Over many centuries, the homing pigeon has been selectively bred for returning home from a distan... more Over many centuries, the homing pigeon has been selectively bred for returning home from a distant location. As a result of this strong selective pressure, homing pigeons have developed an excellent spatial navigation system. This system passes through the hippocampal formation (HF), which shares many striking similarities to the mammalian hippocampus; there are a host of shared neuropeptides, interconnections, and its role in the storage and manipulation of spatial maps. There are some notable differences as well: there are unique connectivity patterns and spatial encoding strategies. This review summarizes the comparisons between the avian and mammalian hippocampal systems, and the responses of single neurons in several general categories: (1) location and place cells responding in specific areas, (2) path and goal cells responding between goal locations, (3) context-dependent cells that respond before or during a task, and (4) pattern, grid, and boundary cells that increase firing at stable intervals. Head-direction cells, responding to a specific compass direction, are found in mammals and other birds but not to date in pigeons. By studying an animal that evolved under significant adaptive pressure to quickly develop a complex and efficient spatial memory system, we may better understand the comparative neurology of neurospatial systems, and plot new and potentially fruitful avenues of comparative research in the future.
The hippocampus (HF) of birds and mammals is essential for the map-like representation of environ... more 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.
Adult zebra finch song is irreversibly altered when birds are deprived of correct feedback by dea... more Adult zebra finch song is irreversibly altered when birds are deprived of correct feedback by deafening or denervation of the syrinx. To clarify the role of feedback in song maintenance, we developed a reversible technique to distort vocal output without damaging the auditory or vocal systems. We implanted flexible beads adjacent to the syrinx to alter its biomechanics. Immediate song aberrations included low volume, frequency shifts, missing harmonics, and production of click-like syllables. After a few weeks, seven of nine birds stopped producing some syllables. In six of these birds, the gaps left by the silenced syllables gradually shortened, and the lost syllables did not return when beads were removed 16 weeks after treatment began. The nondeleted syllables of all birds regained their preimplant morphology, insofar as could be detected, within 9 d after bead removal. In four other birds, we removed the beads as soon as syllables were deleted, when the silent intervals were still full length. In these birds, all deleted syllables returned within 1 week. Our results indicate that both silenced syllables and syllable morphology can recover as long as the song's temporal structure is maintained, but once altered, changes in the song sequence can be permanent. A hierarchical organization of the song production system has recently been described (Margoliash, 1997). Reversible disruption of song production by our method appears to permanently alter the higher levels of the system that encode song sequence, but not the lower levels that encode individual syllable structure.
Rotation of visual landmark cues influences the spatial response profile of hippocampal neurons i... more Rotation of visual landmark cues influences the spatial response profile of hippocampal neurons in freely-moving homing pigeons" Behavioural Brain Research Vol. 187 Iss. 2 (2008) p. 473-477. This Article is brought to you for free and open access by the College of Science & Mathematics at Rowan Digital Works. It has been accepted for inclusion in Faculty Scholarship for the College of Science & Mathematics by an authorized administrator of Rowan Digital Works.
Age-related spatial working memory deficits in homing pigeons (Columba livia)
Behavioral Neuroscience, 2014
The hippocampus is particularly susceptible to age-related degeneration that, like hippocampal le... more The hippocampus is particularly susceptible to age-related degeneration that, like hippocampal lesions, is thought to lead to age-related decline in spatial memory and navigation. Lesions to the avian hippocampal formation (HF) also result in impaired spatial memory and navigation, but the relationship between aging and HF-dependent spatial cognition is unknown. To investigate possible age-related decline in avian spatial cognition, the current study investigated spatial working memory performance in older homing pigeons (10+ years of age). Pigeons completed a behavioral procedure nearly identical to the delayed spatial, win-shift procedure in a modified radial arm maze that has been previously used to study spatial working memory in rats and pigeons. The results revealed that the older pigeons required a greater number of choices to task completion and were less accurate with their first 4 choices as compared to younger pigeons (1-2 years of age). In addition, older pigeons were more likely to adopt a stereotyped sampling strategy, which explained in part their impaired performance. To the best of our knowledge, this study is the first to demonstrate an age-related impairment of HF-dependent, spatial memory in birds. Implications and future directions of the findings are discussed.
Single unit recording The hippocampus (HF) of birds and mammals is essential for the map-like rep... more Single unit recording 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...
BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access t... more BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.
Box 1 | Avian Brain Nomenclature Consortium Authors are ordered alphabetically in two groups: the... more Box 1 | Avian Brain Nomenclature Consortium Authors are ordered alphabetically in two groups: the first group, along with the first two and last two authors, are the core Avian Brain Nomenclature Forum Thinktank group; the second group are professors, postdoctoral fellows and students who also participated in the Avian Brain Nomenclature Forum. (For author affiliations see online supplementary information S1 (box).
Over many centuries, the homing pigeon has been selectively bred for returning home from a distan... more Over many centuries, the homing pigeon has been selectively bred for returning home from a distant location. As a result of this strong selective pressure, homing pigeons have developed an excellent spatial navigation system. This system passes through the hippocampal formation (HF), which shares many striking similarities to the mammalian hippocampus; there are a host of shared neuropeptides, interconnections, and its role in the storage and manipulation of spatial maps. There are some notable differences as well: there are unique connectivity patterns and spatial encoding strategies. This review summarizes the comparisons between the avian and mammalian hippocampal systems, and the responses of single neurons in several general categories: (1) location and place cells responding in specific areas, (2) path and goal cells responding between goal locations, (3) context-dependent cells that respond before or during a task, and (4) pattern, grid, and boundary cells that increase firin...
Many of the assumptions of homology on which the standard nomenclature for the cell groups and fi... more Many of the assumptions of homology on which the standard nomenclature for the cell groups and fiber tracts of avian brains have been based are in error, and as a result that terminology promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains. Recognizing this problem, a number of avian brain researchers began an effort to revise the terminology, which culminated in the Avian Brain Nomenclature Forum, held at Duke University from July 18 to 20, 2002. In the new terminology approved at this Forum, the flawed conception that the telencephalon of birds consists nearly entirely of a hypertrophied basal ganglia has been purged from the telencephalic terminology, and the actual parts of the basal ganglia and its brainstem afferent cell groups have been given names reflecting their now evident homologies. The telencephalic regions that were erroneously named to reflect presumed homology to mammalian basal ganglia were...
The standard nomenclature that has been used for many telencephalic and related brainstem structu... more The standard nomenclature that has been used for many telencephalic and related brainstem structures in birds is based on flawed assumptions of homology to mammals. In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is neurochemically, hodologically, and functionally comparable to the mammalian neocortex, claustrum, and pallial amygdala (all of which derive from
SYNOPSIS. The extraordinary navigational ability of homing pigeons provides a unique spatial cogn... more SYNOPSIS. 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 ac-count 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 rhyth-mic theta activity and the electrophysiolo...
Uploads
Papers by Gerald Hough