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 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.

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.

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.

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.

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.

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.

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.

On the transfer of spatial learning between geometrically different shaped environments in the terrestrial toad, Rhinella arenarum.

When trained in a rectangular arena, some research has suggested that rats are guided by local features rather than overall boundary geometry. We explored this hypothesis using the terrestrial toad, Rhinella arenarum, as a comparative contrast. In two experiments, toads were trained to find a water-reward goal location in either a featureless rectangular arena (Experiment 1) or in a rectangular arena with a removable colored feature panel covering one short wall (Experiment 2). After learning to successfully locate the water reward, probe trials were carried out by changing the shape of the arena into a kite form with two 90°-angled corners, and in the case of Experiment 2, also shifting the location of the color panel. The results of Experiment 1 indicated that the toads, in contrast to rats, relied primarily on overall shape or boundary geometry to encode the location of a goal. Under the probe conditions of the altered environmental geometry in Experiment 2, the toads seemed to preferentially choose a corner that was generally correct relative to the feature panel experienced during training. Together, the data of the current study suggest that toads and rats differ in the strategies they employ to represent spatial information available in a rectangular arena. Further, the results support the hypothesis that amphibians and mammals engage different neural mechanisms, perhaps related to different evolutionary selective pressures, for the representation of environmental geometry used for navigation.

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.

The Mating Call of the Terrestrial Toad, Rhinella arenarum, as a Cue for Spatial Orientation and Its Associated Brain Activity.

Acoustic communication is essential for reproduction and predator avoidance in many anuran species. For example, mating calls are generally produced by males and represent a conspicuous communication signal employed during the breeding season. Although anuran mating calls have been largely studied to analyze content and phonotaxis toward choruses, they are rarely discussed as sources of information guiding spatial behavior in broader contexts. This is striking if we consider that previous studies have shown anurans to be impressive navigators. In the current study, we investigated whether terrestrial toad (Rhinella arenarum) males can use a mating call as a spatial cue to locate a water reward in a laboratory maze. Male toads could indeed learn the location of a reward guided by a mating call. This navigational ability, as indicated by c-Fos, was associated with greater neuronal activity in the telencephalic hippocampal formation (HF; also referred to in amphibians as medial pallium), the medial septum (MS), and the central amygdala (CeA). HF and MS are telencephalic structures associated with spatial navigation in mammals and other vertebrates. The CeA, by contrast, has been studied in the context of acoustic processing and communication in other amphibian species. The results are discussed in the framework of an evolutionary conserved, HF-septal spatial-cognitive network shared by amphibians and mammals.

Requiem for a heavyweight - can anything more be learned from homing pigeons about the sensory and spatial-representational basis of avian navigation?

The homing pigeon (Columba livia) has long served as a study species to exhaustively investigate the sensory and spatial (map)-representational mechanisms that guide avian navigation. However, several factors have contributed to recent questioning of whether homing pigeons are as valuable as they once were as a general model for the study of the sensory and map-like, spatial-representational mechanisms of avian navigation. These reservations include: the success of this research program in unveiling navigational mechanisms; the burgeoning of new tracking technologies making navigational experiments on long-distance migratory and other wild birds much more accessible; the almost complete loss of the historically dominant, large-scale pigeon loft/research facilities; and prohibitive university per diem costs as well as animal care and use restrictions. Nevertheless, I propose here that there remain good prospects for homing pigeon research that could still profoundly influence how one understands aspects of avian navigation beyond sensory mechanisms and spatial-representational strategies. Indeed, research into neural mechanisms and brain organization, social/personality influences and genetics of navigation all offer opportunities to take advantage of the rich spatial behavior repertoire and experimental convenience of homing pigeons. Importantly, research in these areas would not necessarily require the large number of birds typically used in the past to study the sensory guidance of navigation. For those of us who have had the opportunity to work with this remarkable animal, one research door may be closing, but a window into exciting future opportunities lies ajar.

The avian hippocampus and the hypothetical maps used by navigating migratory birds (with some reflection on compasses and migratory restlessness).

The homology between the avian hippocampal formation (HF) and mammalian hippocampus nurtures the expectation that HF plays a fundamental role in navigation by migratory birds. Indeed, HF of migratory birds displays anatomical properties that differ from non-migratory species. Using a hypothetical framework of multiple maps of differing spatial resolution and range, homing pigeon data suggest that HF is important for navigating by landscape features near familiar breeding, over-wintering, and stop-over sites. By contrast, HF would be unimportant for an olfactory navigational map, which could be operational over unfamiliar space farther away from a goal location, nor is there any evidence for HF involvement in the sun or geomagnetic compass. The most intriguing question that remains open is what role HF may play in navigation when a migrant is thousands kms away from a familiar area, where homing pigeon data are uninformative and a geomagnetic map may be operational. Beyond navigation, successful migration depends on seasonal timing and often becoming nocturnally active. There is little evidence that HF plays a role in the timing of circannual and circadian cycles. Rather, circadian pacemakers including the pineal gland may control circadian timing of nocturnal restlessness and photoperiodic seasonal pacemakers likely control circannual expression.

Development of site fidelity in the nocturnal amblypygid, Phrynus marginemaculatus.

Amblypygids are capable of navigation in the complex terrain of rainforests in near complete darkness. Path integration is unnecessary for successful homing, and the alternative mechanisms by which they navigate have yet to be elucidated. Here, our aims were to determine whether the amblypygid Phrynus marginemaculatus could be trained to reliably return to a target shelter in a laboratory arena-indicating goal recognition-and to document changes in behavior associated with the development of fidelity. We recorded nocturnal movements and space use by individuals over five nights in an arena in which subjects were provided with two shelters that differed in quality. The target shelter, unlike the alternative shelter, shielded subjects from light in daylight hours. Individuals consistently exited and returned to a shelter each night and from the third night onward chose the target shelter more often than the alternative shelter. Indeed, on the fifth night, every subject chose the target shelter. This transition was associated with changes in movement and space use in the arena. Notably, the movement features of outbound and inbound paths differed but did not change across nights. Individuals were also characterized by distinct behavioral strategies reflecting candidate homing mechanisms.

Importance of the antenniform legs, but not vision, for homing by the neotropical whip spider Paraphrynus laevifrons.

Amblypygids, or whip spiders, are nocturnal, predatory arthropods that display a robust ability to navigate to their home refuge. Prior field observations and displacement studies in amblypygids demonstrated an ability to home from distances as far away as 10 m. In the current study, micro-transmitters were used to take morning position fixes of individual Paraphrynus laevifrons following an experimental displacement of 10 m from their home refuge. The intention was to assess the relative importance of vision compared with sensory input acquired from the antenniform legs for navigation as well as other aspects of their spatial behavior. Displaced individuals were randomly assigned to three treatment groups: (i) control individuals; (ii) vision-deprived individuals, VD; and (iii) individuals with sensory input from the tips of their antenniform legs compromised, AD. Control and VD subjects were generally successful in returning home, and the direction of their movement on the first night following displacement was homeward oriented. By contrast, AD subjects experienced a complete loss of navigational ability, and movement on the first night indicated no hint of homeward orientation. The data strongly support the hypothesis that sensory input from the tips of the antenniform legs is necessary for successful homing in amblypygids following displacement to an unfamiliar location, and we hypothesize an essential role of olfaction for this navigational ability.

Reflections on the Structural-Functional Evolution of the Hippocampus: What Is the Big Deal about a Dentate Gyrus?

The vertebrate hippocampal formation has been central in discussions of comparative cognition, nurturing an interest in understanding the evolution of variation in hippocampal organization among vertebrate taxa and the functional consequences of that variation. Assuming some similarity between the medial pallium of extant amphibians and the hippocampus of stem tetrapods, we propose the hypothesis that the hippocampus of modern amniotes began with a medial pallium characterized by a relatively undifferentiated cytoarchitecture, more direct thalamic and olfactory sensory inputs, and a broad role in associative learning and memory processes that nonetheless included the map-like representation of space. From this modest beginning evolved the cognitively more specialized hippocampal formation of birds and the hippocampus of mammals with its confounding dentate gyrus. Much has been made of trying to identify a dentate homologue in birds, but there are compelling reasons to believe no such structural homologue/functional equivalent exists. The uniqueness of the mammalian dentate then raises the question of what might be the functional consequences of a hippocampus with a dentate compared to one without. One might be tempted to speculate that the presence of a dentate gyrus facilitates so-called pattern separation, but birds with their suspected dentate-less hippocampus display excellent hippocampal-dependent pattern separation relying on space. Perhaps one consequence of a dentate is a hippocampus better designed to process a broader array of stimuli beyond space to more robustly support episodic memory. What is clear is that any meaningful reconstruction of hippocampal evolution and the eventual identification of any subdivisional homologies will require more data on the neurobiological and functional properties of the nonmammalian hippocampus, particularly those of amphibians and reptiles.

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.

Network structure of functional hippocampal lateralization in birds.

Functional hemispheric asymmetry is a common feature of vertebrate brain organization, yet little is known about how hemispheric dominance is implemented at the neural level. One notable example of hemispheric dominance in birds is the leading role of the left hippocampal formation in controlling navigational processes that support homing in pigeons. Relying on resting state fMRI analyses (where Functional connectivity (FC) can be determined by placing a reference 'seed' for connectivity in one hemisphere), we show that following seeding in either an anterior or posterior region of the hippocampal formation of homing pigeons and starlings, the emergent FC maps are consistently larger following seeding of the left hippocampus. Left seedings are also more likely to result in FC maps that extend to the contralateral hippocampus and outside the boundaries of the hippocampus. The data support the hypothesis that broader FC is one neural-organizational property that confers, with respect to navigation, functional dominance to the left hippocampus of birds.