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    Connections of the pigeon dorsomedial forebrain studied with WGA-HRP and 3H-proline.

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    The afferent-efferent connections of the pigeon dorsomedial forebrain, which is composed of the "hippocampus" (Hp) and "parahippocampus" (APH), presumed homologues of the mammalian hippocampal complex, were studied. Afferent projections were identified by wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP) and efferent projections were identified by 3H-proline and WGA-HRP. In addition to identified intrinsic connections within Hp and APH, both Hp and APH were found to be in receipt of ipsilateral forebrain afferents from each other, the hyperstriatum accessorium, nucleus of the diagonal band, nucleus taeniae, and area corticoidea dorsolateralis. Only Hp received input from the contralateral Hp while only APH received input from the ipsilateral hyperstriatum dorsale and archistriatum, pars ventralis. Both Hp and APH received ipsilateral diencephalic afferents from the nucleus mamillaris lateralis, stratum cellulare internum, nucleus lateralis hypothalami, and nucleus paramedianus internus thalami. Only APH received bilateral input from the nucleus superficialis parvicellularis (this nucleus may send a small projection to Hp) and nucleus dorsolateralis anterior thalami, pars medialis, and an ipsilateral projection from the nucleus subrotundus. Brainstem afferents to Hp and APH included ipsilateral projections from the area ventralis (Tsai) nucleus reticularis pontis oralis, nucleus raphes, nucleus subceruleus dorsalis, and nucleus centralis superior of Bechterew, and bilateral projections from the nucleus linearis caudalis and locus ceruleus, of which the nucleus subceruleus dorsalis, nucleus centralis superior of Bechterew, and locus ceruleus projected to APH only. Forebrain efferents from both Hp and APH were found to project ipsilaterally to the septum, the area of the fasciculus diagonalis Brocae, nucleus taeniae, and area corticoidea dorsolateralis. Only Hp appeared to send efferents to the contralateral septum and Hp, while only APH sent efferents to the hyperstriatum dorsale and the archistriatum. A hypothalamic projection from Hp and APH was found to partially terminate near the nucleus mamillaris lateralis. At the level of pathway connections, the results demonstrate a striking similarity between the avian dorsomedial forebrain and the dorsomedial cortex of reptiles and the mammalian hippocampus

    The avian hippocampus: Evidence for a role in the development of the homing pigeon navigational map

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    Young homing pigeons were subjected to hippocampal lesion before being placed in their permanent loft to examine what effect such treatment may have on the development of their navigational map, which supports homing from distant unfamiliar locations. When later released from 3 distant unfamiliar locations, the hippocampal-lesioned pigeons were impaired in taking up a homeward bearing. The results identify a deficit in the acquisition of navigational ability after hippocampal ablation in homing pigeons. The results strongly suggest a deficit in navigational map acquisition, but alternative interpretations cannot be excluded. The findings offer the first insight into the central neural structures involved in the acquisition of the pigeon navigational map. Further, the results identify the hippocampus as a structure critical for the regulation of navigational behavior that manifests itself in a natural setting

    Impaired retention of preoperatively acquired spatial reference memory in homing pigeons following hippocampal ablation

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    Hippocampal-parahippocampal-ablated homing pigeons have been shown to suffer a retrograde loss of information used in the recognition of their home loft. Here we report that the range of retrograde deficits includes spatial reference memory in the form of information gained from repeated training sites that can be used to direct a homeward orientation response. Following 8 training releases from each of two sites, 28 of 42 homing pigeons underwent hippocampal-parahippocampal ablation. In the subsequent test releases from the two sites, untreated controls whose navigational map was rendered temporarily dysfunctional by an anosmic procedure showed no impairment in determining the home direction, indicating the successful retention and utilization of directionally useful information around the release sites. Hippocampal-ablated controls who were not rendered anosmic and thus had access to their navigational map also showed no impairment in determining the home direction, indicating no general impairment in initial orientation as a result of hippocampal ablation. In contrast, hippocampal-ablated pigeons whose navigational map was rendered temporarily dysfunctional failed to successfully orient homeward from the training sites, indicating impairment in the retention and/or implementation of directional information gathered at the release sites during training. The data reveal a spatial reference memory deficit involving pre-ablation acquired directional information in homing pigeons following hippocampal ablation

    Hippocampal ablated homing pigeons show a persistent impairment in the time taken to return home

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    Homing pigeons were subjected to ei- ther hippocampal or control anterior forebrain ab- lations to examine what role the hippocampus and related structures may play in homing behavior. One year after surgery, the test birds were released from five locations where they had never been be- fore. Both groups were successful in orienting ho- meward from the release sites, indicating that the hippocampus is not necessary for the neural regu- lation of a pigeon's map and compass system. Nonetheless, hippocampal ablated pigeons were significantly poorer with respect to the time re- quired to return home, indicating a homing perfor- mance impairment. Alternative hypotheses are dis- cussed to explain this result, the most parsimoni- ous being impaired ability on the part of the hippo- campal ablated birds to direct a course homewar

    Homing behavior of pigeons after telencephalic ablations

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    In a first experiment, dorsomedial forebrain ablated birds showed similar homeward orientation when compared to untreated controls independent of whether the birds were released from a previous training site or a site they had never been before. However, although all control birds returned to the home loft, only 2 of 28 birds with lesions homed successfully. In a subsequent experiment, both sham operated control birds and birds with lesions of the visual Wulst homed successfully when released only 800 m from and in full view of their respective home lofts. Pigeons with dorsomedial forebrain lesions, however, failed to return to their respective home lofts. The results show that the avian dorsomedial forebrain plays a critical role in that step of the homing process by which a pigeon returns to its home loft once in its vicinity, and that the failure to reassociate with the home loft is a likely result of deficient recognition of the home loft and/or its surrounding area. In an additional experiment, pigeons with Wulst lesions were shown to orient as controls and to successfully return to the home loft when released from two distant sites. This experiment demonstrated that the avian Wulst plays no necessary role in the homing behavior of pigeons

    Connections of the piriform cortex of the homing pigeon Columba livia studied with fast blue and WGA-HRP

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    The piriform cortex in homing pigeons receives a projection from the olfactory bulb and is necessary for the operation of those aspects of the navigational map based on olfactory stimuli in these animals. The afferent and efferent projections of the piriform cortex were studied using retrograde migration of wheat-germ agglutinin horseradish peroxidase (WGA-HRP) and Fast Blue, and anterograde migration of WGA-HRP. The piriform cortex was found to receive projections from, and send projections to, numerous regions and nuclei in the telencephalon, diencephalon and lower brainstem. A reciprocal connection with the parahippocampal region suggests that the piriform cortex and hippocampal formation may be part of a neural system that regulates navigational map learning. The piriform cortex also connects reciprocally with a large portion of the anterior telencephalon, including the cortex prepiriformis and hyperstriatum dorsale. In general, the pathway connections of the piriform cortex in homing pigeons are similar to those of the piriform cortex in mammals

    Unimpaired acquisition of spatial reference memory, but impaired homing performance in hippocampal-ablated pigeons

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    Hippocampal ablated homing pigeons have been shown to suffer a retrograde spatial reference memory deficit involving a preoperatively acquired homeward orientation response based on local cues around a previously visited release site. Here we report that the postoperative acquisition of such a response is unimpaired. Initially, 25 hippocampal ablated and 11 sham-operated controls were given 5 training releases from each of two sites. In the subsequent experimental releases from the two training sites, the controls and half the hippocampal-ablated pigeons had their navigational maps rendered dysfunctional via an anosmic procedure. Nonetheless, both groups successfully oriented homeward, indicating that the hippocampal-ablated pigeons were unimpaired in the acquisition and implementation of directionally useful information around the training sites to direct a homeward orientation response. The remaining half of the hippocampal-ablated pigeons who were not rendered anosmic, and thus served as controls, also oriented homeward. The data indicate that, for hippocampal-ablated homing pigeons, postoperative acquisition is unimpaired in the same spatial reference memory task where a robust retrograde impairment was observed. However, the hippocampal-ablated pigeons were impaired in the time required to return home, indicating a deficit in homing performance beyond the initial orientation stage

    Dorsomedial forebrain ablations and home loft association behavior in homing pigeons

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    In a series of experiments which involved only short distance experimental releases (800 m or less and within view of the home loft), it was demonstrated that dorsomedial forebrain ablated pigeons generally failed to reassociate with their home loft if the postablation experimental release took place soon postablation or if during the time between ablation and experimental release they were kept away from their home loft. In contrast, if dorsomedial forebrain ablated pigeons were allowed to recover at their home loft prior to experimental release, they succeeded in associating with their home loft in a manner similar to controls. However, only postablation exposure to a pigeon's own loft was sufficient to permit continued home loft association. Pigeons from one loft failed to associate with a foreign postablation recovery loft when released within sight of it. The results show that dorsomedial forebrain ablations result in pigeons which no longer succeed in associating with their home loft; recovery from failed home loft association behavior is possible with postablation exposure to the home loft, and a pigeon's previous association with a loft was a precondition if postablation association was to be affected. The results suggest that dorsomedial forebrain ablated pigeons retain something like a 'home loft trace' which they can use to mediate retrieval and reformation of the recognition properties needed for proper home loft association
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