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V P Bingman

Publications and source records attributed to V P Bingman.

At least 19 recordsLinked to original sources

The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period.

Homing pigeons can learn a navigational map by relying on the heterogeneous distribution of atmospheric odours in the environment. To test whether there might be a sensitive period for learning an olfactory-based navigational map, we maintained a group of young pigeons in an aviary screened from the winds until the age of three to four months post-fledging. Subsequently, the screens were removed and the pigeons were exposed to the winds and the environmental odours they carry for three months. One control group of pigeons was held in a similar aviary but exposed to the winds immediately upon Hedging, while another control group of pigeons was allowed free-flight. When the pigeons from the three groups were released from two distant release sites at about six months of age post-fledging, the two control groups were found to be equally good at orientating and returning home, while the experimental pigeons held in the shielded aviary for the first three months post-fledging were unable to orientate homeward and they were generally unsuccessful in returning home. This result supports the hypothesis that environmental experience during the first three months post-fledging is critical for some aspect of navigational map learning and that navigational map learning displays sensitive period-like properties.

Animals↗

Hippocampus and homing in pigeons: left and right hemispheric differences in navigational map learning.

One-month-old, inexperienced homing pigeons, prior to any opportunity to learn a navigational map, were subjected to either right or left unilateral ablation of the hippocampal formation (HF). These pigeons were then held together with a group of age-matched control birds in an outdoor aviary, where they were kept for about 3 months with the opportunity to learn a navigational map. When subsequently tested for navigational map learning at about 4 months of age posthatching, control and right HF-ablated pigeons were equally good at orienting homeward from distant, unfamiliar locations, indicating successful navigational map learning. By contrast, left HF-ablated pigeons were impaired in orienting homeward, indicating a failure to learn a navigational map. Interestingly, both right and left HF-ablated pigeons displayed impaired homing performance relative to controls. These results suggest that different aspects of homing pigeon navigation may be lateralized to different hemispheres, and in particular, the HF of the different hemispheres. The left HF appears critical for navigational map learning, i.e. determining an approximate direction home from distant, unfamiliar locations. The right HF, and possibly the left HF as well, appear to play an important role in local navigation near the loft, which is likely based on familiar landmarks.

Animals↗

Further experiments on the relationship between hippocampus and orientation following phase-shift in homing pigeons.

Following a clock- or phase-shift of the light dark cycle, hippocampal lesioned pigeons (Columba livia) consistently display a larger deviation in vanishing bearings away from the homeward direction compared to intact birds; an effect never seen in unshifted birds. In Experiment 1, control and hippocampal lesioned pigeons oriented similarly after being held 1 week under artificial lighting in the absence of a phase-shift. Housing under artificial light by itself does not result in between group orientation differences. In Experiment 2, control and hippocampal lesioned pigeons oriented equally well under overcast conditions, indicating that both groups had a functional magnetic compass. The between group difference in orientation following phase-shift does not appear to be a consequence of control birds being able to use both the sun and earth's magnetic field for orientation and the hippocampal lesioned pigeons only being able to use the sun. In Experiment 3, lengthening the time held under 6-h clock-shift from 1 to 2 weeks had no effect on the magnitude of the difference in orientation, but fast shifting produced clearer effects than slow shifting. Taken together, the data suggest that hippocampal lesions alter how a pigeon responds to a rapidly changing light-dark cycle, particularly following a fast-shift manipulation, suggesting an as yet unspecified relationship between the avian hippocampus and the circadian rhythm(s) that regulate sun compass orientation.

Animals↗

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.

Animals↗

Hippocampal participation in navigational map learning in young homing pigeons is dependent on training experience.

The homing pigeon navigational map is perhaps one of the most striking examples of a naturally occurring spatial representation of the environment used to guide navigation. In a previous study, it was found that hippocampal lesions thoroughly disrupt the ability of young homing pigeons held in an outdoor aviary to learn a navigational map. However, since that study an accumulation of anecdotal data has hinted that hippocampal-lesioned young pigeons allowed to fly during their first summer could learn a navigational map. In the present study, young control and hippocampal-lesioned homing pigeons were either held in an outdoor aviary or allowed to fly during the time of navigational map learning. At the end of their first summer, the birds were experimentally released to test for navigational map learning. Independent of training experience, control pigeons oriented homeward during the experimental releases demonstrating that they learned a navigational map. Surprisingly, while the aviary-held hippocampal-lesioned pigeons failed to learn a navigational map as reported previously, hippocampal-lesioned birds allowed flight experience learned a navigational map indistinguishable from the two control groups. A subsequent experiment revealed that the navigational map learned by the three groups was based on atmospheric odours. The results demonstrate that hippocampal participation in navigational map learning depends on the type of experience a young bird pigeon has, and presumably, the type of navigational map learned.

Animals↗

Partial experience with the arc of the sun is sufficient for all-day sun compass orientation in homing pigeons, Columba livia.

The ability of animals to learn to use the sun for orientation has been explored in numerous species. In birds, there is conflicting evidence about the experience needed for sun compass orientation to develop. The prevailing hypothesis is that birds need entire daytime exposure to the arc of the sun to use the sun as an orientation cue. However, there is also some evidence indicating that, even with limited exposure to the arc of the sun, birds, like insects, can use the sun to orient at any time of day. We re-examine this issue in a study of compass orientation in a cue-controlled arena. Two groups of young homing pigeons received different exposure to the sun. The control group experienced the sun throughout the day; the experimental group experienced only the apparent descent of the sun. After 8 weeks of sun exposure, we trained both groups in the afternoon to find food in a specific compass direction in an outdoor arena that provided a view of the sun but not landmarks. We then tested the pigeons in the morning for their ability to use the morning sun as an orientation cue. The control group and the experimental group, which was exposed to the morning sun for the first time, succeeded in orienting in the training direction during test 1. The orientation of the experimental group was no different from that of the control group, although the experimental first trial directional response latencies were greater than the control latencies. Subsequently, we continued training both groups in the afternoon and then tested the pigeons during the morning under complete cloud cover. Both groups displayed random directional responses under cloud cover, indicating that the observed orientation was based on the visibility of the sun. The data indicate that pigeons with limited exposure to the arc of the sun can, like insects, use the sun for orientation at any time of day.

Animals↗

Reduced growth of intra- and infra-pyramidal mossy fibers is produced by continuous exposure to polychlorinated biphenyl.

Exposure to polychlorinated biphenyl (PCB) has been shown to produce cognitive deficits in both humans and laboratory animals. However, no study to date has identified long-term brain changes which could account for these problems. This study employed Timm's silver sulfide staining to visualize the hippocampal mossy fibers in Sprague-Dawley rats continuously exposed to either 125 ppm Aroclor 1254 or untreated control food beginning in utero. Reduced growth of hippocampal intra-and infra-pyramidal (II-P) mossy fibers were found in PCB treated rats compared to controls. Other measured hippocampal subdivisions remained relatively unaffected by PCB treatment, as did cortical thickness. The changes observed in hippocampal morphology in response to PCB exposure are the first to provide a potential explanation for at least part of the long-term PCB-induced cognitive deficits.

Aging↗

Neurochemical evidence for at least two regional subdivisions within the homing pigeon (Columba livia) caudolateral neostriatum.

The distributions of one neurotransmitter, two neurotransmitter-related substances, and five neuropeptides were examined within the homing pigeon caudolateral neostriatum (NCL). All eight neuroactive substances were found within a tyrosine hydroxylase (TH)-dense region that defines the NCL. Overall regional variation in the relative density of these substances suggested at least two neurochemically distinct portions of NCL. Dorsal NCL contained relatively dense staining for TH, choline acetyltransferase, and substance P, whereas vasoactive intestinal polypeptide was more abundant in ventral portions of NCL. Serotonin and cholecystokinin were found to be densest in intermediate portions of NCL. Somatostatin and leucine-enkephalin were homogeneously distributed throughout NCL. The results suggest that NCL may consist of multiple subdivisions. Investigations into the behavioral importance of these regions are necessary to clarify the role of this brain region in avian behavior.

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Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation.

When given repeated training from a location, homing pigeons acquire the ability to use familiar landmarks to navigate home. Both control and hippocampal-lesioned pigeons succeed in learning to use familiar landmarks for homing. However, the landmark representations that guide navigation are strikingly different. Control and hippocampal-lesioned pigeons were initially given repeated training flights from two locations. On subsequent test days from the two training locations, all pigeons were rendered anosmic to eliminate use of their navigational map and were phase- or clock-shifted to examine the extent to which their learned landmark representations were dependent on the use of the sun as a compass. We show that control pigeons acquire a landmark representation that allows them to directly use landmarks without reference to the sun to guide their flight home, called "pilotage". Hippocampal-lesioned birds only learn to use familiar landmarks at the training location to recall the compass direction home, based on the sun, flown during training, called "site-specific compass orientation." The results demonstrate that for navigation of 20 km or more in a natural field setting, the hippocampal formation is necessary if homing pigeons are to learn a spatial representation based on numerous independent landmark elements that can be used to directly guide their return home.

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Hippocampal lesions do not impair the geomagnetic orientation of migratory savannah sparrows.

The avian hippocampal formation is known to participate in naturally occurring spatial behavior such as homing in pigeons and cache recovery in food storing passerines, but its participation in the often spectacular migrations of birds remains uncertain. As a first investigation into the possible role of hippocampal formation in migration, the effect of hippocampal formation lesions on the geomagnetic migratory orientation of Savannah sparrows was examined. When tested indoors, hippocampal formation-lesioned sparrows were able to orient in an appropriate migratory direction indicating no necessary role for hippocampal formation in geomagnetic migratory orientation. However, hippocampal formation-lesioned birds displayed significantly less migratory (nocturnal) activity, a result that inspires further study.

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The effects of hippocampal lesions in homing pigeons on a one-trial food association task.

The role of the avian hippocampal formation in a one-trial food association task was investigated across various retention intervals. Control pigeons, lesioned controls, and pigeons with hippocampal formation lesions were allowed to find food hidden in one of four uniquely decorated bowls in a specific location in a room. After retention intervals of 10 min, 1 h, 7 h, and 24 h, pigeons were placed back in the room with the same bowl in the same location (unmanipulated trials) or with the previously rewarding bowl in a new location and a different bowl in the previously rewarding location (test trials). Although all groups chose the correct bowl during unmanipulated trials, hippocampal formation lesioned birds' choices to the bowl in the correct location decreased compared to the combined controls during the test trials. The results suggest that hippocampal formation lesions do not impair long-term memory of a goal after one experience but significantly decrease the use of spatial information to return to that goal.

Animal Feed↗

The effects of lesions to the caudolateral neostriatum on sun compass based spatial learning in homing pigeons.

To better define the role of the avian caudolateral neostriatum (NCL) in spatial behavior, we used homing pigeons to explore the effects of NCL lesions on a sun compass based spatial learning task. Although NCL lesioned birds learned the task, they required more sessions to reach criterion than controls. NCL lesioned pigeons were also able to acquire a color discrimination task that was procedurally similar to the sun compass spatial learning task, but they made more errors than controls. Both the deficits observed in sun compass based spatial learning and color discrimination were correlated with the volume of lesion damage to dorsal rather than ventral portions of NCL. Overall, these findings suggest that the role of NCL in homing pigeon navigation from distant unfamiliar locations is not related to a bird's ability to learn stimulus-direction associations using a sun compass. However NCL does appear involved in a pigeon's ability to perform at least some behaviors common to both the color discrimination and the sun compass based spatial learning tasks.

Animals↗

Paired-associate learning is unaffected by combined hippocampal and parahippocampal lesions in homing pigeons.

To examine whether the avian hippocampus-parahippocampus (HF) is necessary for nonspatial, paired-associate learning, as has been suggested for rodents, HF-lesioned and control homing pigeons were tested on a visual paired-associate learning task. Both groups learned equally well to discriminate trials that consisted of a stimulus preceded by its paired associate from trials that consisted of a stimulus preceded by stimuli from other paired associates (mispair trials), even when a mispair was experienced for the first time. The groups also learned equally well not to respond to 2 stimuli that were never rewarded. The results demonstrate that HF lesions do not impair nonspatial paired-associate learning in birds, suggesting that the role of HF in nonspatial cognition differs between birds and mammals.

Analysis of Variance↗

The homing pigeon hippocampus and the development of landmark navigation.

The role of the homing pigeon hippocampal formation was examined in the development of loft fidelity and landmark navigation. During the course of five summers, different groups of young pigeons (hippocampal-lesioned, control-lesioned, and unoperated controls) were given free flight experience followed by short distance training and experimental releases. In Experiment 1, a census of which loft each pigeon entered revealed that hippocampal lesioned pigeons displayed less loft fidelity than controls. In Experiment 2 and 3, the percent of young birds lost during their first summer of training and their first experimental release was examined. Despite displaying similarly good homeward-oriented vanishing bearings, significantly more hippocampal lesioned pigeons were lost compared to control groups. The results support the hypothesis that the homing pigeon hippocampal formation participates in the learning/operation of a spatial representation of local landmarks near the loft that can be used for loft recognition and navigation.

Animals↗

Piriform cortex ablations block navigational map learning in homing pigeons.

Young homing pigeons were subjected to ablations of the piriform cortex or left intact and allowed to learn a navigational map. Three months later, control and piriform cortex lesioned pigeons were released from three unfamiliar locations. Control pigeons oriented homeward indicating successful navigational map learning. In contrast, piriform cortex ablated pigeons consistently oriented east, took more time to return home and were more likely to get lost. The results demonstrate that piriform cortex ablations in young homing pigeons disrupt navigational learning. The data support the conclusion that participation of the piriform cortex is necessary for navigational map learning, and its role in navigational learning cannot be substituted for by other telencephalic olfactory processing regions. Further, the results show that the role of olfactory cues in building up the navigational map cannot be replaced by other non olfactory environmental stimuli.

Animals↗

Goal recognition and hippocampal formation in the homing pigeon (Columba livia).

Stimulus control of food-site recognition and role of the hippocampal formation (HF) were investigated. Control and HF-lesioned pigeons were trained to find food located in a colored bowl, near a landmark beacon, in a constant room location. During later test trials, the sources of information were individually removed and/or disassociated. For all test trial types, HF-lesioned pigeons consistently chose bowls associated with one of the training stimuli. Controls were more sensitive to the changes introduced during the test trials; choosing like HF-lesioned pigeons on some test trials but choosing randomly on others. The data identify a critical role of the avian HF in learning the spatial relationship among environmental stimuli.

Animals↗

The neuroethology of cognitive maps: contributions from research on the hippocampus and homing pigeon navigation.

The rich ethological tradition that characterizes the homing behavior of pigeons offers an excellent opportunity to examine the importance of the hippocampal formation for the regulation of spatial cognitive mechanisms. The present review summarizes both anatomical and behavioral data obtained in researches on the pigeon hippocampal formation that have been performed over the last 12 years. Pathway connection studies and investigations on the neurochemical organization of the avian hippocampal formation show that this structure shares many similarities with the mammalian hippocampus and provide the basis for structural as well as functional homology. The initial research on the role of the hippocampal formation in the homing behavior showed that this brain structure is likely to be involved in phenomena of spatial cognition. Therefore, the homing behavior of pigeons has been extensively used as an experimental model to investigate the role of the hippocampal formation in spatial cognition related to a naturally occurring behavior. These studies have revealed that the hippocampal formation plays a fundamental role in the learning of a navigational map based on atmospheric odors, but it doesn't seem to be involved in the operation of such a map. In contrast, both the learning and the operation of a navigational map based on the recognition of familiar landmarks require a functional hippocampal formation. Further investigations indicated that these functions of the hippocampal formation are mediated by its involvement in the use of the sun compass, and suggested that the hippocampal formation plays a fundamental role in a cognitive process in which the sun compass is specifically used to learn about the location of stimuli in space. The studies reviewed in the present paper have provided a considerable amount of experimental data both on the anatomical/neurochemical organization of the avian hippocampal formation and on the role played by this brain structure in spatial cognition. The future development of these researches will need to consider the contribution to hippocampal function of specific transmitter systems that are involved in hippocampal circuitry. In particular, the afferent cholinergic system and some of the peptidergic systems intrinsic to the hippocampal formation deserve particular attention in view of their possible involvement in the acquisition and/or operation of spatial cognitive abilities by homing pigeons.

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