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David C. Airey, Ph.D.

  Dave Airey
Center for Neuroscience and
Department of Anatomy and Neurobiology
University of Tennessee
855 Monroe Avenue
Memphis, TN 38163 USA

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    (901) 448-7557
(901) 448-7018
(901) 448-7193
dairey@nb.utmem.edu
http://www.nervenet.org/

Contents/Directory

Papers
Abstracts
Research Focus
Professional Appointments
Society Memberships
Awards
Teaching
Ph.D. Thesis



Degrees

Ph.D. (1999) Psychology, Cornell University
B.S. (1992) with Honors and Summa cum Laude, Psychology, University of Maryland, College Park
 

Interests

Development and evolution of neural circuits
Distribution of cell number in neural circuits
Behavioral or performance correlates of neuroanatomical variation
Song control system
Cerebellum
Retina
 

Professional Experience

1999–present: Postdoctoral Trainee to Professor Robert W. Williams, University of Tennessee, Department of Anatomy and Neurobiology
 

Professional Society Memberships

Society for Neuroscience
International Mammalian Genome Society
Behavioral Genetics Association
 

Grants and Fellowships

2000–present: National Research Service Award (5.10.00 to 5.9.03)
1992–1995: National Science Foundation Fellow
1992: Summer UMCP Undergraduate Research Award ($2500).
 

Awards

Phi Beta Kappa 1992

 

Papers

Airey DC, Kroodsma DE and DeVoogd TJ. (2000) Differences in the complexity of song tutoring cause differences in the amount learned and in dendritic spine density in a songbird telencephalic song control nucleus. Neurobiology of Learning and Memory. 73(3):274-81

Airey DC, Buchanan KL, Székely T, Catchpole CK, and DeVoogd TJ. (2000) Song, sexual selection and a song control nucleus (HVc) in the brains of European sedge warblers. J Neurobiol. 44(1):1-6

Airey DC and DeVoogd TJ. (2000) Greater song complexity is associated with augmented song system anatomy in zebra finches. NeuroReport. 11(10):2339-44

Airey DC, Castillo-Juarez H, Casella G, Pollak EJ and DeVoogd TJ. (in press) Variation in the volume of zebra finch song control nuclei is heritable: developmental and evolutionary implications. Proc Roy Soc Lond Series B.

Airey DC, Lu L and Williams RW. (in preparation) Gene loci for quantitative differences in cerebellum size of mice. J Neurosci.

Lu L, Airey DC and Williams RW. (in review) Genetic architecture of the mouse hippocampus: indentification of quantitative trait loci with specific effects on hippocampal size. J Neurosci.

Willliams RW, Airey DC, Kulkarni A, Zhou G, and Lu L (in press) Genetic dissection of olfactory bulbs in mice: QTLs on 4, 6, 11, and 17 modulate bulb size. Behavioral Genetics.

 

Abstracts

Epelboim J, Booth J, Airey DC and Steinman RM. (1992) Eye movements while reading unspaced text. ARVO Abstracts.

Airey DC, DeVoogd TJ and Kroodsma DE. (1994) Morphometry of song control neurons in differentially tutored Eastern marsh wrens (Cistothous palustris). Society for Neuroscience Abstracts.

Airey DC, Niederer JK, Nelson AL, DeVoogd TJ and Finlay BL. (1996) High vocal center and encephalization: Specialization and developmental constraints. Society for Neuroscience Abstracts.

Collins CE, Airey DC, Guzman J, Lisi V, Nam N, Tremper K and DeVoogd TJ. (1996) Developmental effects of song deprivation in zebra finches. Society for Neuroscience Abstracts.

Airey DC, Strom R and Williams RW. (1998). Genetic architecture of normal variation in cerebellar size. Society for Neuroscience Abstracts.

Williams RW, Strom R, Zhou G, Airey DC. (1998) New QTLs that modulate eye and brain development: comparison of RIs, F2s, and an advanced intercross. 12th International Mouse Genome Conference.

Airey DC, Castillo HJ, Pollak EJ, Casella G and DeVoogd TJ. (1999) Phenotypic and quantitative genetic description of Nissl-defined volumes of song control nuclei in zebra finches. Society for Neuroscience Abstracts.

Lu L, Airey DC, Gilissen E, Zhou G, Williams RW. (1999) New murine hippocampus-specific QTL maps to distal Chr. 1. 13th International Mouse Genome Conference.

Airey DC, Lu L, Strom R, Gilissen E, Zhou G, Williams RW. (1999) Cerebellum-specific QTLs in the mouse brain. 13th International Mouse Genome Conference.

Johnson D, Ferkin M, Hamre KM, Matthews D, Mittleman G, Williams RW, Airey DC, Rinchik E, and Goldowitz D. (2000) Generation of Neurological mutant mice using ENU-mutagenesis of discrete regions of the genome. Society for Neuroscience Abstracts.

Airey DC, Lu L, Williams RW. (2000) Gene loci for mouse cerebellum and internal granule layer size. Society for Neuroscience Abstracts.

Lu L, Airey DC, Williams RW. (2000) Complex trait analysis of the mouse hippocampus. Society for Neuroscience Abstracts.

Kulkarni A, Airey DC, Williams (2000) Genetic architecture of the mouse retinogeniculate system: A QTL analysis of numerical matching. Society for Neuroscience Abstracts.

 

Teaching

Psychology 322: Hormones and Behavior, Cornell University, Spring 1998
Psychology 322-1: Hormones and Neural Circuits, Cornell University, Spring 1998
Psychology 326: Evolution of Human Behavior, Cornell University, Fall 1997
Psychology 332: Neurobiol. of Learn. and Mem., Cornell University, Spring 1997
Psychology 123: Introduction to Biopsychology, Cornell University, Fall 1996
Psychology 101: Introduction to Psychology, Cornell University, Summer 1996
Psychology 276: Motivation, Cornell University, Spring 1996
Psychology 324: Research Methods in Biopsychology, Cornell University, Fall 1994
General Honors 100: Introduction to Research Methods at UMCP, Spring 1992


  Thesis Summary

Neuroanatomical correlates of bird song: individual differences and evolution

David C. Airey, Ph.D.
May, 1999


Thesis Advisor: Timothy J. DeVoogd
Associate Professor
Department of Psychology and Field of Neurobiology and Behavior
Cornell University

Thesis Committee Member: Barbara L. Finlay
Professor and Department Chair
Department of Psychology
Cornell University

Thesis Committee Member: Bob Johnston
Professor
Department of Psychology
Cornell University


Summary

A central goal in behavioral neuroscience is the study and explanation of correlations between brain and behavior. In my doctoral thesis, "Neuroanatomical correlates of bird song: individual differences and evolution", I sought to explore and explain a positive correlation between natural variation in the size of a brain region in songbirds and variation in song behavior. I describe four original studies from my thesis below that add to our understanding of how differences in song learning affect the brain and how differences in brain size affect the capacity for song learning. My work also informs our understanding of the evolution of neural capacity for behavioral differences. I first present background and rationale.

Three articles best illustrate the fascinating and core observation between brain and behavior in songbirds. Canady, Kroodsma, and Nottebohm (1984) found positive correlations between variation in volume of the song control nucleus HVc (proper name) and the number of song types recorded from individual Eastern or Western marsh wrens. This paper was the first to show a correlation between HVc and song repertoire size within and across wild songbird populations. Within either subspecies, wrens with a larger HVc had a larger song repertoire. Western wrens, which naturally sing a repertoire of about 150 song types, had a larger HVc than Eastern wrens that naturally sing about 50 song types. There was no estimated difference in overall brain size between the two marsh wren populations. Because song is learned by juveniles from singing adults, a key question was raised. Does learning cause HVc size or does HVc size limit learning? Kroodsma and Canady (1985) brought nestling Eastern and Western marsh wrens into the laboratory where they were artificially tutored with a supernormal repertoire of combined Eastern and Western song types. Despite this common rearing environment, individual Eastern wrens developed repertoire sizes typical for Eastern wrens and Western wrens developed repertoire sizes typical of Western wrens. In addition, the volume estimate of HVc for Western wrens was larger than for Eastern wrens. The differences between Eastern and Western wrens in repertoire size and the volume of HVc was thus presumed to have a genetic basis. Brenowitz, Lent, and Kroodsma (1995) addressed the direction of causation for the observed HVc and repertoire size correlation by asking if learning a small or large repertoire of song types caused differences in HVc size. Nestling Eastern marsh wrens were brought into the laboratory and artificially tutored with either a small repertoire or a large repertoire of songs. While the tutoring successfully created a large behavioral difference, there were no differences in the volumes of HVc between groups. Within the group that heard a large repertoire, the correlation between the volume of HVc and repertoire size approached significance.


The results of these three studies suggest that the size of the song control nucleus HVc is unaffected by early acoustic learning experiences related to hearing or producing different repertoire sizes, and that the size of HVc may set an upper limit to the size of the song repertoire that can be acquired. This working hypothesis claims that birds with large HVc can sing either large or small repertoires, but that birds with small HVc may not sing large repertoires. The hypothesis does not, however, explain how or why the correlation occurs.


Good explanations of biological causation address questions related to both how and why a behavior occurs. Tinbergen (1963) usefully partitioned biological causation into four complementary descriptions. To ask how a bird sings a large song repertoire is to inquire after mechanism or development. To ask why a bird sings a large song repertoire is to inquire after fitness consequences or ancestral qualities. Mechanism, ontogeny, phylogeny, and adaptation are each necessary pieces of a complete biological causal statement of repertoire size (e.g., Kroodsma and Byers 1998; DeVoogd and Szekely 1998). I organized my study of the correlation between HVc and repertoire size in songbirds with three questions: (1) What is the developmental basis for differences in HVc size? (2) Do differences in HVc size translate to performance differences in song behavior? (3) Do performance differences in song behavior (and differences in HVc size) translate to differences in reproductive success?


Chapter 2, "Sexual selection and brain size", provides a broad background of material related to why repertoire size is important to songbirds. I define sexual selection and provide a brief survey of reviews describing sexual selection of song in animals, particularly songbirds. I conclude that song has two primary functions, territory defense and mate attraction, and that repertoire size is a cue used by females to choose mates. I follow this review with another broad background of material related to the developmental sources of size variance in brains and brain parts, particularly nucleus HVc. The intersection of sexual selection and brains has been addressed by Jacobs (1996). She asserted, "if females...can assess a male's ability to learn more information, or learn more quickly than rival males, then the demonstration of enhanced learning abilities could be a sign of a superior mate. The rationale for this is based on the idea of limited 'brain space'; learning requires an investment in brain tissue, which is extremely metabolically expensive. Hence, if enhanced learning demands increased allocation to 'brain space', then conspicuous indicators of learning ability (and their underlying brain structures) could be subject to sexual selection."


Chapter 3 presents a study titled, "Differences in the complexity of song tutoring cause differences in the amount learned and in dendritic spine density in a songbird telencephalic song control nucleus" (Airey et al., 2000a). This study tested whether differential experience that leads to differences in adult song repertoire affects dendritic spine density in HVc and its efferent target RA (robustus archistriatalis). Juvenile eastern marsh wrens were tape tutored with either 5 or 45 song types. As adults, the small repertoire group had learned mostly 5 or 6 song types, the large repertoire group 36 to 47. Wrens that learned the large song repertoires had a greater dendritic spine density for the most spiny neurons present in HVc (mean difference, 36%), but not in RA. Recent physiological evidence describes HVc as a premotor area coding syllables, motifs, and higher-order song patterns, and my data now clearly reveal that differences in the size of the song repertoire that are experienced lead to differences both in song learning and in the density of dendritic spines in HVc. In the forebrain song nuclei of these songbirds, as in some other vertebrate systems, differences in learning and performance are associated with differences in synaptic anatomy specifically in the region that organizes the learned pattern. This study was conducted in collaboration with Donald E. Kroodsma on the alternate hemispheres of the brains of the same marsh wrens used in the study by Brenowitz et al. (1995) described above. Although those authors showed that learning either a small or a large song repertoire does not cause gross changes in the volume of HVc, my results suggest that the working hypothesis above should be modified to respect the distinction between fine and gross anatomical correlates of learning a small or a large song repertoire.


Chapter 4 presents a study titled, "Song, sexual selection and a song control nucleus (HVc) in the brains of European sedge warblers" (Airey et al., 2000b). Prior studies showed that repertoire size is a cue female sedge warblers use to choose mates (Buchanan and Catchpole, 1997). This study tests two predictions concerning HVc size in male sedge warblers: first, that males with more complex songs will have a larger HVc, and second, that males who pair successfully will have a larger HVc than unpaired males. Data on song composition and pairing status were collected from wild sedge warblers breeding in Hungary. I found that male HVc volume standardized over telencephalon volume predicts three measures of song complexity, including repertoire size. I did not detect a group difference in HVc volume between six paired males and six unpaired males. I could not claim female choice as a source of directional selection for increased HVc size in sedge warblers. However, power analysis also suggests caution in claiming evidence that the groups are not different. Further study of this population is required to address the effects of age and female choice on HVc size in male sedge warblers. The results contribute to a growing body of evidence supporting a functional relationship between individual differences in song performance and HVc size.


Chapter 5 presents a study titled, "Greater song complexity is associated with augmented song system anatomy in zebra finches" (Airey and DeVoogd, 2000c). In this study I revisited the relation between brain anatomy and song behavior in zebra finches, believing that two prior studies were not conclusive for all zebra finches in all environments. I found that differences in song behavior (repertoire size and phrase duration) are related to differences in HVc size in zebra finches that have learned song in a complex social setting. This is similar to previous investigations of song complexity and HVc size in canaries, marsh wrens, starlings, and sedge warblers. I advanced the study of brain and behavior correlations in songbirds by showing that repertoire size in zebra finches can be well predicted by the combined variance in several brain nuclei (multiple R = 0.871), providing the first demonstration that volumetric differences across multiple components of a neural network are predictive of song behavior. The result apparently depends on the ratio of the neostriatal nuclei (HVc and lMAN) to the paleostriatal nucleus Area X. Thus, larger song repertoires and longer songs may require greater amounts of the nucleus HVc to represent more song units or the temporal sequences of linked acoustic units, but in zebra finches a greater amount of HVc per se may not be as important as the amount relative to the volumes of other circuit nuclei.


Chapter 6 presents a large-scale neuroanatomical study titled "Variation in the volume of zebra finch song control nuclei is heritable: developmental and evolutionary implications" (Airey et al., 2000d), in which I estimated the additive genetic determinants of size variance in HVc and other song control nuclei by measuring the volume of all major song nuclei and of the telencephalon in more than 100 adult male zebra finches from 38 families. In many songbird species, females prefer males who sing a larger repertoire of syllables. Males with more elaborate songs have a larger nucleus HVc, the highest structure in the song production pathway. HVc size is thus a potential target of sexual selection. I found evidence that the size of HVc and other song production nuclei are heritable across individual males within a species. In contrast, I found that heritabilities of other nuclei in a song learning pathway are lower and are not different from zero, suggesting that variation in the sizes of these structures is more closely tied to developmental and environmental differences between individuals. I found that evolvability, a statistical measure that predicts response to selection, is higher for HVc and its target for song production, RA, than for all other brain volumes measured. This suggests that selection based on the functions of these two structures would result in rapid major shifts in their anatomy. I also found that the size of each song control nucleus is significantly phenotypically correlated with the song related nuclei to which it is monosynaptically connected, and that the correlation between HVc and RA contains a significant genetic component. This suggests that selection on HVc through female choice on male song complexity may produce correlated shifts in the anatomy of RA. Finally, I found that the volume of the telencephalon is 8% larger in males than in females, a result which suggests that selection on HVc size may be more costly than previously suspected, as HVc correlates significantly with telencephalon size.


These findings begin to join theoretical analyses of the role of female choice in the evolution of bird song to neurobiological mechanisms by which the evolutionary changes in behavior are expressed. Because aspects of song behavior in songbirds are learned, song is in part a culturally transmitted behavior, and this may be the strongest immediate factor determining song complexity for individual songbirds. But evidence suggests that the size of the song nucleus HVc may set an upper limit to the size of the song repertoire that can be learned. A role for the genetic transmission of repertoire size must also be considered. I raised three questions at the outset, (1) What is the developmental basis for differences in HVc size? (2) Do differences in HVc size translate to performance differences in song behavior? (3) Do performance differences in song behavior (and differences in HVc size) translate to differences in reproductive success? I have shown that the developmental basis of HVc size and other song control regions includes additive genetic contributions of the parental genome. I have also shown that performance differences in male song behavior correlate robustly with male HVc size. Continued research may also show that females that choose males with more complex song or larger HVc are ensuring the reproductive benefits of these characters in their sons.

References


Airey DC, Kroodsma DE and DeVoogd TJ. (2000a) Differences in the complexity of song tutoring cause differences in the amount learned and in dendritic spine density in a songbird telencephalic song control nucleus. Neurobiology of Learning and Memory: 73(3), 274-81.


Airey DC, Buchanan KL, Székely T, Catchpole CK, and DeVoogd TJ. (2000b) Song, sexual selection and a song control nucleus (HVc) in the brains of European sedge warblers. J Neurobiol. In press.


Airey DC and DeVoogd TJ (2000c) Greater song complexity is associated with augmented song system anatomy in zebra finches. NeuroReport. In press.


Airey DC, Castillo-Juarez H, Casella G, Pollak EJ andDeVoogd TJ. (2000d) Variation in the volume of zebra finch song control nuclei is heritable: developmental and evolutionary implications. Proc Roy Soc Lond Series B. In review.


Buchanan KL and Catchpole CK. (1997) Female choice in the sedge warbler, Acrocephalus schoenobaenus: multiple cues from song and territory quality. Proc Roy Soc Lond Series B 364, 521-526.


Brenowitz EA, Lent K and Kroodsma DE. (1995) Brain space for learned song in birds develops independently of song learning. J Neurosci 15(9), 6281-6286.


Canady RA, Kroodsma DE and Nottebohm F. (1984) Population differences in complexity of a learned skill are correlated with the brain space involved. Proc Natl Acad Sci USA 81, 6232-6234.


DeVoogd TJ and Székely T. (1998) Causes of avian song: Using neurobiology to integrate proximate and ultimate levels of analysis. In: Animal Cognition in Nature (pp. 337-380): Academic Press.


Jacobs LF. (1996) Sexual selection in the brain. Trends in Ecology and Evolution 11(2), 82-86.


Kroodsma DE and Canady RR. (1985) Differences in repertoire size, singing behavior, and associated neuroanatomy among marsh wren populations have a genetic basis. Auk 102(3), 439-446.


Kroodsma DE and Byers BE. (1998) Songbird song repertoires: an ethological approach to studying cognition. In: Animal Cognition in Nature (pp. 305-336): Academic Press.


Tinbergen N. (1963) On aims and methods of ethology. Zeitschrift fur Tierpsychologie 20, 410-433.


CV formatted for web by Alex Williams (alexgraehl@usa.net).

 



Since 16 May 2000, Updated 16 May 2000