Neural specialization for hovering in hummingbirds: hypertrophy of the pretectal nucleus Lentiformis mesencephali

Hummingbirds possess an array of morphological and physiological specializations that allow them hover such that they maintain a stable position in space for extended periods. Among birds, this sustained hovering is unique to hummingbirds, but possible neural specializations underlying this behavior have not been investigated. The optokinetic response (OKR) is one of several behaviors that facilitates stabilization. In birds, the OKR is generated by the nucleus of the basal optic root (nBOR) and pretectal nucleus lentiformis mesencephali (LM). Because stabilization during hovering is dependent on the OKR, we predicted that nBOR and LM would be significantly enlarged in hummingbirds. We examined the relative size of nBOR, LM, and other visual nuclei of 37 species of birds from 13 orders, including nine hummingbird species. Also included were three species that hover for short periods of time (transient hoverers; a kingfisher, a kestrel, and a nectarivorous songbird). Our results demonstrate that, relative to brain volume, LM is significantly hypertrophied in hummingbirds compared with other birds. In the transient hoverers, there is a moderate enlargement of the LM, but not to the extent found in the hummingbirds. The same degree of hypertrophy is not, however, present in nBOR or the other visual nuclei measured: nucleus geniculatus lateralis, pars ventralis, and optic tectum. This selective hypertrophy of LM and not other visual nuclei suggests that the direction-selective optokinetic neurons in LM are critical for sustained hovering flight because of their prominent role in the OKR and gaze stabilization.