et al., birds offer intriguing possibilities as model species for investigating the behavioral and neurological bases of navigation in 3D space. Studies on homing pigeons (Columba livia) suggest that the topography of the landscape is an important source of information for bird navigation. As mentioned by Jeffery et al., sloped terrain provides a global feature and – at least locally – a directional reference frame. The extent to which pigeons encode and use this reference frame, when walking on a slanted floor, is impressive (Nardi & Bingman Reference Nardi and Bingman2009a; Nardi et al. Reference Nardi, Nitsch and Bingman2010). A crucial attribute of slope – and more generally, the vertical dimension – is the involvement of effort. This has been highlighted in rats, which show a strategy preference for horizontal movements relative to vertical movements (Grobéty & Schenk Reference Grobéty and Schenk1992a; Jovalekic et al. Reference Jovalekic, Hayman, Becares, Reid, Thomas, Wilson and Jeffery2011). In pigeons, evidence suggests that effort, modulated by different, energetically demanding upward and downward movements, affects how a sloped environment is represented, or at least used (Nardi et al. Reference Nardi, Mauch, Klimas and Bingman2012). This strengthens the hypothesis that effort could be used as a “contextual” cue, in the sense proposed by Jeffery et al., derived from kinesthetic/proprioceptive information during locomotion on a slope. Importantly, hippocampal lesions in pigeons do not impair the slope-based goal representation (Nardi & Bingman Reference Nardi and Bingman2009b), despite having disruptive effects on memory for other spatial cues (e.g., Gagliardo et al. Reference Gagliaro, Ioalè and Bingman1999; Vargas et al. Reference Vargas, Petruso and Bingman2004). Possibly slope does not engage the hippocampus because it is used more as a source of directional, compass-like information than for determining distances and map-like information. More studies are needed to ascertain the role of effort in the representation of sloped – and volumetric – space, and its neurological underpinnings.
Beyond pigeons, the class Aves, with its rich diversity in natural history, offers exciting opportunities to apply comparative methods for better understanding the representation of 3D space. Although Jeffery et al. acknowledge that evolutionary adaptation (and constraints), reflected in species natural history, may be important in how vertical and horizontal space may be integrated, they offer few explicit hypotheses that can be answered by comparative-based research. As a well-known example of the power of comparative research, the larger hippocampus and superior spatial cognitive abilities of food-storing birds (e.g., Pravosudov & Clayton Reference Pravosudov and Clayton2002) indicate that differential evolutionary pressure can lead to variation in natural history, which co-occurs with variation in brain-behavior organization. We are similarly convinced that interesting differences can also be found with respect to navigating 3D space at both the relatively easily studied behavioral level and the more difficult to study neurobiological level. Almost all species of birds fly and necessarily inhabit a three-dimensional world, but often differ with respect to their “3D occupancy profile.” For example, ground birds, such as some quail species (family Odontophoridae) inhabit a robustly horizontal space, whereas tree creepers (family Certhididae) search for food vertically but move horizontally among different trees, and wallcreepers (family Tichodromidae) live in the substantially vertical world of cliff faces.Footnote
1
How might natural differences in horizontal, vertical, and volumetric occupancy influence the representation of space and its neural encoding in the hippocampal formation or elsewhere in the brain?
In our opinion, the most exciting and novel hypothesis advanced by Jeffery et al. is the notion that horizontal space is more richly represented and is dissociated, at least partially, from the relatively impoverished, contextual representation of vertical space. And this may indeed be true for species such as rats and even humans. We wonder, however, how generally applicable this idea may be. The black-capped chickadee (Poecile atricapillus) is a remarkable species of bird that routinely lives in the complex volumetric space of deciduous trees and will seasonally store and later recover seeds within the chaotic world of intersecting tree branches – a behavior dependent on the integrity of the hippocampal formation (Sherry & Vaccarino Reference Sherry and Vaccarino1989). Chickadees apply their robust, spatial memory ability in a 3D space, which may appear multilayered but, because deciduous tree branches can intersect at almost any angle, would often be better characterized as true volumetric space. (Coniferous trees have a more multilayered quality.) The survival of individuals is very much dependent on “volumetric encoding” of stored food that would likely suffer if only a contextual heuristic would be used to encode vertical location. From a purely adaptationist perspective, if any species – and more generally, any natural history profile – would support the evolution of a unified representation of volumetric space, it would be the black-capped chickadee and other species that store seeds in deciduous trees. As a natural comparative experiment, chickadees could be contrasted with the Clark's nutcracker (Nucifraga columbiana), which also stores seeds and has an extraordinary ability to recall the locations of those seeds (e.g., Kamil et al. Reference Kamil, Balda and Olson1994). However, whereas chickadees store seeds within the volumetric space of tree limbs, nutcrackers store them in the ground, in a rolling but two-dimensional horizontal space. Would chickadees outperform nutcrackers in a spatial memory task in a sloping, multilayered or volumetric space? Would hippocampal neurons in chickadees be more likely to encode aspects of volumetric space?
We are not advocating that comparative approaches would answer all the important questions raised by Jeffery et al., but we hope we have convinced the reader that comparative research – not necessarily limited to birds – is a powerful experimental strategy that can reveal much about the diversity of three-dimensional spatial representations.
Jeffery et al.'s target article is a fascinating synthesis of the relatively scarce but expanding research on three-dimensional navigation, in addition to proposing an engaging hypothesis on the neural representation of vertical space. As recognized by Jeffery et al., birds offer intriguing possibilities as model species for investigating the behavioral and neurological bases of navigation in 3D space. Studies on homing pigeons (Columba livia) suggest that the topography of the landscape is an important source of information for bird navigation. As mentioned by Jeffery et al., sloped terrain provides a global feature and – at least locally – a directional reference frame. The extent to which pigeons encode and use this reference frame, when walking on a slanted floor, is impressive (Nardi & Bingman Reference Nardi and Bingman2009a; Nardi et al. Reference Nardi, Nitsch and Bingman2010). A crucial attribute of slope – and more generally, the vertical dimension – is the involvement of effort. This has been highlighted in rats, which show a strategy preference for horizontal movements relative to vertical movements (Grobéty & Schenk Reference Grobéty and Schenk1992a; Jovalekic et al. Reference Jovalekic, Hayman, Becares, Reid, Thomas, Wilson and Jeffery2011). In pigeons, evidence suggests that effort, modulated by different, energetically demanding upward and downward movements, affects how a sloped environment is represented, or at least used (Nardi et al. Reference Nardi, Mauch, Klimas and Bingman2012). This strengthens the hypothesis that effort could be used as a “contextual” cue, in the sense proposed by Jeffery et al., derived from kinesthetic/proprioceptive information during locomotion on a slope. Importantly, hippocampal lesions in pigeons do not impair the slope-based goal representation (Nardi & Bingman Reference Nardi and Bingman2009b), despite having disruptive effects on memory for other spatial cues (e.g., Gagliardo et al. Reference Gagliaro, Ioalè and Bingman1999; Vargas et al. Reference Vargas, Petruso and Bingman2004). Possibly slope does not engage the hippocampus because it is used more as a source of directional, compass-like information than for determining distances and map-like information. More studies are needed to ascertain the role of effort in the representation of sloped – and volumetric – space, and its neurological underpinnings.
Beyond pigeons, the class Aves, with its rich diversity in natural history, offers exciting opportunities to apply comparative methods for better understanding the representation of 3D space. Although Jeffery et al. acknowledge that evolutionary adaptation (and constraints), reflected in species natural history, may be important in how vertical and horizontal space may be integrated, they offer few explicit hypotheses that can be answered by comparative-based research. As a well-known example of the power of comparative research, the larger hippocampus and superior spatial cognitive abilities of food-storing birds (e.g., Pravosudov & Clayton Reference Pravosudov and Clayton2002) indicate that differential evolutionary pressure can lead to variation in natural history, which co-occurs with variation in brain-behavior organization. We are similarly convinced that interesting differences can also be found with respect to navigating 3D space at both the relatively easily studied behavioral level and the more difficult to study neurobiological level. Almost all species of birds fly and necessarily inhabit a three-dimensional world, but often differ with respect to their “3D occupancy profile.” For example, ground birds, such as some quail species (family Odontophoridae) inhabit a robustly horizontal space, whereas tree creepers (family Certhididae) search for food vertically but move horizontally among different trees, and wallcreepers (family Tichodromidae) live in the substantially vertical world of cliff faces.Footnote 1 How might natural differences in horizontal, vertical, and volumetric occupancy influence the representation of space and its neural encoding in the hippocampal formation or elsewhere in the brain?
In our opinion, the most exciting and novel hypothesis advanced by Jeffery et al. is the notion that horizontal space is more richly represented and is dissociated, at least partially, from the relatively impoverished, contextual representation of vertical space. And this may indeed be true for species such as rats and even humans. We wonder, however, how generally applicable this idea may be. The black-capped chickadee (Poecile atricapillus) is a remarkable species of bird that routinely lives in the complex volumetric space of deciduous trees and will seasonally store and later recover seeds within the chaotic world of intersecting tree branches – a behavior dependent on the integrity of the hippocampal formation (Sherry & Vaccarino Reference Sherry and Vaccarino1989). Chickadees apply their robust, spatial memory ability in a 3D space, which may appear multilayered but, because deciduous tree branches can intersect at almost any angle, would often be better characterized as true volumetric space. (Coniferous trees have a more multilayered quality.) The survival of individuals is very much dependent on “volumetric encoding” of stored food that would likely suffer if only a contextual heuristic would be used to encode vertical location. From a purely adaptationist perspective, if any species – and more generally, any natural history profile – would support the evolution of a unified representation of volumetric space, it would be the black-capped chickadee and other species that store seeds in deciduous trees. As a natural comparative experiment, chickadees could be contrasted with the Clark's nutcracker (Nucifraga columbiana), which also stores seeds and has an extraordinary ability to recall the locations of those seeds (e.g., Kamil et al. Reference Kamil, Balda and Olson1994). However, whereas chickadees store seeds within the volumetric space of tree limbs, nutcrackers store them in the ground, in a rolling but two-dimensional horizontal space. Would chickadees outperform nutcrackers in a spatial memory task in a sloping, multilayered or volumetric space? Would hippocampal neurons in chickadees be more likely to encode aspects of volumetric space?
We are not advocating that comparative approaches would answer all the important questions raised by Jeffery et al., but we hope we have convinced the reader that comparative research – not necessarily limited to birds – is a powerful experimental strategy that can reveal much about the diversity of three-dimensional spatial representations.
ACKNOWLEDGMENT
We would like to thank David Sherry for providing some helpful advice.