J. Martin Wild

Neural pathways for the control of birdsong production

As in humans, song production in birds involves the intricate coordination of at least three major groups of muscles: namely, those of the syrinx, the respiratory apparatus, and the upper vocal tract, including the jaw. The pathway in songbirds that controls the syrinx originates in the telencephalon and projects via the occipitomesencephalic tract directly upon vocal motoneurons in the medulla. Activity in this pathway configures the syrinx into phonatory positions for the production of species typical vocalizations. Another component of this pathway mediates control of respiration during vocalization, since it projects upon both expiratory and inspiratory groups of premotor neurons in the ventrolateral medulla, as well as upon several other nuclei en route. This pathway appears to be primarily involved with the control of the temporal pattern of song, but is also importantly involved in the control of vocal intensity, mediated via air sac pressure. There are extensive interconnections between the vocal and respiratory pathways, especially at brain-stem levels, and it may be these that ensure the necessary temporal coordination of syringeal and respiratory activity. The pathway mediating control of the jaw appears to be different from those mediating control of the syrinx and respiratory muscles. It originates in a different part of the archistriatum and projects upon premotor neurons in the medulla that appear to be separate from those projecting upon the syringeal motor nucleus. The separateness of this pathway may reflect the imperfect correlation of jaw movements with the dynamic and acoustic features of song. The brainstem pathways mediating control of vocalization and respiration in songbirds have distinct similarities to those in mammals such as cats and monkeys. However, songbirds, like humans, but unlike most other non-songbirds, have developed a telencephalic vocal control system for the production of learned vocalizations.

Magnetoreception and its trigeminal mediation in the homing pigeon

Two conflicting hypotheses compete to explain how a homing pigeon can return to its loft over great distances. One proposes the use of atmospheric odours and the other the Earths magnetic field in the ‘map’ step of the ‘map and compass’ hypothesis of pigeon homing. Although magnetic effects on pigeon orientation provide indirect evidence for a magnetic ‘map’, numerous conditioning experiments have failed to demonstrate reproducible responses to magnetic fields by pigeons. This has led to suggestions that homing pigeons and other birds have no useful sensitivity to the Earths magnetic field. Here we demonstrate that homing pigeons (Columba livia) can discriminate between the presence and absence of a magnetic anomaly in a conditioned choice experiment. This discrimination is impaired by attachment of a magnet to the cere, local anaesthesia of the upper beak area, and bilateral section of the ophthalmic branch of the trigeminal nerve, but not of the olfactory nerve. These results suggest that magnetoreception (probably magnetite-based) occurs in the upper beak area of the pigeon. Traditional methods of rendering pigeons anosmic might therefore cause simultaneous impairment of magnetoreception so that future orientation experiments will require independent evaluation of the pigeons magnetic and olfactory systems.

Visual but not trigeminal mediation of magnetic compass information in a migratory bird.

Magnetic compass information has a key role in bird orientation, but the physiological mechanisms enabling birds to sense the Earth’s magnetic field remain one of the unresolved mysteries in biology. Two biophysical mechanisms have become established as the most promising magnetodetection candidates. The iron-mineral-based hypothesis suggests that magnetic information is detected by magnetoreceptors in the upper beak and transmitted through the ophthalmic branch of the trigeminal nerve to the brain. The light-dependent hypothesis suggests that magnetic field direction is sensed by radical pair-forming photopigments in the eyes and that this visual signal is processed in cluster N, a specialized, night-time active, light-processing forebrain region. Here we report that European robins with bilateral lesions of cluster N are unable to show oriented magnetic-compass-guided behaviour but are able to perform sun compass and star compass orientation behaviour. In contrast, bilateral section of the ophthalmic branch of the trigeminal nerve in European robins did not influence the birds’ ability to use their magnetic compass for orientation. These data show that cluster N is required for magnetic compass orientation in this species and indicate that it may be specifically involved in processing of magnetic compass information. Furthermore, the data strongly suggest that a vision-mediated mechanism underlies the magnetic compass in this migratory songbird, and that the putative iron-mineral-based receptors in the upper beak connected to the brain by the trigeminal nerve are neither necessary nor sufficient for magnetic compass orientation in European robins.

The avian nucleus retroambigualis: a nucleus for breathing, singing and calling

Nucleus retroambigualis in songbirds and pigeon was found to contain expiratory-related neurons having spinal projections with terminations in close proximity to abdominal expiratory motoneurons. It was also shown to receive projections from the dorsomedial nucleus (DM) of the intercollicular complex and, in songbirds, from the nucleus robustus archistriatalis (nRbA) of the telencephalon. Nucleus retroambigualis is thus an important nexus in the final common pathway for respiration and vocalization.

The avian somatosensory system: connections of regions of body representation in the forebrain of the pigeon

In order to establish the basic connectivity of physiologically identified somatosensory regions of the thalamus and telencephalon in the pigeon, injections of wheatgerm agglutinin-horseradish peroxidase were made under electrophysiological control and the projections were charted following conventional neurohistochemistry. The physiological recordings generally confirmed the findings of Delius and Bennetto (Brain Research, 37 (1972) 205-221) of somatosensory sites within the dorsal thalamus, anterior hyperstriatum and caudomedial neostriatum, and the anatomical results show that the thalamic cells of origin of the projections to the two telencephalic regions are largely separate: a rostral cell group comprising nucleus dorsalis intermedius ventralis anterior projects to the anterior hyperstriatum accessorium (HA), whilst a caudal cell group comprising caudal regions of nucleus dorsolateralis posterior (DLP) projects to the medial neostriatum intermedium and caudale (NI/NC). Caudal DLP is also the origin of a visual projection to NI/NC, and its terminal field also approximates that of the thalamic auditory nucleus ovoidalis. Since the anterior HA and NI/NC were here shown to be reciprocally connected, there is a possibility of multimodal input to both telencephalic regions. HA was also further defined as the origin of the basal branch of the septomesencephalic tract, and hence potentially provides an outlet for both telencephalic somatosensory regions. The results are discussed within a comparative context.

Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions.

The organization of the pigeon hippocampal formation was examined by tract tracing by using biotinylated dextran amine (BDA) and cholera toxin B subunit (CTB) and by injections of kainic acid to produce excitotoxic lesions. The hippocampal formation was divided into seven subdivisions based on Nissl staining and intrinsic and septal connections: dorsomedial (DM), dorsolateral (DL), triangular (Tr), V‐shaped layer, magnocellular (Ma), parvocellular, and cell‐poor regions. DL was composed of dorsal and ventral portions and sent associational fibers to DM, the V‐shaped layer, and Tr. DL had strong reciprocal connections with the densocellular part of the hyperpallium (HD) and projected to the dorsolateral corticoid area. DM had reciprocal fiber connections with the V‐shaped layer, Ma, and DL as well as with several subdivisions of the arcopallium. DL and DM, but not the V‐shaped layer, projected fibers to the septum where those from DM exceeded in number those from DL. These projections further extended to the hypothalamus, particularly the lateral hypothalamic area. The lateral and medial septal nuclei projected back a very small number of ascending fibers to the hippocampal formation. Intraventricular injections of kainic acid induced neuronal loss widely in the hippocampal formation and subsequently produced gliosis in DM. These results indicate that DL receives its main afferents from HD and in turn sends inputs to an intrinsic circuit composed of hippocampal subdivisions DM, Ma, Tr, and the V‐shaped layer; and also that DM is the main exit to the septum and hypothalamus. It is suggested that neurons in the V‐shaped layer are intrinsic. Together, the results suggest that the V‐shaped layer is comparable to the dentate gyrus of the mammalian hippocampal formation and that DM incorporates components comparable to both Ammons horn and the subiculum. J. Comp. Neurol. 475:426–461, 2004.

Brainstem and Forebrain Contributions to the Generation of Learned Motor Behaviors for Song

Brainstem nuclei have well established roles in generating nonlearned rhythmic behaviors or as output pathways for more complex, forebrain-generated behaviors. However, the role of the brainstem in providing information to the forebrain that is used to initiate or assist in the control of complex behaviors is poorly understood. In this study, we used electrical microstimulation in select nuclei of the avian song system combined with recordings of acoustic and respiratory output to examine how forebrain and brainstem nuclei interact in the generation of learned vocal motor sequences. We found that brief stimulation in the forebrain nuclei HVC (used as a proper name) and RA (robust nucleus of the arcopallium) caused a short-latency truncation of ongoing song syllables, which ultimately led to a cessation of the ongoing motor sequence. Stimulation within the brainstem inspiratory-related nucleus paraambigualis, which receives input from RA and projects back to HVC via the thalamus, caused syllable truncations and interruptions similar to those observed in HVC and RA. In contrast, stimulation in the tracheosyringal portion of the hypoglossal nucleus, which innervates the syrinx (the avian vocal organ) but possesses no known projections back into the song system, did not cause any significant changes in the song motor pattern. These findings suggest that perturbation of premotor activity in any nucleus within the recurrent song system motor network will disrupt the ongoing song motor sequence. Given the anatomical organization of this network, our results are consistent with a model in which the brainstem respiratory nuclei form an integral part of the song motor programming network by providing timing signals to song control nuclei in the forebrain.

Functional neuroanatomy of the sensorimotor control of singing.

Abstract: Reviews of the songbird vocal control system frequently begin by describing the forebrain nuclei and pathways that form anterior and posterior circuits involved in song learning and song production, respectively. They then describe extratelencephalic projections upon the brainstem respiratory‐vocal system in a manner suggesting, quite erroneously, that this system is itself well understood. One aim of this chapter is to demonstrate how limited is our understanding of that system. I begin with an overview of the neural network for the motor control of song production, with a particular emphasis on brainstem structures, including the tracheosyringeal motor nucleus (XIIts), which innervates the syrinx, and nucleus retroambigualis (RAm), which projects upon XIIts and upon spinal motor neurons innervating expiratory muscles. I describe the sources of afferent projections to XIIts and RAm and discuss their probable role in coordinating the bilateral activity of respiratory and syringeal muscles during singing. I then consider the routes by which sensory feedback, which could arise from numerous structures involved in singing, might access the song system to guide song learning, maintain accurate song production, and inform the song system of the requirements for air. I describe possible routes of access of auditory feedback, which is known to be necessary for song learning and maintenance, and identify potential sites of interaction with somatosensory and visceral feedback that could arise from the syrinx, the lungs and air sacs, and the upper vocal tract, including the jaw. I conclude that the incorporation of brainstem‐based respiratory‐vocal variables is likely to be a necessary next step in the construction of more sophisticated models of the control of vocalization.

Intratelencephalic connections of the hippocampus in pigeons (Columba livia)

Behavioral experiments using ablation of the hippocampus are increasingly being used to address the hypothesis that the avian hippocampus plays a role in memory, as in mammals. However, the morphological basis of the avian hippocampus has been poorly understood. In the present study, the afferent and efferent connections of the hippocampus in the pigeon telencephalon were defined by injections, at various rostrocaudal sites, of neuronal tracers mainly into the triangular part located between its V‐shaped layer of densely packed neurons. The major results obtained in the present study were as follows. 1) A topographical organization of the commissural projections was confirmed. These projections had two courses that projected to the contralateral side, one traveling through the fiber wall of the ventromedial telencephalon, which was the main path from neurons in the caudal hippocampus, and the other running down through the septohippocampal junction, which was the main path from neurons in the middle to rostral hippocampus. Both courses passed through the pallial commissure. 2) The hippocampus projected bilaterally to the septum, parahippocampal area (APH), and dorsolateral cortical area (CDL). These projections were also distributed topographically, with contralateral efferents crossing through the pallial commissure. 3) The hippocampus had ipsilateral reciprocal connections with APH, CDL, and the dorsal hyperstriatum. Septal afferents to the ipsilateral hippocampus were very small. 4) Intrinsic connections were found between the triangular part of the hippocampus and the lateral limb of the V‐shaped layer of neurons. 5) The hippocampus projected ipsilaterally to the ventral basal ganglia and the fasciculus diagonalis Brocae. In sum, these connections of the hippocampus may form a neuronal circuit for the processing of spatial memory in pigeons. J. Comp. Neurol. 447:177–199, 2002.

Calcium-binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata).

Nucleus HVC of the avian song system is essential to song patterning and is a prime site for auditory–vocal integration important to vocal learning. These processes require precise, high‐frequency action potential activity, which, in other systems, is often correlated with the expression of calcium‐binding proteins. To characterize any such functional specializations in HVC, we retrogradely labeled projection neurons innervating HVCs known targets, namely, area X or nucleus robustus arcopallialis (RA), then stained HVC sections with antibodies to the calcium‐binding proteins parvalbumin, calbindin, and calretinin. Under epifluorescent illumination, neither projection neuron type exhibited detectable levels of calcium‐binding protein immunoreactivity, whereas a third cell type, made up of nonprojection neurons (interneurons), was immunopositive for one, two, or all three of the calcium‐binding proteins. In fact, most of these interneurons were either doubly or triply labeled. To explore the link between the electrical and calcium‐binding protein properties of individual HVC neurons, we used intracellular methods in brain slices to record from identified HVC cell types based on their intrinsic electrical properties. Intracellular neurobiotin combined with immunostaining revealed that fast‐spiking interneurons, but not the slower‐spiking projection neurons, were positive for one or more calcium‐binding proteins. Confocal microscopy confirmed these results and also revealed that RA‐projecting cells might contain very low levels of parvalbumin. These results indicate that HVC interneurons are specialized in their calcium‐binding proteins and suggest how it might be possible to resolve the details of HVC microcircuits underlying song selectivity and auditory–vocal learning. J. Comp. Neurol. 483:76–90, 2005.