Sensory systems in birds: What we have learned from studying sensory specialists

Abstract

"Diversity" is an apt descriptor of the research career of Jack Pettigrew as it ranged from the study of trees, to clinical conditions, to sensory neuroscience. Within sensory neuroscience, he was fascinated by the evolution of sensory systems across species. Here, we review some of his work on avian sensory specialists and research that he inspired in others. We begin with an overview of the importance of the Wulst in stereopsis and the need for further study of the Wulst in relation to binocularity across avian species. Next, we summarize recent anatomical, behavioral, and physiological studies on optic flow specializations in hummingbirds. Beyond vision, we discuss the first evidence of a tactile "fovea" in birds and how this led to detailed studies of tactile specializations in waterfowl and sensorimotor systems in parrots. We then describe preliminary studies by Pettigrew of two endemic Australian species, the plains-wanderer (Pedionomus torquatus) and letter-winged kite (Elanus scriptus), that suggest the evolution of some unique auditory and visual specializations in relation to their unique behavior and ecology. Finally, we conclude by emphasizing the importance of a comparative and integrative approach to understanding avian sensory systems and provide an example of one system that has yet to be properly examined: tactile facial bristles in birds. Through reviewing this research and offering future avenues for discovery, we hope that others also embrace the comparative approach to understanding sensory system evolution in birds and other vertebrates.

Neural Code of Motor Planning and Execution during Goal-Directed Movements in Crows

“…Birds such as crows even use elaborate head-beak movements to build and use tools (Weir et al, 2002;Bird and Emery, 2009). Such coordinated actions require acute senses (Iwaniuk and Wylie, 2020), but most of all delicate motor planning and motor execution capabilities (Davies and Green, 1994;Brecht et al, 2019). With the exception of birdsong research, a research area that resulted in detailed knowledge on the neuroanatomy and neurophysiology of song production (Elemans, 2014;Schmidt and Wild, 2014;Murphy et al, 2017;Kersten et al, 2021), and despite the solid understanding of the neuroanatomy of the avian motor system (Dubbeldam, 2000), the neurophysiological mechanisms of motor plans and actions are rarely explored in birds.…”

Endocranial Anatomy of the Giant Extinct Australian Mihirung Birds (Aves, Dromornithidae)

“…That dromornithids have large, forward facing eyes (see Section 4.4.2.1), robust optic nerves (see Section 3.1.2), and enlarged morphology of trigeminal (V) innervation (see Section 4.4.1), further supports our argument that dromornithids were likely diurnal taxa with a strong reliance on stereopsis and trigeminal (V) somatosensory input. These results also suggest that caution is required when deriving functional or behavioural inference from comparisons of optic lobe absolute size, without accounting for the collective morphology of somatosensory "circuits" (e.g., [150] (p. 9)), such as those of the thalamofugal, tectofugal and third visual pathways (see Section 4.4.2).…”

“…Furthermore, stereotyped species-specific behaviour [93,148], pecking accuracy [149], and the processing of visual information such as brightness, colour, and pattern discrimination [118], have been attributed to processes within the caudolateral telencephalon. Pettigrew and Frost [130] showed that the maxillary (V 2 ) division of the trigeminal (V) nerve, which innervates the upper bill (see Section 4.4.1 above), transmits to extensive terminal fields in the region of the rostrodorsal mesopallium (e.g., [150] (Figure 3b), see also [139]). Similarly, Dubbeldam et al [99] showed that ascending maxillary (V 2 ) and mandibular (V 3 ) trigeminal (V) projections transmitted rostrodorsally, via the nucleus basalis, to mesopallial terminal fields [140].…”

“…These sensorimotor and somatosensory projections were related to the "detection" of food particles, particularly in low-visibility feeding in anseriforms [151][152][153][154], and food grasping in columbiforms [140,155] and passeriforms [156]. Located in the caudal telencephalon, the medial spiriform nucleus receives projections from both somatosensory and visual parts of the wulst (see [121]; and Section 4.4.2.1 above), along with arcopallial projections associated with "motor planning information" from the caudoventral telencephalon, and projects to the cerebellum (see Section 4.4.2.4 below), forming the "telencephalic-cerebellar loop" (sensu [150] (p. 9)).…”

“…Hellmann et al [158] (p. 395) characterised the optic lobe as a "relay station" for transmitting ascending visual output to the forebrain (see Section 4.4.2.1 above), projecting descending output to the premotor regions of the hindbrain (see Section 4.4.2.4 below), and comprise multiple "retinotopically organised, and functionally specific" cell types. So called "optic flow" (sensu [159]), are retinal stimuli generated by self-motion through stationary environments (see [150,160] and references therein). Optic flow stimuli are analysed by recipient nuclei in the accessory optic system and pretectum, wherein the lentiformis mesencephali, or pretectal nucleus, responds to "moving large-field" visual stimuli and generates optokinetic response for the control of posture, eye movement stabilisation, and compensatory movement during locomotion ( [117,150,[160][161][162][163][164] and references therein), facilitated by processes within the cerebellum [87,165].…”