Amphibian spatial cognition, medial pallium and other supporting telencephalic structures.

Vertebrate hippocampal formation is central to conversations on the comparative analysis of spatial cognition, especially in light of variation found in different vertebrate classes. Assuming the medial pallium (MP) of extant amphibians resembles the hippocampal formation (HF) of ancestral stem tetrapods, we propose that the HF of modern amniotes began with a MP characterized by a relatively undifferentiated cytoarchitecture, more direct thalamic/olfactory sensory inputs, and a more generalized role in associative learning-memory processes. As such, hippocampal evolution in amniotes, especially mammals, can be seen as progressing toward a cytoarchitecture with well-defined subdivisions, regional connectivity, and a functional specialization supporting map-like representations of space. We then summarize a growing literature on amphibian spatial cognition and its underlying brain organization. Emphasizing the MP/HF, we highlight that further research into amphibian spatial cognition would provide novel insight into the role of the HF in spatial memory processes, and their supporting neural mechanisms. A more complete reconstruction of hippocampal evolution would benefit from additional research on non-mammalian vertebrates, with amphibians being of particular interest.

The avian olfactory system and hippocampus: Complementary roles in the olfactory and visual guidance of homing pigeon navigation.

The homing pigeon is the foundational model species used to investigate the neural control of avian navigation. The olfactory system is critically involved in implementing the so-called olfactory map, used to locate position relative to home from unfamiliar locations. The hippocampal formation supports a complementary navigational system based on familiar visual landmarks. Insight into the neural control of pigeon navigation has been revolutionised by GPS-tracking technology, which has been crucial for both detailing the critical role of environmental odours for navigation over unfamiliar areas as well as offering unprecedented insight into the role of the hippocampal formation in visual landscape/landmark-based navigation, including a possible, unexpected role in visual-spatial perception.

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.

GPS tracking technology and re-visiting the relationship between the avian visual Wulst and homing pigeon navigation.

Within their familiar areas homing pigeons rely on familiar visual landscape features and landmarks for homing. However, the neural basis of visual landmark-based navigation has been so far investigated mainly in relation to the role of the hippocampal formation. The avian visual Wulst is the telencephalic projection field of the thalamofugal pathway that has been suggested to be involved in processing lateral visual inputs that originate from the far visual field. The Wulst is therefore a good candidate for a neural structure participating in the visual control of familiar visual landmark-based navigation. We repeatedly released and tracked Wulst-lesioned and control homing pigeons from three sites about 10-15 km from the loft. Wulst lesions did not impair the ability of the pigeons to orient homeward during the first release from each of the three sites nor to localise the loft within the home area. In addition, Wulst-lesioned pigeons displayed unimpaired route fidelity acquisition to a repeated homing path compared to the intact birds. However, compared to control birds, Wulst-lesioned pigeons displayed persistent oscillatory flight patterns across releases, diminished attention to linear (leading lines) landscape features, such as roads and wood edges, and less direct flight paths within the home area. Differences and similarities between the effects of Wulst and hippocampal lesions suggest that although the visual Wulst does not seem to play a direct role in the memory representation of a landscape-landmark map, it does seem to participate in influencing the perceptual construction of such a map.

Unpacking the navigation toolbox: insights from comparative cognition.

The study of navigation is informed by ethological data from many species, laboratory investigation at behavioural and neurobiological levels, and computational modelling. However, the data are often species-specific, making it challenging to develop general models of how biology supports behaviour. Wiener et al. outlined a framework for organizing the results across taxa, called the 'navigation toolbox' (Wiener et al. In Animal thinking: contemporary issues in comparative cognition (eds R Menzel, J Fischer), pp. 51-76). This framework proposes that spatial cognition is a hierarchical process in which sensory inputs at the lowest level are successively combined into ever-more complex representations, culminating in a metric or quasi-metric internal model of the world (cognitive map). Some animals, notably humans, also use symbolic representations to produce an external representation, such as a verbal description, signpost or map that allows communication of spatial information or instructions between individuals. Recently, new discoveries have extended our understanding of how spatial representations are constructed, highlighting that the hierarchical relationships are bidirectional, with higher levels feeding back to influence lower levels. In the light of these new developments, we revisit the navigation toolbox, elaborate it and incorporate new findings. The toolbox provides a common framework within which the results from different taxa can be described and compared, yielding a more detailed, mechanistic and generalized understanding of navigation.

A different perspective on avian hippocampus function: Visual-spatial perception.

The behavioral and neural mechanisms that support spatial cognition have been an enduring interest of psychologists, and much of that enduring interest is attributable to the groundbreaking research of Ken Cheng. One manifestation of this interest, inspired by the idea of studying spatial cognition under natural field conditions, has been research carried out to understand the role of the avian hippocampal formation (HF) in supporting homing pigeon navigation. Emerging from that research has been the conclusion that the role of HF in homing pigeon navigation aligns well with the canonical narrative of a hippocampus important for spatial memory and the implementation of such memories to support navigation. However, recently an accumulation of disparate observations has prompted a rethinking of the avian HF as a structure also important in shaping visual-spatial perception or attention antecedent to any memory processing. In this perspective paper, we summarize field observations contrasting the behavior of intact and HF-lesioned homing pigeons from several studies, based primarily on GPS-recorded flight paths, that support a recharacterization of HF's functional profile to include visual-spatial perception. Although admittedly still speculative, we hope the offered perspective will motivate controlled, experimental-laboratory studies to further test the hypothesis of a HF important for visual-perceptual integration, or scene construction, of landscape elements in support of navigation.

A bird's eye view of the hippocampus beyond space: Behavioral, neuroanatomical, and neuroendocrine perspectives.

Although the hippocampus is one of the most-studied brain regions in mammals, research on the avian hippocampus has been more limited in scope. It is generally agreed that the hippocampus is an ancient feature of the amniote brain, and therefore homologous between the two lineages. Because birds and mammals are evolutionarily not very closely related, any shared anatomy is likely to be crucial for shared functions of their hippocampi. These functions, in turn, are likely to be essential if they have been conserved for over 300 million years. Therefore, research on the avian hippocampus can help us understand how this brain region evolved and how it has changed over evolutionary time. Further, there is a strong research foundation in birds on hippocampal-supported behaviors such as spatial navigation, food caching, and brood parasitism that scientists can build upon to better understand how hippocampal anatomy, network circuitry, endocrinology, and physiology can help control these behaviors. In this review, we summarize our current understanding of the avian hippocampus in spatial cognition as well as in regulating anxiety, approach-avoidance behavior, and stress responses. Although there are still some questions about the exact number of subdivisions in the avian hippocampus and how that might vary in different avian families, there is intriguing evidence that the avian hippocampus might have complementary functional profiles along the rostral-caudal axis similar to the dorsal-ventral axis of the rodent hippocampus, where the rostral/dorsal hippocampus is more involved in cognitive processes like spatial learning and the caudal/ventral hippocampus regulates emotional states, anxiety, and the stress response. Future research should focus on elucidating the cellular and molecular mechanisms - including endocrinological - in the avian hippocampus that underlie behaviors such as spatial navigation, spatial memory, and anxiety-related behaviors, and in so doing, resolve outstanding questions about avian hippocampal function and organization.

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.

Neuronal activation in the geomagnetic responsive region Cluster N covaries with nocturnal migratory restlessness in white-throated sparrows (Zonotrichia albicollis).

Cluster N is a region of the visual forebrain of nocturnally migrating songbirds that supports the geomagnetic compass of nocturnal migrants. Cluster N expresses immediate-early genes (ZENK), indicating neuronal activation. This neuronal activity has only been recorded at night during the migratory season. Night-to-night variation in Cluster N activity in relation to migratory behaviour has not been previously examined. We tested whether Cluster N is activated only when birds are motivated to migrate and presumably engage their magnetic compass. We measured immediate-early gene activation in Cluster N of white-throated sparrows (Zonotrichia albicollis) in three conditions: daytime, nighttime migratory restless and nighttime resting. Birds in the nighttime migratory restlessness group had significantly greater numbers of ZENK-labelled cells in Cluster N compared to both the daytime and the nighttime resting groups. Additionally, the degree of migratory restlessness was positively correlated with the number of ZENK-labelled cells in the nighttime migratory restless group. Our study adds to the number of species observed to have neural activation in Cluster N and demonstrates for the first time that immediate early gene activation in Cluster N is correlated with the amount of active migratory behaviour displayed across sampled individuals. We conclude that Cluster N is facultatively regulated by the motivation to migrate, together with nocturnal activity, rather than obligatorily active during the migration season.

Neuronal circuits within the homing pigeon hippocampal formation.

The current study aimed to reveal in detail patterns of intrahippocampal connectivity in homing pigeons (Columba livia). In light of recent physiological evidence suggesting differences between dorsomedial and ventrolateral hippocampal regions and a hitherto unknown laminar organization along the transverse axis, we also aimed to gain a higher-resolution understanding of the proposed pathway segregation. Both in vivo and high-resolution in vitro tracing techniques were employed and revealed a complex connectivity pattern along the subdivisions of the avian hippocampus. We uncovered connectivity pathways along the transverse axis that started in the dorsolateral hippocampus and continued to the dorsomedial subdivision, from where information was relayed to the triangular region either directly or indirectly via the V-shaped layers. The often-reciprocal connectivity along these subdivisions displayed an intriguing topographical arrangement such that two parallel pathways could be discerned along the ventrolateral (deep) and dorsomedial (superficial) aspects of the avian hippocampus. The segregation along the transverse axis was further supported by expression patterns of the glial fibrillary acidic protein and calbindin. Moreover, we found strong expression of Ca2+ /calmodulin-dependent kinase IIα and doublecortin in the lateral but not medial V-shape layer, indicating a difference between the two V-shaped layers. Overall, our findings provide an unprecedented, detailed description of avian intrahippocampal pathway connectivity, and confirm the recently proposed segregation of the avian hippocampus along the transverse axis. We also provide further support for the hypothesized homology of the lateral V-shape layer and the dorsomedial hippocampus with the dentate gyrus and Ammon's horn of mammals, respectively.

Comparative biology of spatial navigation in three arachnid orders (Amblypygi, Araneae, and Scorpiones).

From both comparative biology and translational research perspectives, there is escalating interest in understanding how animals navigate their environments. Considerable work is being directed towards understanding the sensory transduction and neural processing of environmental stimuli that guide animals to, for example, food and shelter. While much has been learned about the spatial orientation behavior, sensory cues, and neurophysiology of champion navigators such as bees and ants, many other, often overlooked animal species possess extraordinary sensory and spatial capabilities that can broaden our understanding of the behavioral and neural mechanisms of animal navigation. For example, arachnids are predators that often return to retreats after hunting excursions. Many of these arachnid central-place foragers are large and highly conducive to scientific investigation. In this review we highlight research on three orders within the Class Arachnida: Amblypygi (whip spiders), Araneae (spiders), and Scorpiones (scorpions). For each, we describe (I) their natural history and spatial navigation, (II) how they sense the world, (III) what information they use to navigate, and (IV) how they process information for navigation. We discuss similarities and differences among the groups and highlight potential avenues for future research.

Deconstructing the flight paths of hippocampal-lesioned homing pigeons as they navigate near home offers insight into spatial perception and memory without a hippocampus.

The aim of this study was to exploit detailed analyses of GPS-recorded tracks to better characterise the impact of hippocampal (HF) lesion on spatial memory and perception in the context of homing pigeon navigation when reliant on familiar landscape features near the home loft following repeated releases from the same three locations. As reported previously, following HF lesion, a low spatio-temporal resolution analysis revealed that homing pigeons fly less direct paths home once near the loft. We now further show that 1) HF-lesioned pigeons are less likely to display fidelity to a particular flight path home when released from the same locations multiple times, 2) intact pigeons are more likely to exploit leading-line landscape features, e.g., a road or the border of a woodlot, in developing flight-path fidelity and 3) even when flying a straight path HF-lesioned homing pigeons are more likely to display relatively rapid, oscillatory heading changes as if casting about for sensory, presumably visual information. The flight behaviour differences between the intact and HF-lesioned pigeons persisted across the four releases from the three locations, although the differences became smaller with increasing experience. Taken together, the GPS-track data offer a detailed characterisation of the effects of HF lesion on landscape-based, homing pigeon navigation, offering new insight into the role of the hippocampal formation in supporting memory-related, e.g., fidelity to a familiar route home, and perhaps perceptual-related, e.g., oscillating headings, navigational processes.

The medial pallium and the spatial encoding of geometric and visual cues in the terrestrial toad, Rhinella arenarum.

The medial pallium (MP) of amphibians is the homologue of the mammalian hippocampus, and previous research has implicated MP for locating a using the boundary geometry of an environment. MP-lesioned, sham-operated and intact control terrestrial toads, Rhinella arenarum, were trained to locate a goal in a rectangular arena with a visual feature cue placed on one of the short walls. Whereas the sham-operated and intact subjects successfully learned to locate the goal, the MP-lesioned toads showed no evidence of learning. The data support the hypothesis that the amphibian MP is involved when the boundary geometry of an environment is used to locate a goal, which is consistent with evidence from other vertebrate groups. Curious, however, is that the MP lesions also resulted in the toads' inability to locate the goal based on the visual feature cue. This result supports previous research and suggests that, in contrast to the hippocampal homologue of amniotes, the amphibian medial pallium plays a broader role in spatial learning processes.

Exploring Higher-Order Conceptual Learning in an Arthropod with a Large Multisensory Processing Center.

Comparative cognition aims to understand the evolutionary history and current function of cognitive abilities in a variety of species with diverse natural histories. One characteristic often attributed to higher cognitive abilities is higher-order conceptual learning, such as the ability to learn concepts independent of stimuli-e.g., 'same' or 'different'. Conceptual learning has been documented in honeybees and a number of vertebrates. Amblypygids, nocturnal enigmatic arachnids, are good candidates for higher-order learning because they are excellent associational learners, exceptional navigators, and they have large, highly folded mushroom bodies, which are brain regions known to be involved in learning and memory in insects. In Experiment 1, we investigate if the amblypygid Phrynus marginimaculatus can learn the concept of same with a delayed odor matching task. In Experiment 2, we test if Paraphrynus laevifrons can learn same/different with delayed tactile matching and nonmatching tasks before testing if they can transfer this learning to a novel cross-modal odor stimulus. Our data provide no evidence of conceptual learning in amblypygids, but more solid conclusions will require the use of alternative experimental designs to ensure our negative results are not simply a consequence of the designs we employed.

Space, feature, and risk sensitivity in homing pigeons (Columba livia): Broadening the conversation on the role of the avian hippocampus in memory.

David Sherry has been a pioneer in investigating the avian hippocampal formation (HF) and spatial memory. Following on his work and observations that HF is sensitive to the occurrence of reward (food), we were interested in carrying out an exploratory study to investigate possible HF involvement in the representation goal value and risk. Control sham-lesioned and hippocampal-lesioned pigeons were trained in an open field to locate one food bowl containing a constant two food pellets on all trials, and two variable bowls with one containing five pellets on 75% (High Variable) and another on 25% (Low Variable) of their respective trials (High-Variable and Low-Variable bowls were never presented together). One pairing of pigeons learned bowl locations (space); another bowl colors (feature). Trained to color, hippocampal-lesioned pigeons performed as rational agents in their bowl choices and were indistinguishable from the control pigeons, a result consistent with HF regarded as unimportant for non-spatial memory. By contrast, when trained to location, hippocampal-lesioned pigeons differed from the control pigeons. They made more first-choice errors to bowls that never contained food, consistent with a role of HF in spatial memory. Intriguingly, the hippocampal-lesioned pigeons also made fewer first choices to both variable bowls, suggesting that hippocampal lesions resulted in the pigeons becoming more risk averse. Acknowledging that the results are preliminary and further research is needed, the data nonetheless support the general hypothesis that HF-dependent memory representations of space capture properties of reward value and risk, properties that contribute to decision making when confronted with a choice.

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.

GPS-profiling of retrograde navigational impairments associated with hippocampal lesion in homing pigeons.

The avian hippocampal formation (HF) is homologous to the mammalian hippocampus and plays a central role in the control of spatial cognition. In homing pigeons, HF supports navigation by familiar landmarks and landscape features. However, what has remained relatively unexplored is the importance of HF for the retention of previously acquired spatial information. For example, to date, no systematic GPS-tracking studies on the retention of HF-dependent navigational memory in homing pigeons have been performed. Therefore, the current study was designed to compare the pre- and post-surgical navigational performance of sham-lesioned control and HF-lesioned pigeons tracked from three different sites located in different directions with respect to home. The pre- and post-surgical comparison of the pigeons' flight paths near the release sites and before reaching the area surrounding the home loft (4 km radius from the loft) revealed that the control and HF-lesioned pigeons displayed similarly successful retention. By contrast, the HF-lesioned pigeons displayed dramatically and consistently impaired retention in navigating to their home loft during the terminal phase of the homing flight near home, i.e., where navigation is supported by memory for landmark and landscape features. The data demonstrate that HF lesions lead to a dramatic loss of pre-surgically acquired landmark and landscape navigational information while sparing those mechanisms associated with navigation from locations distant from home.

Multisensory integration supports configural learning of a home refuge in the whip spider Phrynus marginemaculatus.

Whip spiders (Amblypygi) reside in structurally complex habitats and are nocturnally active yet display notable navigational abilities. From the theory that uncertainty in sensory inputs should promote multisensory representations to guide behavior, we hypothesized that their navigation is supported by a multisensory and perhaps configural representation of navigational inputs, an ability documented in a few insects and never reported in arachnids. We trained Phrynus marginemaculatus to recognize a home shelter characterized by both discriminative olfactory and tactile stimuli. In tests, subjects readily discriminated between shelters based on the paired stimuli. However, subjects failed to recognize the shelter in tests with either of the component stimuli alone. This result is consistent with the hypothesis that the terminal phase of their navigational behavior, shelter recognition, can be supported by the integration of multisensory stimuli as an enduring, configural representation. We hypothesize that multisensory learning occurs in the whip spiders' extraordinarily large mushroom bodies, which may functionally resemble the hippocampus of vertebrates.

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.