Bigger Brains or Bigger Nuclei? Regulating the Size of Auditory Structures in Birds

Abstract

Increases in the size of the neuronal structures that mediate specific behaviors are believed to be related to enhanced computational performance. It is not clear, however, what developmental and evolutionary mechanisms mediate these changes, nor whether an increase in the size of a given neuronal population is a general mechanism to achieve enhanced computational ability. We addressed the issue of size by analyzing the variation in the relative number of cells of auditory structures in auditory specialists and generalists. We show that bird species with different auditory specializations exhibit variation in the relative size of their hindbrain auditory nuclei. In the barn owl, an auditory specialist, the hindbrain auditory nuclei involved in the computation of sound location show hyperplasia. This hyperplasia was also found in songbirds, but not in non-auditory specialists. The hyperplasia of auditory nuclei was also not seen in birds with large body weight suggesting that the total number of cells is selected for in auditory specialists. In barn owls, differences observed in the relative size of the auditory nuclei might be attributed to modifications in neurogenesis and cell death. Thus, hyperplasia of circuits used for auditory computation accompanies auditory specialization in different orders of birds.

Maps of interaural time difference in the chicken’s brainstem nucleus laminaris

“…There are several interesting differences between the chicken and the owl NL, not least the different anatomical orientation of the ITD maps. However, this is convincingly explained by the hyperplasia of the owl's NL and its specialisations for highfrequency processing (reviews in Grothe et al 2004;Kubke et al 2004). A recent in vitro study on the emu's NL showed physiological delay lines along the same anatomical axis and in the same direction as in the chicken (MacLeod et al 2006), supporting the hypothesis that this is the plesiomorphic pattern in birds.…”

The Evolution of Cerebrotypes in Birds

“…For example, comparisons of relative forebrain size have suggested a similar overall neural architecture in corvids and parrots [Psittaciformes; Emery and Clayton, 2004]. Volumetric studies also indicate the convergent neural evolution of telencephalic composition in some aquatic species [Carezzano and Bee de Speroni, 1995], medullary nuclei in auditory specialists [Kubke et al, 2004] and overall brain composition in parrots and passerines [Iwaniuk et al, 2005]. In a recent analysis of major brain components, Burish et al [2004] also provide some evidence for cerebrotypes in birds.…”

The Independent Evolution of the Enlargement of the Principal Sensory Nucleus of the Trigeminal Nerve in Three Different Groups of Birds

“…This correlation is called the 'principle of proper mass' whereby the size of a neural structure is a reflection of the complexity of the behaviors that it subserves [Jerison, 1973]. Examples of this correlation are found in all sensory systems and in all vertebrates [e.g., somatosensory: Pubols et al, 1965;Pubols and Pubols, 1972;visual: Barton, 1998;Iwaniuk and Wylie, 2007;gustatory: Finger, 1975; auditory: Kubke et al, 2004]. Some of the best-studied examples of this correlation between sensory systems and behavior come from examinations of the trigeminal system in small mammals and its representation in the primary somatosensory cortex .…”