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Verner P Bingman

Publications and source records attributed to Verner P Bingman.

At least 19 recordsLinked to original sources

Asymmetrical participation of the left and right hippocampus for representing environmental geometry in homing pigeons.

Control, right and left HF lesioned homing pigeons (Columba livia) were trained to locate a goal in one corner of a rectangular enclosure with a distinctive feature cue. Probe tests revealed that all groups were able to encode in parallel geometric (enclosure shape) and feature information, and in the absence of one of them, they could us the other to locate the goal. However, left HF lesioned pigeons learned the task at a faster rate, and when the geometric and feature information were set in conflict, they relied more on the feature cue compared to control and right HF lesioned pigeons. It was also found that pigeons, independent of group, trained to a goal adjacent to the feature cue learned the task in fewer sessions and relied more on feature information compared to pigeons trained to a goal opposite the feature cue. The latter group relied more on geometric information. The results support the hypothesis that the left HF plays a more important role in the representation of a goal location with respect to environmental shape/geometry. We further propose that the observed functional asymmetry can be explained by the lateralized properties of the pigeon tectofugal visual system.

Analysis of Variance↗

Time-space learning in homing pigeons (Columba livia): orientation to an artificial light source.

Time-space learning reflects an ability to represent in memory event-stimulus properties together with the place and time of the event; a capacity well developed in birds. Homing pigeons were trained in an indoor octagonal arena to locate one food goal in the morning and a different food goal in the late afternoon. The goals differed with respect to their angular/directional relationship to an artificial light source located outside the arena. Further, the angular difference in reward position approximated the displacement of the sun's azimuth that would occur during the same time period. The experimental birds quickly learned the task, demonstrating the apparent ease with which birds can adopt an artificial light source to discriminate among alternative spatial responses at different times of the day. However, a novel midday probe session following successful learning revealed that the light source was interpreted as a stable landmark and not as a surrogate sun that would support compass orientation. Probe sessions following a phase shift of the light-dark cycle revealed that the mechanism employed to make the temporal discrimination was prevailingly based on an endogenous circadian rhythm and not an interval timing mechanism.

Animals↗

The effects of a changing ambient magnetic field on single-unit activity in the homing pigeon hippocampus.

The central representation of geomagnetic information in the avian brain continues to challenge researchers. Although the homing pigeon hippocampal formation primarily participates in the map-like representation of landmarks, some suggestive data indicate that it may also participate in spatial behavior guided by geomagnetic information. Forty-four isolated neurons were recorded from the hippocampal formation of homing pigeons trained to shuttle between two goal locations under changing (direction and intensity, and direction only) magnetic field conditions. Of the 37 slow-firing cells sampled (<14 spikes/s), none displayed a change in firing rate at the time of magnetic field transitions or during different ambient magnetic field conditions. By contrast, three of seven fast firing cells (>17 spikes/s) clearly displayed a phasic increase in firing during at least one of the magnetic field transitions used. The results are consistent with the hypothesis that a subset of hippocampal formation neurons receives information regarding changes in the earth's magnetic field that may be used to guide behavior.

Action Potentials↗

Small-scale spatial cognition in pigeons.

Roberts and Van Veldhuizen's [Roberts, W.A., Van Veldhuizen, N., 1985. Spatial memory in pigeons on the radial maze. J. Exp. Psychol.: Anim. Behav. Proc. 11, 241-260] study on pigeons in the radial maze sparked research on landmark use by pigeons in lab-based tasks as well as variants of the radial-maze task. Pigeons perform well on open-field versions of the radial maze, with feeders scattered on the laboratory floor. Pigeons can also be trained to search precisely for buried food. The search can be based on multiple landmarks, but is sometimes controlled by just one or two landmarks, with the preferred landmarks varying across individuals. Findings are similar in landmark-based searching on a computer monitor and on a lab floor, despite many differences between the two kinds of tasks. A number of general learning principles are found in landmark-based searching, such as cue competition, generalization and peak shift, and selective attention. Pigeons also learn the geometry of the environment in which they are searching. Neurophysiological studies have implicated the hippocampal formation (HF) in avian spatial cognition, with the right hippocampus hypothesized to play a more important role in the spatial recognition of goal locations. Most recently, single-cell recording from the pigeon's hippocampal formation has revealed cells with different properties from the classic 'place' cells of rats, as well as differences in the two sides of the hippocampus.

Animals↗

A selective serotonin reuptake inhibitor reduces REM sleep in the homing pigeon.

Avian and mammalian 'rapid eye movement' sleep (REM sleep) resemble each other in several aspects. However, the question of whether REM sleep has a shared evolutionary ancestry in birds and mammals has yet to be thoroughly explored. The brain regions and neurotransmitter systems involved in the generation of mammalian REM sleep are phylogenetically ancient, and are also found in extant birds and reptiles. Several pharmacological experiments in birds indicate that similar neural substrates are involved in the regulation of avian and mammalian sleep. However, because the drugs used in these studies generally resulted in non-specific sleep loss, the neurochemical regulation of avian REM sleep in particular remains uncertain. The selective serotonin reuptake inhibitor (SSRI) zimelidine is known to reduce REM sleep in mammals. If avian REM sleep is similarly regulated by serotonin, it would be expected that an acute dose of a SSRI should also reduce avian REM sleep. To investigate a putative role of serotonin in the regulation of avian REM sleep, changes in sleep electroencephalogram (EEG) and behavior were recorded in five pigeons (Columba livia) after the administration of an acute dose of zimelidine. Our results demonstrate that the effects of zimelidine on avian REM sleep are comparable to those observed in mammals, indicating that serotonin may serve a similar function in the control of avian and mammalian REM sleep.

Animals↗

Lateralized functional components of spatial cognition in the avian hippocampal formation: evidence from single-unit recordings in freely moving homing pigeons.

Previous research has revealed that the functional components of spatial cognition are lateralized in the forebrain of birds, including the hippocampal formation (HF). To investigate how HF cells in the left and right avian brain may differentially participate in representations of space, we recorded single-units from the HF of homing pigeons as they ran a plus maze for food. The rate maps of left HF cells often displayed elongated regions of increased activity in the center of the maze and along the maze corridors, whereas right HF cells tended to display patches at the ends of maze arms at/near goal locations. Left HF cells displayed a higher degree of spatial-specificity compared with right HF cells, including higher patch-specificity, higher reliability, and a higher incidence of location-correlated activity. Analysis of speed-correlated and trajectory-dependent activity also revealed significant HF-lateralized differences. Right HF cells tended to display significant negative correlations between spike rate and speed, although speed-dependent rate maps indicate that this relationship did not explain their space-specific activity. Left HF cells displayed a significantly higher incidence of trajectory-dependent space-specific activity than was observed in the right HF, suggesting that left HF cells may participate in navigating among goal locations. Differences in the correlates of left and right pigeon HF cells are consistent with unilateral HF-lesion data suggesting that the functional components of spatial cognition are lateralized in the avian brain, and furthermore, provide a basis for hypotheses regarding how the left and right HF support different aspects of spatial cognition.

Animals↗

Spared feature-structure discrimination but diminished salience of environmental geometry in hippocampal-lesioned homing pigeons (Columba livia).

Homing pigeons (Columba livia) were trained to locate a goal in one corner of a rectangular arena by either its shape (geometry) or the left-right configuration of colored features located in each corner (feature structure). Control and hippocampal-lesioned pigeons learned at a similar rate, but the control birds made proportionally more geometric errors during acquisition. On conflict probe trials, the control birds preferred geometrically correct corners, whereas the hippocampal-lesioned birds displayed a greater preference for the correct corner defined by feature structure. On geometry-only probe trials, both groups demonstrated an ability to identify the goal location. Hippocampal lesions do not interfere with goal recognition by the feature structure of local cues but diminish the salience of arena shape.

Animals↗

Neuronal implementation of hippocampal-mediated spatial behavior: a comparative evolutionary perspective.

The hippocampal formation (HF) of mammals and birds plays a strikingly similar role in the representation of space. This evolutionarily conserved property, however, belies the contrasting spatial ecology of animals such as rats and homing pigeons, differing spatial ecologies that should have promoted the evolution of group-specific adaptations to the HF representation of space. However, the spatial response properties of pigeon and rat HF neurons reveal surprising similarity in the contribution of position, direction, and trajectory toward explaining spatial variation in firing rate. By contrast, the asymmetrical distribution of neuronal response properties in the left and right HF of homing pigeons, but not rats, indicates a difference in network organization. The authors propose that hippocampal evolution may be characterized by inertia with respect to changes in the basic spatial elements that determine the response properties of neurons but considerable plasticity in how the neuronal response elements are organized into functional networks.

Animals↗

Representing the richness of avian spatial cognition: properties of a lateralized homing pigeon hippocampus.

Brain organization and its relationship to behavior in any extant species is a reflection of a long evolutionary history of adaptive change. Therefore, it follows that the relationship between the hippocampus and spatial cognition in any species or taxonomic group would be characterized by features adapted to its spatial ecology. Birds are the animal world's supreme navigators, and aspects of their navigational ability are dependent on the integrity of the hippocampal formation. Using the homing pigeon as a model species, we review an accumulating body of data indicating that the avian hippocampus is functionally lateralized. The spatial response properties of left hippocampal neurons, as recorded in freely moving pigeons in a laboratory environment, differ from the response properties of right hippocampal neurons. Left hippocampal lesions generally disrupt navigational behavior under field conditions more than right lesions, while right lesions are more likely to disrupt goal localization behavior under laboratory conditions. We propose that the available data are consistent with a hypothesis of a left hippocampus more involved in navigational processes, and a right hippocampus more involved in representing the locations of events. We also discuss the extent to which the observed hippocampal lateralization should be viewed as an intrinsic property of the hippocampus itself or imposed by the lateralized properties of visual inputs originating in other brain regions. Whatever the nature of the observed hippocampal lateralization, it is likely one adaptive variation in hippocampal organization that supports the extraordinary spatial behavior of birds.

Animals↗

Spatial-specificity of single-units in the hippocampal formation of freely moving homing pigeons.

The importance of space-specific single-unit activity for hippocampal formation (HF)-mediated learning and memory in rodents has been extensively studied, yet little is known about how the unit findings in rodents generalize to other vertebrate species. We report a first assessment of the space-specific single-unit activity recorded from the HF of homing pigeons as they moved through a plus maze for food reward. Rate maps of pigeon HF single-unit activity typically revealed multiple regions (2-5 per cell) of increased activity (on average, 2.5 times higher than other regions of the maze) that in 27% of slow-firing cells was reliably space-specific over time. The qualitative appearance of rate maps and the degree of spatial-specificity observed for most all pigeon HF cells suggests more modest space-specific activity than typically reported for rat hippocampal cells. The nature of space-specific activity in the pigeon HF includes (1) often transiently reliable regions of increased activity for many cells, (2) multiple patches of activity that were sometimes observed in analogous maze areas, and (3) cells displaying substantial decreases in firing rate between baseline and maze-run conditions that could not be explained by a simple relationship between firing rate and a pigeon's speed. These observations suggest that pigeon HF cells may be coding for an unspecified behavioral/motivational/environmental factors in addition to a pigeon's momentary location. The data further suggest that the spatial ecology and evolutionary history of different species may be a critical feature shaping how HF neurons capture properties of space.

Action Potentials↗

A lateralized avian hippocampus: preferential role of the left hippocampal formation in homing pigeon sun compass-based spatial learning.

The hippocampal formation (HF) plays a crucial role in amniote spatial cognition. There are also indications of functional lateralization in the contribution of the left and right HF in processes that enable birds to navigate space. The experiments described in this study were designed to examine left and right HF differences in a task of sun compass-based spatial learning in homing pigeons (Columba livia). Control, left (HFL) and right (HFR) HF lesioned pigeons were trained in an outdoor arena to locate a food reward using their sun compass in the presence or absence of alternative feature cues. Subsequent to training, the pigeons were subjected to test sessions to determine if they learned to represent the goal location with their sun compass and the relative importance of the sun compass vs. feature cues. Under all test conditions, the control pigeons demonstrated preferential use of the sun compass in locating the goal. By contrast, the HFL pigeons demonstrated no ability to locate the goal by the sun compass but an ability to use the feature cues. The behaviour of the HFR pigeons demonstrated that an intact left HF is sufficient to support sun compass-based learning, but in conflict situations and in contrast to controls, they often relied on feature cues. In conclusion, only the left HF is capable of supporting sun compass-based learning. However, preferential use of the sun compass for learning requires an intact right HF. The data support the hypothesis that the left and right HF make different but complementary contributions toward avian spatial cognition.

Animals↗

Spatial response properties of homing pigeon hippocampal neurons: correlations with goal locations, movement between goals, and environmental context in a radial-arm arena.

The amniote hippocampal formation plays an evolutionarily-conserved role in the neural representation of environmental space. However, species differences in spatial ecology nurture the expectation of species differences in how hippocampal neurons represent space. To determine the spatial response properties of homing pigeon ( Columba livia) HFneurons, we recorded from isolated units in birds freely navigating a radial arena in search of food present at four goal locations. Fifty of 76 neurons displayed firing rate variations that could be placed into three response categories. Location cells ( n=25) displayed higher firing rates at restricted locations in the arena space, often in proximity to goal locations. Path cells ( n=13) displayed higher firing rates as a pigeon moved between a subset of goal locations. Arena-off cells ( n=12) were more active when a pigeon was in a baseline holding space compared to inside the arena. Overall, reliability and coherence scores of the recorded neurons were lower compared to rat place cells. The differences in the spatial response profiles of pigeon hippocampal formation neurons, when compared to rats, provide a departure point for better understanding the relationship between spatial behavior and how hippocampal formation neurons participate in the representation of space.

Action Potentials↗

Participation of the thalamofugal visual pathway in a coarse pattern discrimination task in an open arena.

The purpose of this study was to examine the role of the thalamofugal pathway in far-field visual processing. Experiment 1 examined the role of the visual wulst and the ectostriatum in a far-field pattern discrimination task in a large open arena. Control pigeons, pigeons with ectostriatum lesions, and pigeons with wulst lesions were trained to discriminate between four patterns within the arena. Ectostriatum-lesioned pigeons were unimpaired and behaved similar to controls. By contrast, wulst-lesioned pigeons were severely impaired in the pattern discrimination task in the open arena and performed poorer than control pigeons and pigeons with ectostriatum lesions. Statistical analyses of regional contributions to the observed impairment identified the left visual wulst and bilateral hyperstriatum ventrale, which lies outside the wulst, as interesting areas. To ensure that the impairment was not due to a general learning deficit, experiment 2 involved training the pigeons in a pattern discrimination task carried out in an operant chamber, which presumably required use of near-field visual information. Wulst-lesioned pigeons were able to learn the task and performed at a level no different from control pigeons. The results of these experiments support the proposal that the wulst may be important for processing far-field information.

Animals↗

Hippocampal lesions do not disrupt navigational map retention in homing pigeons under conditions when map acquisition is hippocampal dependent.

In contrast to map-like navigation by familiar landmarks, understanding the relationship between the avian hippocampal formation (HF) and the homing pigeon navigational map has remained a challenge. With the goal of filling an empirical gap, we performed an experiment in which young homing pigeons learned a navigational map while being held in an outdoor aviary, and then half the birds were subjected to HF ablation. The question was whether HF lesion would impair retention of a navigational map learned under conditions known to require participation of HF. The pigeons, which had never flown from the aviary before, together with an additional control group that learned a navigational map with free-flight experience, were then released from two distant release sites. Contrary to expectation, the HF-lesioned birds oriented in a homeward direction in manner indistinguishable from the intact control pigeons raised in the same outdoor aviary. HF lesion did not result in a navigational map retention deficit. Together with previous results, it is now clear that regardless of the learning environment present during acquisition, HF plays no necessary role in the subsequent retention or operation of the homing pigeon navigational map.

Animals↗

Transitive behavior in hippocampal-lesioned pigeons.

The hippocampus of birds and mammals is critical for the learning of map-like memory representations of environmental space. It has been suggested that the hippocampus of rats also participates in non-spatial relational learning, including the learning of non-spatial transitive relationships among odor stimuli [Bunsey and Eichenbaum, Nature 1996]. Although transitive-like learning has been demonstrated in a variety of vertebrate species, from a comparative perspective the role of the hippocampus in this form of learning has not been tested in other amniote groups. We trained control and hippocampal-lesioned homing pigeons on a series of visual, non-spatial, go/no-go conditional discriminations and then tested them on novel transitivity probe trials. The hippocampal-lesioned pigeons were as successful as control pigeons in responding appropriately to correct and incorrect transitivity pairs. The finding that the homing pigeon hippocampal formation is not necessary for solving this serial, conditional discrimination task is important for further understanding hippocampal function across species, and represents one of the few studies that have attempted to localize a brain region responsible for the phenomenon of transitive behavior learning.

Animals↗

Lateralization of spatial learning in the avian hippocampal formation.

The authors investigated lateralization of spatial learning within the avian hippocampal formation (HF). In Experiment 1, homing pigeons (Columba livia) with unilateral lesions of the right or left HF were trained to locate a goal in a square room containing local landmarks and global room cues. All groups learned the task. During probe trials, when landmarks were rotated or removed, intact pigeons and left HF-lesioned pigeons relied exclusively on global room cues to locate the food goal. Pigeons with right HF lesions were the only group to demonstrably use the landmarks. The results suggest that the right HF is preferentially involved in the representation of global environmental space, whereas only the left HF may be sensitive to local landmarks for navigation.

Animals↗

What does a pigeon (Columba livia) brain look like during homing? selective examination of ZENK expression.

Lesion studies have shown that the avian hippocampus plays a crucial role in homing pigeon (Columba livia) navigation. Using the expression of the immediate early gene protein ZENK in intact pigeons, the authors found regional variation in hippocampal activation as a consequence of homing and, necessarily, the behavior and internal states that accompany it. Specifically, pigeons that homed displayed a significant increase in the number of ZENK-labeled cells in the lateral hippocampal formation compared with pigeons that did not home, whereas no difference was seen in the medial hippocampus. Significant changes in ZENK expression were also found in the medial striatum, which resembles the mammalian ventral striatum. The results identify portions of the hippocampal formation and the medial striatum as sites of plasticity associated with homing.

Animals↗