Towards the neurobiology of large-scale spatial cognition (Commentary on Gagliardo et al.)

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Spatial learning and memory in laboratory animals such as rats and mice has become almost a synonym for hippocampus and cognition, ever since O’Keefe and Nadel’s seminal book ‘The hippocampus as a cognitive map’ (O’Keefe & Nadel, 1978). Nonetheless, some nagging doubts remained, chiefly because practically all those lesion studies and place cell recordings took place in spatially constrained laboratory settings. In comparison to humans, these studies would reflect the rules of how a person moves from the bedroom to the toilet and back. But would these findings and concepts apply to real-world situations, in particular to animals that navigate efficiently across long distances, or might they eventually be classified as phenomena valid only in the spatial constraints of the typical laboratory?

In this issue of EJN, Gagliardo et al. (2009) found that the hippocampal formation is indeed involved in large-scale navigation. Homing pigeons have emerged as valuable subjects for the topic of animal navigation, because they return from unknown locations over many 100 km. The mechanisms underlying such long-distance navigation are still debated. However, within a so-called familiar home range or along a pre-trained route, precise path-tracking by means of GPS loggers has revealed that pigeons often use prominent landmarks or guiding structures (Lipp et al., 2004), particularly when flying alone (Dell’Ariccia et al., 2008). Recent work in our group has also shown that the EEG of flying pigeons responds to such landmarks (Vyssotski et al., 2006, 2009).

As it was known that lesions of the hippocampus do not interfere with long-distance navigation but impair classic navigational parameters (such as vanishing bearings) within the familiar home range, Gagliardo et al. (2009) aimed at elucidating the role of the avian hippocampus in this familiar-range navigation. However, they faced a problem because pigeons have redundant and partially hippocampus-independent navigational mechanisms that permit them to overcome missing bits of spatial information – a feature useful for the bird but an obstacle for the experimenter.

The beauty of these experiments is that they introduced a deliberate error in the navigation system of the pigeon by a classical procedure known as phase shifting. Homing pigeons use, inter alia, the position of the sun in determining a compass direction home. Keeping them under a time-shifted illumination schedule usually entails a bias in vanishing bearings under sunny skies, depending on whether the internal clock is shifted clock- or counterclockwise. At some point of their journey, the pigeons start to correct their flight path, and arrive at home within a moderate delay only. The authors now used this clock-shifting technique to monitor by GPS the time course of path correction in hippocampally lesioned and control birds, and found that lesioned birds took more time to correct and, perhaps more importantly, neglected some prominent landscape features such as the coastline. This is a strong argument in favor of a role of the avian hippocampus in assembling a visual mental map within a range where they use it naturally.

Further experiments will be needed to dissect the role the participating brain structures, but the presented paper demonstrates that behavioral neuroscience is not bound to the laboratory. As shown here, modern GPS-tracking and data-logging techniques enable scientists to tackle the neurobiological and cognitive mechanisms of fascinating and hitherto unapproachable phenomena such as animal migration, homing and navigation in real-world scenarios.

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