Owls are capable of great accuracy in detecting ITDs, and their auditory system shows morphological adaptations that contribute to this increased acuity. Among these are the asymmetry of the external ears, the organization of the facial ruff, an attenuation of tympanic interactions via the interaural canal, and hyperplasia of the auditory nuclei (Payne, 1971
; Moiseff and Konishi, 1981
; Calford and Piddington, 1988
; Massoglia, 1997
) (M. F. Kubke, C. E. Carr, unpublished observations).
The organization of NL, and its inputs from NM, varies considerably among different species of birds (Ariëns Kappers et al., 1967
; Kubke and Carr, 2000
). Basal birds, such as the emu and kiwi, as well as crocodilians, show an organization resembling that of the chicken (Craige, 1930
; Carr and Code, 2000
; Soares et al., 2001
) (Kubke and Carr, unpublished observations). We assume that this organization represents a primitive (plesiomorphic) condition. The owl’s organization must consequently be considered a derived (apomorphic) state. Given that ontogenetic changes must underlie circuit remodeling, comparisons between homologous circuits may identify which elements have been changed during evolution. Because the development of the plesiomorphic chicken auditory system has been studied thoroughly (for review, see Rubel and Parks, 1988
; Kubke and Carr, 2000
; Rubel and Fritzsch, 2002
), we were able to compare the morphology of embryonic auditory structures in the owl with those of chicken. Because the morphological specializations seen in the auditory hindbrain of owls must result from changes to the ancestral pattern, we investigated the events that led to the reorganization of the owl map of ITDs during development.
Embryonic owl development closely resembled chicken development until late in embryogenesis, when the organization of NL took on the characteristic apomorphic form associated with the reorganization of the map of ITDs (Harkmark, 1954
; Knowlton, 1967
; Rubel et al., 1976
; Book and Morest, 1990
). The striking similarities between the early development of the chicken and owl auditory system support the hypothesis that small changes in the development of the NL circuit lead to the reorganization seen in owl NL and also to the behavioral changes in acuity observed in the owl (Nishikawa, 1997
). The emergence of this novel secondary morphogenetic phase suggests that the reorganization of NL may be an adaptation for accurate detection of ITDs. This reorganization is characterized by three major events. These are the loss of the laminar organization, the retraction of dendrites in NL neurons, and the redistribution of NM–NL synapses.
The loss of the laminar organization found in basal birds and crocodilians appears to be a fundamental difference between chickens and owls and results in an expansion in the dorsoventral dimension. The laminar organization of NL in the chicken restricts the configuration in which ITD can be mapped to a single dimension along the mediolateral anatomical axis within each isofrequency band (Young and Rubel, 1983
; Overholt et al., 1992
; Joseph and Hyson, 1993
). In contrast, the reorganization of the NM–NL circuit in the owl gives rise to additional NM axonal segments within a newly added dorsoventral dimension. These segments provide the delay required for mapping the ITDs associated with the contralateral hemifield (Sullivan and Konishi, 1986
; Carr and Boudreau, 1991
). The short NM axonal segments within NL can provide the required delay within the spatial limits of the dorsoventral span of the nucleus because of a reduction of the internodal distance and axonal diameter, which results in slower conduction velocity within NL. Delayed myelination of these axonal segments has been proposed as a mechanism by which internodal distances are reduced (Carr, 1994
; Cheng, 2001
The segregation of ipsilateral and contralateral inputs onto dorsal and ventral dendrites appears to be an important feature in the ability of the neuron to perform coincidence detection in the chicken (Overholt et al., 1992
; Agmon-Snir et al., 1998
). This segregation, however, does not favor ITD computations at frequencies above 2 kHz (Agmon-Snir et al., 1998
; Simon et al., 1999
). Owls accurately compute ITDs between 4 and 8 kHz, a range above that of other vertebrates (Konishi, 1999
), and their NL neurons are characterized by many short unpolarized dendrites (Carr and Boudreau, 1993
). The owl-like organization of NL can also be found in other bird species with hearing ranges that extend above 4 kHz (Kubke, Dent, and Carr, unpublished observations). The loss of the laminar structure and the reorganization of the delay lines are accompanied by the loss of the bitufted NL cell morphology. Whether the redistribution of dendrites and synapses improves ITD computation or whether it is a consequence of external signals remains to be established.
The role of biochemical signaling has been shown in the NL in the chicken. Here, NM projects to the dorsal dendrites of ipsilateral NL neurons and to the ventral dendrites of contralateral NL neurons. Tyrosine kinase signaling may be involved in establishing these spatially segregated connections (Cochran et al., 1999
; Cramer et al., 2000b
). When NM–NL projections are forming, EphA4 expression in NL is asymmetric, with higher expression in the dorsal NL neuropil than in the ventral neuropil. At the same time, a complementary pattern of tyrosine kinase B receptor is observed with higher levels of expression in the ventral neuropil. The interplay between these two signaling systems may serve to guide growing axons to the appropriate region (Cochran et al., 1999
; Cramer et al., 2000b
). Developmental studies in owl may reveal whether these expression patterns have changed.
Improvements in behavioral acuity can be the result of modifications of a single circuit or increases in the areas devoted to a given computation. Examples of the latter include increasing the number and expanse of visual areas in primates and auditory areas in bats (Suga et al., 1987
; Northcutt and Kaas, 1995
; Krubitzer et al., 1997
). These increases in cortex most likely result from prolonged development and protracted neurogenesis (Finlay and Darlington, 1995
). Circuit modification occurs during development of the ITD circuit in the brainstem of the owl. Secondary morphogenetic events remodel the NM–NL circuit and its associated azimuthal map. This circuit modification may contribute to the increased acuity of sound localization in owls. The nervous system is evolutionarily conservative, and small changes in structure can lead to profound changes in function and behavior (Nishikawa, 1997
). Understanding how these morphogenetic changes take place in the context of increased behavioral function should illuminate mechanisms by which neural circuits evolve.