For more than 30 years, a growing number of researchers have been attracted to the challenge of understanding the neurobiological organization of the avian hippocampal formation (HF) and its relationship to the remarkable spatial cognitive abilities of birds. In this selective review, we highlight recent anatomical and developmental findings that reveal a HF design that defies any simple comparison to the mammalian hippocampus and leaves unanswered the seemingly enduring question of whether a dentate gyrus homologue is to be found in HF. From a functional perspective, we highlight the recent discoveries that implicate HF in the use of space for memory pattern segregation and continued interest in the role HF neurogenesis may play in supporting memory function and its relationship to memory decline in aging birds. We also summarize data that nurture a fundamental reinterpretation of the role of HF in spatial cognition by suggesting HF involvement in spatial perception antecedent to any memory formation. Given the disproportionate adaptive significance of space for birds, which has led to the evolution of their exceptional navigational and memory abilities, there is little doubt that the avian HF will continue to provide important and unexpected insights into the neural basis of spatial cognition.

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The hippocampus is particularly susceptible to age-related degeneration that, like hippocampal lesions, is thought to lead to age-related decline in spatial memory and navigation. Lesions to the avian hippocampal formation (HF) also result in impaired spatial memory and navigation, but the relationship between aging and HF-dependent spatial cognition is unknown. To investigate possible age-related decline in avian spatial cognition, the current study investigated spatial working memory performance in older homing pigeons (10+ years of age). Pigeons completed a behavioral procedure nearly identical to the delayed spatial, win-shift procedure in a modified radial arm maze that has been previously used to study spatial working memory in rats and pigeons. The results revealed that the older pigeons required a greater number of choices to task completion and were less accurate with their first 4 choices as compared to younger pigeons (1-2 years of age). In addition, older pigeons were more likely to adopt a stereotyped sampling strategy, which explained in part their impaired performance. To the best of our knowledge, this study is the first to demonstrate an age-related impairment of HF-dependent, spatial memory in birds. Implications and future directions of the findings are discussed.

The importance of the vertebrate hippocampus in spatial cognition is often related to its broad role in memory. However, in birds, the hippocampus appears to be more specifically involved in spatial processes. The maturing of GPS-tracking technology has enabled a revolution in navigation research, including the expanded possibility of studying brain mechanisms that guide navigation in the field. By GPS-tracking homing pigeons released from distant, unfamiliar sites prior to and after hippocampal lesion, we observed, as has been reported previously, impaired navigational performance post-lesion over the familiar/memorized space near the home loft, where topographic features constitute an important source of navigational information. The GPS-tracking revealed that many of the lost pigeons, when lesioned, approached the home area, but nevertheless failed to locate their loft. Unexpectedly, when they were hippocampal-lesioned, the pigeons showed a notable change in their behaviour when navigating over the unfamiliar space distant from home; they actually flew straighter homeward-directed paths than they did pre-lesion. The data are consistent with the hypothesis that, following hippocampal lesion, homing pigeons respond less to unfamiliar visual, topographic features encountered during homing, and, as such, offer the first evidence for an unforeseen, perceptual neglect of environmental features following hippocampal damage.

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It is generally accepted that the geometry of an environment is a reliable source of information for spatial navigation used by most vertebrate species. However, there is a continuing debate on which geometrical properties of space are the ones that matter for reorientation. In this study, pigeons were trained to find a food reward hidden in 2 opposite corners in a rectangular arena. The animals were then tested in a kite-shaped environment similar to Pearce, Good, Jones, and McGregor (2004). We found that pigeons, unlike rats, were not able to identify the correct corner in the kite arena even though elements clearly preserved the correct long wall-short wall geometric configuration and the local aspect of the trained goal. This behavioral study was followed by a c-Fos, IEG analysis of brain activation that contrasted pigeons exposed to the trained, familiar rectangular environment with pigeons that were exposed to an unfamiliar, trapezoid arena. The hippocampal formation (HF) displayed greater c-Fos expression in the animals exposed to the familiar, training arena, which further supports the conclusion that pigeons do not substantially rely on local geometric features for reorientation.

A visuocentric bias has dominated the literature on spatial navigation and reorientation. Studies on visually accessed environments indicate that, during reorientation, human and non-human animals encode the geometric shape of the environment, even if this information is unnecessary and insufficient for the task. In an attempt to extend our limited knowledge on the similarities and differences between visual and non-visual navigation, here we examined whether the same phenomenon would be observed during auditory-guided reorientation. Provided with a rectangular array of four distinct auditory landmarks, blindfolded, sighted participants had to learn the location of a target object situated on a panel of an octagonal arena. Subsequent test trials were administered to understand how the task was acquired. Crucially, in a condition in which the auditory cues were indistinguishable (same sound sample), participants could still identify the correct target location, suggesting that the rectangular array of auditory landmarks was encoded as a geometric configuration. This is the first evidence of incidental encoding of geometric information with auditory cues and, consistent with the theory of functional equivalence, it supports the generalisation of mechanisms of spatial learning across encoding modalities.