Age-related reductions in whole brain mass and telencephalon volume in very old white Carneau pigeons (Columba livia).

While studies have identified age-related cognitive impairment in pigeons (Columba livia), no study has detected the brain atrophy which typically accompanies cognitive impairment in older mammals. Instead, Coppola and Bingman (Aging is associated with larger brain mass and volume in homing pigeons (Columba livia), Neurosci. Letters 698 (2019) 39-43) reported increased whole brain mass and telencephalon volume in older, compared to younger, homing pigeons. One reason for this unexpected finding might be that the older pigeons studied were not old enough to display age-related brain atrophy. Therefore, the current study repeated Coppola and Bingman, but with a sample of older white Carneau pigeons that were on average 5.34 years older. Brains from young and old homing pigeons were weighed and orthogonal measurements of the telencephalon, cerebellum, and optic tectum were obtained. Despite having a heavier body mass than younger pigeons, older pigeons had a significant reduction in whole brain mass and telencephalon volume, but not cerebellum or optic tectum volume. This study is therefore the first to find that pigeons experience age-related brain atrophy.

Investigating boundary-geometry use by whip spiders (Phrynus marginemaculatus) during goal-directed navigation.

Previous studies have shown that whip spiders (Amblypygi) can use a variety of cues to navigate to and recognize a home refuge. The current study aimed to determine whether whip spiders were capable of using the boundary geometry of an experimental space (geometric information) to guide goal-directed navigation and to investigate any preferential use of geometric or feature (visual) information. Animals were first trained to find a goal location situated in one corner of a rectangular arena (geometric information) fronting a dark-green-colored wall, which created a brightness contrast with the other three white walls (feature information). Various probe trials were then implemented to determine cue use. It was found that animals were capable of directing their choice behavior towards geometrically correct corners at a rate significantly higher than chance, even when the feature cue was removed. By contrast, choice behavior dropped to random chance when geometric information was removed (test in a square arena) and only feature information remained. Choice behavior was also reduced to chance when geometric and feature information were set in conflict (by moving the feature cue to one of the longer walls in the rectangular arena). The data thus suggest that whip spiders are capable of using geometric information to guide goal-directed navigation and that geometric information is preferred over feature guidance, although a feature cue may set the context for activating geometry-guided navigation. Experimental design limitations and future directions are discussed.

Spatial reorientation with a geometric array of auditory cues.

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.

Visual control of refuge recognition in the whip spider Phrynus marginemaculatus.

Amblypygids, or whip spiders, are nocturnally active arachnids which live in structurally complex environments. Whip spiders are excellent navigators that can re-locate a home refuge without relying on visual input. Therefore, an open question is whether visual input can control any aspect of whip spider spatial behavior. In the current study, Phrynus marginemaculatus were trained to locate an escape refuge by discriminating between differently oriented black and white stripes placed either on the walls of a testing arena (frontal discrimination) or on the ceiling of the same testing arena (overhead discrimination). Regardless of the placement of the visual stimuli, the whip spiders were successful in learning the location of the escape refuge. In a follow-up study of the overhead discrimination, occluding the median eyes was found to disrupt the ability of the whip spiders to locate the shelter. The data support the conclusion that whip spiders can rely on vision to learn and recognize an escape shelter. We suggest that visual inputs to the brain's mushroom bodies enable this ability.

Age-associated decline in septum neuronal activation during spatial learning in homing pigeons (Columba livia).

The relationship between hippocampal aging and spatial-cognitive decline in birds has recently been investigated. However, like its mammalian counterpart, the avian hippocampus does not work in isolation and its relationship to the septum is of particular interest. The current study aimed to investigate the effects of age on septum (medial and lateral) and associated nucleus of the diagonal band (NDB) neuronal activation (as indicated by c-Fos expression) during learning of a spatial, delayed non-match-to-sample task conducted in a modified radial arm maze. The results indicated significantly reduced septum, but not NDB, activation during spatial learning in older pigeons. We also preliminarily investigated the effect of age on the number of cholinergic septum and NDB neurons (as indicated by expression of choline acetyltransferase; ChAT). Although underpowered to reveal a statistical effect, the data suggest that older pigeons have substantially fewer ChAT-expressing cells in the septum compared to younger pigeons. The data support the hypothesis that reduced activation of the septum contributes to the age-related, spatial cognitive impairment in pigeons.

Vertical-surface navigation in the Neotropical whip spider Paraphrynus laevifrons (Arachnida: Amblypygi).

Studies on whip spider navigation have focused on their ability to locate goal locations in the horizontal plane (e.g., when moving along the ground). However, many species of tropical whip spiders reside and move along surfaces in the vertical plane (e.g., trees). Under controlled laboratory conditions, the current study investigated the ability of the tropical whip spider, Paraphrynus laevifrons, to return to a home shelter on a vertical surface in the presence of numerous, similar and competing refuge sites, as well as the distribution of navigational errors in the vertical, horizontal and diagonal plane. We also assessed the relative importance of sensory cues originating from a previously occupied home shelter compared to the position of a previously occupied shelter in guiding shelter choice. It was found that P. laevifrons displays robust fidelity in re-locating a home shelter on a vertical surface. When navigational errors did occur, they were not significantly different in all three directions. Additionally, cue-conflict test trials revealed that cues associated with an original home shelter, likely self-deposited chemical signals, were more important than sources of positional information in guiding the shelter choice of P. laevifrons.

c-Fos revealed lower hippocampal participation in older homing pigeons when challenged with a spatial memory task.

Homing pigeons experience age-related spatial-cognitive decline similar to that seen in mammals. In contrast to mammals, however, previous studies have shown the hippocampal formation (HF) of old, cognitively impaired pigeons to be greater in volume and neuron number compared with young pigeons. As a partial explanation of the cognitive decline in older birds, it was hypothesized that older pigeons have reduced HF activation during spatial learning. The present study compared HF activation (via the activity-dependent expression of the immediate early gene c-Fos) between younger and older pigeons during learning of a spatial, delayed nonmatch-to-sample task. On the last day of training, c-Fos activation significantly correlated with behavioral performance in the young, but not old, pigeons suggesting more HF engagement by the young pigeons in solving the task. The behavioral correlation was additionally associated with consistently higher, but insignificant c-Fos activation across practically every HF subdivision in the young compared with the old pigeons. In sum, the results of the present study are consistent with the hypothesis that age-related decline in the spatial cognitive ability of homing pigeons is in part a result of an older HF being less responsive to the processing of spatial information. However, alternative interpretations of the data are discussed.

Aging is associated with larger brain mass and volume in homing pigeons (Columba livia).

In mammals, the brain decreases in mass and volume as a function of age. The current study is, to the best of our knowledge, the first to investigate age-related changes in brain mass and volume in birds. Following perfusion, brains from young and old homing pigeons were weighed on a balance and orthogonal measurements of the telencephalon, cerebellum, and tecta were obtained with a digital caliper. It was found that older pigeons had heavier brains than younger pigeons, a difference that remained after controlling for body mass. Additionally, older pigeons had on average greater estimated telencephalon volumes than younger pigeons, again also after controlling for body mass. Cerebellum and right tectum volumes also differed between age groups after controlling for body mass, with older pigeons having a larger cerebellum and right tectum than younger pigeons. In sum, brains are on average heavier and larger in old pigeons, which display age-related cognitive decline, compared to young adult pigeons. The larger brain in older homing pigeons also lies in stark contrast with aging of the mammalian brain.

Local geometric properties do not support reorientation in hippocampus-engaged homing pigeons.

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. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Changes in hippocampal volume and neuron number co-occur with memory decline in old homing pigeons (Columba livia).

The mammalian hippocampus is particularly susceptible to age-related structural changes, which have been used to explain, in part, age-related memory decline. These changes are generally characterized by atrophy (e.g., a decrease in volume and number of synaptic contacts). Recent studies have reported age-related spatial memory deficits in older pigeons similar to those seen in older mammals. However, to date, little is known about any co-occurring changes in the aging avian hippocampal formation (HF). In the current study, it was found that the HF of older pigeons was actually larger and contained more neurons than the HF of younger pigeons, a finding that suggests that the pattern of structural changes during aging in the avian HF is different from that seen in the mammalian hippocampus. A working hypothesis for relating the observed structural changes with spatial-cognitive decline is offered.

The maturation of research into the avian hippocampal formation: Recent discoveries from one of the nature's foremost navigators.

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.

An age-related deficit in spatial-feature reference memory in homing pigeons (Columba livia).

Age-related memory decline in mammals has been well documented. By contrast, very little is known about memory decline in birds as they age. In the current study we trained younger and older homing pigeons on a reference memory task in which a goal location could be encoded by spatial and feature cues. Consistent with a previous working memory study, the results revealed impaired acquisition of combined spatial-feature reference memory in older compared to younger pigeons. Following memory acquisition, we used cue-conflict probe trials to provide an initial assessment of possible age-related differences in cue preference. Both younger and older pigeons displayed a similarly modest preference for feature over spatial cues.

Age-related spatial working memory deficits in homing pigeons (Columba livia).

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.

Evidence for perceptual neglect of environmental features in hippocampal-lesioned pigeons during homing.

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.

Hippocampal lesions in homing pigeons do not impair feature-quality or feature-quantity discrimination.

The role of the avian hippocampal formation (HF) in spatial cognition is well demonstrated. However, it remains uncertain if the avian hippocampus, like its mammalian counterpart, has a role in the integration of elements that could compose a memory independent of space. The two experiments in the current study examined whether the HF of homing pigeons (Columba livia) was required to encode into memory a discriminative representation of food quality (Experiment 1) and quantity (Experiment 2) with different food bowl-features. Pigeons were exposed to an array of different colored bowls, two of which contained food rewards differing in preferred quality or quantity. To render space irrelevant for memory encoding, the location of the food-rewarded bowls was altered between each trial, while the features of the rewarded bowls remained constant. Both groups learned the feature-based quality and quantity discrimination tasks and no difference in performance between control pigeons and those with bilateral lesions of the hippocampus were found. The findings do not support the hypothesis that the avian HF is recruited when only non-spatial elements are integrated into a unified memory. From the current study, and the literature as a whole, it appears that the avian HF, unlike the mammalian hippocampus, may play no necessary role in memory processes where space is irrelevant.