Verner P. Bingman

Mechanisms of animal global navigation: comparative perspectives and enduring challenges

Animals navigate over a range of distances, but it has been the global navigation of species migrating among spatially restricted, seasonal homes separated by thousands of kilometers that continues to defy a thorough mechanistic explanation. We survey the navigational behavior of migratory salmon, whales, sea turtles, and birds, as well as dispersing monarch butterflies, to promote the idea that an explicitly comparative approach to global navigation can provide insight into the evolution and properties of navigational mechanisms. The navigational abilities of migrant birds and sea turtles are used to illustrate the concepts of true navigation and vector navigation, leading us to consider the selective forces that might shape the evolution of navigational mechanisms. We propose that different navigational mechanisms, with different scales of accuracy, are likely employed during the course of migration. Furthermore, superficially similar global migratory behavior in different taxonomic groups is likely characterized by different sensory, representational and neural mechanisms reflective of groupspecific adaptation to the physical properties of a migratory environment.

Homing behavior of hippocampus and parahippocampus lesioned pigeons following short-distance releases.

The avian hippocampal formation has been proposed to play a critical role in the neural regulation of a navigational system used by homing pigeons to locate their loft once in the familiar area near home. In support of this hypothesis, the homing performance of pigeons with target lesions of either the hippocampus or parahippocampus was found to be impaired compared to controls following releases of about 10 km. Further, radio tracking revealed that the in-flight behavior of the hippocampal lesioned homing pigeons was characterized by numerous direction changes and generally poor orientation with respect to the home loft. The results identify a local navigational impairment on the part of the hippocampal lesioned pigeons in the vicinity of the loft where landmark cues are thought to be important. Additionally, target lesions of the hippocampus or parahippocampus were found to be similarly effective in causing homing deficits.

Large-scale network organization in the avian forebrain: a connectivity matrix and theoretical analysis

Many species of birds, including pigeons, possess demonstrable cognitive capacities, and some are capable of cognitive feats matching those of apes. Since mammalian cortex is laminar while the avian telencephalon is nucleated, it is natural to ask whether the brains of these two cognitively capable taxa, despite their apparent anatomical dissimilarities, might exhibit common principles of organization on some level. Complementing recent investigations of macro-scale brain connectivity in mammals, including humans and macaques, we here present the first large-scale “wiring diagram” for the forebrain of a bird. Using graph theory, we show that the pigeon telencephalon is organized along similar lines to that of a mammal. Both are modular, small-world networks with a connective core of hub nodes that includes prefrontal-like and hippocampal structures. These hub nodes are, topologically speaking, the most central regions of the pigeons brain, as well as being the most richly connected, implying a crucial role in information flow. Overall, our analysis suggests that indeed, despite the absence of cortical layers and close to 300 million years of separate evolution, the connectivity of the avian brain conforms to the same organizational principles as the mammalian brain.

The Development of Orientation and Navigation Behavior in Birds

The complex mechanisms of orientation and navigation in birds develop through the interaction of experience with the relevant stimuli and the underlying genetic substrate. Many migratory species show site fidelity, homing to previously occupied breeding and overwintering localities. The ability to do this requires experience at the site and involves a process like imprinting that seems to take place at least twice during a birds first year of life. On the first migration, birds fly directions and distances that are apparently genetically programmed and are sufficient to bring them within the winter range of their population. Little else is known concerning the genetic basis of orientation behavior. The sun, stars, and earths magnetic field provide compasses for migratory and homing orientation. The ontogeny of each sort of compass involves experience-dependent modification during at least the first few months of a birds life. The sun compass is learned by observation of the suns arc in concert with the birds biological clock. There is some evidence that the magnetic field may also be involved in calibrating the sun compass of the homing pigeon. The star compass is established through visual observation of the axis of stellar rotation during the birds first summer. The pole point is defined as north, but the biological basis of this rule is unknown. The sensory basis of the magnetic compass is also unknown, but it is subject to modification by visual cues, probably stars. In this article we discuss the varying degrees of plasticity in the ontogeny of these mechanisms within the evolutionary context of the spatial and temporal variability of the relevant orientation cues. There appears to be a trend in which information flows from more reliable to les reliable cue-systems during development. In addition to a compass, goal-directed orientation, or navigation, requires some means of assesing location relative to the goal. Homing pigeons apparently utilize sensory information acquired during the displacement journey in this context, but such input does not seem to be necessary. The ability to navigate using only those cues available at the release point is thought to be based on a map of some sort. The bases of this map remain controversial: current investigations are focused on odors and magnetic gradients, but these are not mutually exclusive possibilities, nor are they the only ones. In both of the above cases, there is evidence of experiential effects, and we believe that an ontogenetic approach may elucidate the essentials of these mechanisms. Studies of the ontogeny of bird navigation are also likely reveal important things about the development of behavior in general.

Hippocampal formation is required for geometric navigation in pigeons.

The geometric properties of bounded space have attracted considerable attention as a source of spatial information that can guide goal navigation. Although the use of geometric information to navigate has been observed in every species studied to date, the neural mechanisms that support the representation of geometric information are still debated. With the purpose of investigating this topic, we trained pigeons with lesion to the hippocampal formation to search for food in a rectangular‐shaped arena containing one wall of a different color that served as the only distinctive environmental feature. Although lesioned pigeons learned the task even faster than control animals, probe trials showed that they were insensitive to geometric information. Control animals could encode and use both geometric and feature information to locate the goal. By contrast, lesioned pigeons relied exclusively on the feature information provided by the wall of a different color. The results indicate that the avian hippocampal formation is critical for learning the geometric properties of space in homing pigeons.

Sun compass-based spatial learning impaired in homing pigeons with hippocampal lesions

The hippocampal formation is known to be critical for spatial cognition, for example, regulating the learning of environmental maps. But how is a spatial map learned, and what is the role of the hippocampal formation in the learning process? The sun compass is perhaps the most ubiquitous, naturally occurring spatial orientation mechanism found in the animal kingdom. The sun compass may also serve as a directional reference that supports spatial learning. We report that homing pigeons with hippocampal lesions were unable to use the sun compass to learn the directional location of food in an outdoor, experimental arena. Homing pigeons with lesions of the caudal neostriatum readily learned the same task, and showed appropriately shifted directional responses following a clock-shift manipulation demonstrating that they were indeed using the sun compass to learn the task. Finally, both hippocampal and control lesioned birds quickly learned a procedurally similar task where a color cue identified the location of food in the same experimental arena. The results indicate that hippocampal lesions impair sun compass use in the context of learning. As such, the results support the hypothesis that the importance of the hippocampal formation in spatial cognition may be related to its participation in a neural process in which information from a directional reference, in this case the sun compass, is used to learn the directional relationship among stimuli in space.

The Avian Hippocampus, Homing in Pigeons and the Memory Representation of Large-Scale Space

Abstract The extraordinary navigational ability of homing pigeons provides a unique spatial cognitive system to investigate how the brain is able to represent past experiences as memory. In this paper, we first summarize a large body of lesion data in an attempt to characterize the role of the avian hippocampal formation (HF) in homing. What emerges from this analysis is the critical importance of HF for the learning of map-like, spatial representations of environmental stimuli used for navigation. We then explore some interesting properties of the homing pigeon HF, using for discussion the notion that the homing pigeon HF likely displays some anatomical or physiological specialization(s), compared to the laboratory rat, that account for its participation in homing and the representation of large-scale, environmental space. Discussed are the internal connectivity among HF subdivisions, the occurrence of neurogenesis, the presence of rhythmic theta activity and the electrophysiological profile of HF neurons. Comparing the characteristics of the homing pigeon HF with the hippocampus of the laboratory rat, two opposing perspectives can be supported. On the one hand, one could emphasize the subtle differences in the properties of the homing pigeon HF as possible departure points for exploring how the homing pigeon HF may be adapted for homing and the representation of large-scale space. Alternatively, one could emphasize the similarities with the rat hippocampus and suggest that, if homing pigeons represent space in a way different from rats, then the neural specializations that would account for the difference must lie outside HF. Only future research will determine which of these two perspectives offers a better approximation of the truth.

The Homing Pigeon Hippocampus and Space: In Search of Adaptive Specialization

The hippocampus (HF) of birds and mammals is essential for the map-like representation of environmental landmarks used for navigation. However, species with contrasting spatial behaviors and evolutionary histories are likely to display differences, or ‘adaptive specializations’, in HF organization reflective of those contrasts. In the search for HF specialization in homing pigeons, we are investigating the spatial response properties of isolated HF neurons and possible right-left HF differences in the representation of space. The most notable result from the recording work is that we have yet to find neurons in the homing pigeon HF that display spatial response properties similar to HF ‘place cells’ of rats. Of interest is the suggestion of neurons that show higher levels of activity when pigeons are near goal locations and neurons that show higher levels of activity when pigeons are in a holding area prior to be being placed in an experimental environment. In contrast to the rat, the homing pigeon HF appears to be functionally lateralized. Results from a current lesion study demonstrate that only the left HF is sensitive to landmarks that are located within the boundaries of an experimental environment, whereas the right HF is indifferent to such landmarks but sensitive to global environmental features (e.g., geometry) of the experimental space. The preliminary electrophysiological and lateralization results offer interesting departure points for better understanding possible HF specialization in homing pigeons. However, the pigeon and rat HF reside in different forebrain environments characterized by a wulst and neocortex, respectively. Differences in the forebrain organization of pigeons and rats, and birds and mammals in general, must be considered in making sense of possible species differences in how HF participates in the representation of space.

Dissociation of place and cue learning by telencephalic ablation in goldfish.

This study examined the spatial strategies used by goldfish (Carassius auratus) to find a goal in a 4-arm maze and the involvement of the telencephalon in this spatial learning. Intact and telencephalon-ablated goldfish were trained to find food in an arm placed in a constant room location and signaled by a local visual cue (mixed place-cue procedure). Both groups learned the task, but they used different learning strategies. Telencephalon-ablated goldfish learned the task more quickly and made fewer errors to criterion than controls. Probe trials revealed that intact goldfish could use either a place or a cue strategy, whereas telencephalon-ablated goldfish learned only a cue strategy. The results offer additional evidence that place and cue learning in fish are subserved by different neural substrates and that the telencephalon of the teleost fish, or some unspecified structure within it, is important for spatial learning and memory in a manner similar to the hippocampus of mammals and birds.

Telencephalic afferents to the caudolateral neostriatum of the pigeon

The pigeon caudolateral neostriatum (NCL) shares a dopaminergic innervation with mammalian frontal cortical areas and is implicated in the regulation of avian cognitive behavior. Retrograde tracing methods were used to identify forebrain projections to NCL and to suggest a possible role of this area in mediating spatial behavior. NCL receives telencephalic projections from the hyperstriatum accessorium, cells along the border of hyperstriatum dorsale and hyperstriatum ventrale, anterolateral hyperstriatum adjacent to the vallecula, confined cell groups within the anterior neostriatum, and subdivisions of the archistriatum. In addition, labeling of a small number of large cells near the fasciculus prosencephali lateralis was observed at the level of the anterior commissure. In accordance with previous studies, projections of subtelencephalic areas were revealed to originate from the thalamic posterior dorsolateral nucleus and nucleus subrotundus, as well as from the tegmental nucleus pedunculopontinus and locus coeruleus. Forebrain connections of NCL show that somatosensory, visual, and olfactory information can combine in this division of the neostriatum. NCL is therefore suited to participate in a neural circuit that regulates spatial behavior. Moreover, the present study reveals that NCL is reached by a limbic projection from the nucleus taeniae. This projection also suggests similarity between NCL and mammalian frontal cortical areas.