Gerald E. Hough

Revised Nomenclature for Avian Telencephalon and Some Related Brainstem Nuclei

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 In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is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 the pallial sector of the developing telencephalon). Recognizing that this promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains, avian brain specialists began discussions to rectify this problem, culminating in the Avian Brain Nomenclature Forum held at Duke University in July 2002, which approved a new terminology for avian telencephalon and some allied brainstem cell groups. Details of this new terminology are presented here, as is a rationale for each name change and evidence for any homologies implied by the new names.

Avian brains and a new understanding of vertebrate brain evolution

We believe that names have a powerful influence on the experiments we do and the way in which we think. For this reason, and in the light of new evidence about the function and evolution of the vertebrate brain, an international consortium of neuroscientists has reconsidered the traditional, 100-year-old terminology that is used to describe the avian cerebrum. Our current understanding of the avian brain — in particular the neocortex-like cognitive functions of the avian pallium — requires a new terminology that better reflects these functions and the homologies between avian and mammalian brains.

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.

Internal connectivity of the homing pigeon (Columba livia) hippocampal formation: An anterograde and retrograde tracer study

The avian hippocampal formation (HF) is a structure necessary for learning and remembering aspects of environmental space. Therefore, understanding the connections between different HF regions is important for determining how spatial learning processes are organized within the avian brain. The prevailing feed‐forward, trisynaptic internal connectivity of the mammalian hippocampus and its importance for cognition have been well described, but the internal connectivity of the avian HF has only recently been investigated. To examine further the connectivity within the avian HF, small amounts of cholera toxin subunit B, primarily a retrograde tracer (n = 15), or biotinylated dextran amine, primarily an anterograde tracer (n = 10), were injected into localized regions of the HF. Examination of the immunohistochemically labeled tissue showed projections from extrinsic sensory processing areas into dorsolateral HF and the dorsal portion of the dorsomedial HF (DMd). DMd in turn projected into the medial (VM) and lateral (VL) ventral cell layers. A projection from VM into VL was found, and together these areas and DM provided input into the contralateral ventral cell layers. Ipsilaterally, a ventral portion of dorsomedial HF (DMv) received input from VL and VM. From DMv, projections exited HF laterally. The highlighted projections formed a discernible feed‐forward processing network through the avian HF that resembled the trisynaptic circuit of the mammalian HF. J. Comp. Neurol. 459:127–141, 2003.

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.

Intrahippocampal connections in the pigeon (Columba livia) as revealed by stimulation evoked field potentials

The hippocampal formation (HF) of mammals and birds is crucial for spatial learning and memory. However, although the underlying synaptic organization and connectivity of the mammalian HF are well characterized, comparatively little is known about the avian HF. Localized regions of the homing pigeon HF were stimulated at 400–600 μA while evoked field potentials (EFPs) were recorded from adjacent and more distant HF areas relative to the stimulation site. The shortest discernible EFP latency was 12.2 msec. The emerging connectivity profile (using the location of peak EFP amplitude after stimulation and making no determination of the number of intervening synapses) was characterized by projections from the dorsolateral (DL) HF to the dorsomedial (DM) HF (15‐msec latency) at the same anterior/posterior (A/P) level, DM to ventrolateral (VL) and ventromedial (VM; 15 msec) HF across A/P levels, VM to VL (12 msec) and contralateral VM (15 msec) at the same A/P level, and VL to ventral DL (DLv; 15 msec) across A/P levels posterior to the stimulation site. Using these data as a first approximation, connectivity through the avian HF appears to be characterized by a discernible feed‐forward network starting with a projection from DL to DM, DM to VL, VM, and contralateral VM, VM to VL, and VL to posterior ventral DLv. Although still speculative, the results suggest that the internal connectivity of the avian HF is similar to that of the mammalian HF, despite the large evolutionary divergence between the two taxa. J. Comp. Neurol. 452:297–309, 2002.

Rotation of visual landmark cues influences the spatial response profile of hippocampal neurons in freely-moving homing pigeons

Pigeon hippocampal neurons display two spatial response profiles: location fields frequently at goals, and path fields connecting goals. We recorded from 15 location and six path cells, with color cues positioned near four goal locations. Following color cue rotation, most location cells (12/15) shifted their response fields; path cells (5/6) lost their fields. Therefore, local visual cues can independently define a reference frame for location cells, but path cells may be more broadly tuned to context or alternative reference frames.

Age-related spatial working memory deficits in homing pigeons (Columba livia).

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.

The digital archiving project at the Borror Laboratory of Bioacoustics

The Borror Laboratory of Bioacoustics (BLB) at The Ohio State University is a research facility with an archive of recorded animal sounds collected primarily by BLB staff and associates. The 25 000 sound recordings are scientific data that require special treatment to ensure their longevity, and the BLB is, like other sound archives, dedicated to the preservation of these recorded sounds. Traditionally, sound recordings have been archived on analog 1/4‐in. magnetic tape. However, magnetic tape is degraded by time, usage, and excess temperature and humidity. Additionally, access to data on analog tapes is slow. Facing loss of access to data, especially on tapes exceeding their 50‐year life expectancy, we are copying the collection to digital format [compact disk recordable (CDR)] with the aid of funding from the National Science Foundation. Because digital technology has been tested and refined over nearly two decades, and CDR media for storage of digital data now sustains a viable commercial market, ar...