Motor control of birdsong

One of the challenges when considering the motor control of birdsong is to understand how such a wide variety of temporally and spectrally diverse vocalizations are learned and produced. A better understanding of central neural processing, together with direct endoscopic observations and physiological studies of peripheral motor function during singing, has resulted in the formation of new theoretical models of song production. Recent work suggests that it may be more profitable to focus on the temporal relationship between control parameters than to attempt to directly correlate neural processing with details of the acoustic output.     

Peripheral control and lateralization of birdsong

Recent studies on several species of oscine songbirds show that they achieve their varied vocal performances through coordinated activity of respiratory, syringeal, and other vocal tract muscles in ways that take maximum advantage of the acoustic flexibility made possible by the presence of two independently controlled sound sources in their bipartite syrinx (vocal organ). During song, special motor programs to respiratory muscles alter the pattern of ventilation to maintain the supply of respiratory air and oxygen to permit songs of long duration, high syllable repetition rates, or maximum spectral complexity. Each side of the syrinx receives its own motor program that, together with that sent to respiratory muscles, determines the acoustic properties of the ipsilaterally produced sound. The acoustic expression of these bilaterally distinct, phonetic motor patterns depends on the action of dorsal syringeal adductor muscles that, by opening or closing the ipsilateral side of the syrinx to airflow, determine the amount each side contributes to song. The syringeally generated sound is further modified by muscles that control the shape of the vocal tract. Different species have adopted different motor strategies that use the left and right sides of the syrinx in patterns of unilateral, bilateral, alternating, or sequential phonation to achieve the differing temporal and spectral characteristics of their songs. As a result, the degree of song lateralization probably varies between species to form a continuum from unilateral dominance to bilateral equality. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 632–652, 1997     

The neural basis of birdsong

Songbirds represent an excellent model system for understanding the neural mechanisms underlying learning.     

The inverse dynamics problem of neuromuscular control

The myoskeletal inverse dynamics problem and the myocybernetic control inverse problem were investigated with respect to their ill-posedness. The first problem consists of finding from observed experimental motion and reaction force data the resultant muscle moments that generated the observed motion, while the second aims at finding the corresponding neural controls. It is shown that both problems belong to the class of incorrectly posed (ill-posed) problems that, by definition, do not possess unique solutions. To illustrate this point, results of a forward dynamics simulation of a comprehensive neuromusculoskeletal model of the human body are presented. These results demonstrate that fairly chaotic neural control perturbations have very little influence on the resulting motion trajectory, at least in the present example. While a regularization procedure may be applied to solve successfully the myoskeletal inverse dynamics problem, the myocybernetic control inverse problem is unsolvable. The latter fact has the important implication that, based on the somatosensory inputs it receives, the pars intermedia in the cerebellum is not able to control individual motor unit stimulation rates and recruitment patterns but only whole muscles by means of a single compound signal. The latter signal is identified as the “common drive.” Presumably at the spinal level, special neural circuits are used to decompose the common drive signal into motor unit recruitment patterns and stimulation rates that are specific for a given mode of contraction and probably obey certain optimality principles. Received: 26 February 1999 / Accepted in revised form: 11 June 1999     

The evolution of birdsong on islands

Islands are simplified, isolated ecosystems, providing an ideal set‐up to study evolution. Among several traits that are expected to change on islands, an interesting but poorly understood example concerns signals used in animal communication. Islands are typified by reduced species diversity, increased population density, and reduced mate competition, all of which could affect communication signals. We used birdsong to investigate whether there are systematic changes in communication signals on islands, by undertaking a broad comparison based on pairs of closely related island‐mainland species across the globe. We studied song traits related to complexity (number of different syllables, frequency bandwidth), to vocal performance (syllable delivery rate, song duration), and also three particular song elements (rattles, buzzes, and trills) generally implicated in aggressive communication. We also investigated whether song complexity was related to the number of similar sympatric species. We found that island species were less likely to produce broadband and likely aggressive song elements (rattles and buzzes). By contrast, various aspects of song complexity and performance did not differ between island and mainland species. Species with fewer same‐family sympatric species used wider frequency bandwidths, as predicted by the character release hypothesis, both on continents and on islands. Our study supports the hypothesis of a reduction in aggressive behavior on islands and suggests that discrimination against closely related species is an important factor influencing birdsong evolution.     

Simulations of neuromuscular control in lamprey swimming.

The neuronal generation of vertebrate locomotion has been extensively studied in the lamprey. Models at different levels of abstraction are being used to describe this system, from abstract nonlinear oscillators to interconnected model neurons comprising multiple compartments and a Hodgkin-Huxley representation of the most relevant ion channels. To study the role of sensory feedback by simulation, it eventually also becomes necessary to incorporate the mechanical movements in the models. By using simplifying models of muscle activation, body mechanics, counteracting water forces, and sensory feedback through stretch receptors and vestibular organs, we have been able to close the feedback loop to enable studies of the interaction between the neuronal and the mechanical systems. The neuromechanical simulations reveal that the currently known network is sufficient for generating a whole repertoire of swimming patterns. Swimming at different speeds and with different wavelengths, together with the performance of lateral turns can all be achieved by simply varying the brainstem input. The neuronal mechanisms behind pitch and roll manoeuvres are less clear. We have put forward a 'crossed-oscillators' hypothesis where partly separate dorsal and ventral circuits are postulated. Neuromechanical simulations of this system show that it is also capable of generating realistic pitch turns and rolls, and that vestibular signals can stabilize the posture during swimming.     

The escape of Tritonia: dynamics of a neuromuscular control mechanism.

The results of photosynthesis experiments with ¹⁸O labelled water and carbon dioxide are commonly regarded as the strongest arguments for a light-induced water oxidation. In these experiments, however, several sources of error have not been adequately considered. The peculiarities of natural H₂OCO₂ mixtures and their enzymatically enhanced equilibration are discussed. The unequal distribution of the oxygen isotopes is considered. Relevant data are presented on the CO₂ storage in green plant cells and the oxygen burst which is often observed during the beginning of the light period. After the statement of the necessary precautions for isotope experiments data of former measurements of the oxygen isotope discrimination by photosynthetic and respiratory processes are discussed. The data laid down in the literature together with the results of some experiments with deuterated water are taken as disproof of the hypothesis of water oxidation.     

Predictive algorithms for neuromuscular control of human locomotion.

The problem of quantifying muscular activity of the human body can be formulated as an optimal control problem. The current methods used with large-scale biomechanical systems are non-derivative techniques. These methods are costly, as they require numerous integrations of the equations of motion. Additionally, the convergence is slow, making them impractical for use with large systems. We apply an efficient numerical algorithm to the biomechanical optimal control problem. Using direct collocation with a trapezoidal discretization, the equations of motion are converted into a set of algebraic constraint equations. An augmented Lagrangian formulation is used for the optimization problem to handle both equality and inequality constraints. The resulting min-max problem is solved with a generalized Newton method. In contrast to the prevalent optimal control implementations, we calculate analytical first- and second-derivative information and obtain local quadratic convergence. To demonstrate the efficacy of the method, we solve a steady-state pedaling problem with 7 segments and 18 independent muscle groups. The computed muscle activations compare well with experimental EMG data. The computational effort is significantly reduced and solution times are a fraction of those of the non-derivative techniques.     

Muscle mechanics and neuromuscular control

The purpose of this paper is to demonstrate that the properties of the mechanical system, especially muscle elasticity and limb mass, to a large degree determine force output and movement. This makes the control demands of the central nervous system simpler and more robust. In human triceps surae, a muscle with short fibres and a long tendon, the time courses of the total muscle+tendon length and of the length of the contractile component (CC) alone in running are completely different. The muscle tendon complex shows first an eccentric phase with negative work, followed by a concentric phase. The CC, on the other hand, is concentric all the time. Moreover, the work that is done, is done at a speed that guarantees a high energetic efficiency. It is argued that this high efficiency is an in-built property of the muscle mechanics for muscles with a compliant tendon and a low v(max). When a muscle, or a set of muscles, moves a mass, and the duration of the action is short with respect to the isometric time constant of the muscle, we may call it an 'elastic bounce contraction'. In such a case the mass-spring interaction largely determines the time course of the force, and the efficiency of muscle contraction is most of the time close to optimum. In a similar way, whole limbs can be modelled as springs, with a stiffness that can be modulated by flexing the joints more or less. The motor control task of the central nervous system is simple for such elastic bounce contractions: a block-like activation is sufficient, in which timing is critical, but activation level is not. It seems possible that a whole class of actions can be generated by an identical timing sequence, with only a modulation in activation amplitude. An example is walking or running at different speeds.     

Neural mechanisms of birdsong memory

The process through which young male songbirds learn the characteristics of the songs of an adult male of their own species has strong similarities with speech acquisition in human infants. Both involve two phases: a period of auditory memorization followed by a period during which the individual develops its own vocalizations. The avian 'song system', a network of brain nuclei, is the probable neural substrate for the second phase of sensorimotor learning. By contrast, the neural representation of song memory acquired in the first phase is localized outside the song system, in different regions of the avian equivalent of the human auditory association cortex.     

Direct corticospinal pathways contribute to neuromuscular control of perturbed stance.

The antigravity soleus muscle (Sol) is crucial for compensation of stance perturbation. A corticospinal contribution to the compensatory response of the Sol is under debate. The present study assessed spinal, corticospinal, and cortical excitability at the peaks of short- (SLR), medium- (MLR), and long-latency responses (LLR) after posterior translation of the feet. Transcranial magnetic stimulation (TMS) and peripheral nerve stimulation were individually adjusted so that the peaks of either motor evoked potential (MEP) or H reflex coincided with peaks of SLR, MLR, and LLR, respectively. The influence of specific, presumably direct, corticospinal pathways was investigated by H-reflex conditioning. When TMS was triggered so that the MEP arrived in the Sol at the same time as the peaks of SLR and MLR, EMG remained unaffected. Enhanced EMG was observed when the MEP coincided with the LLR peak (P < 0.001). Similarly, conditioning of the H reflex by subthreshold TMS facilitated H reflexes only at LLR (P < 0.001). The earliest facilitation after perturbation occurred after 86 ms. The TMS-induced H-reflex facilitation at LLR suggests that increased cortical excitability contributes to the augmentation of the LLR peaks. This provides evidence that the LLR in the Sol muscle is at least partly transcortical, involving direct corticospinal pathways. Additionally, these results demonstrate that approximately 86 ms after perturbation, postural compensatory responses are cortically mediated.     

Effect of sex hormones on neuromuscular control patterns during landing.

The purpose of the study was to investigate the effects of sex hormones across menstrual cycle phases on lower extremity neuromuscular control patterns during the landing phase of a drop jump. A repeated-measures design was utilized to examine sex hormone effects in 26 recreationally active eumenorrheic women. Varus/valgus knee angle and EMG activity from six lower extremity muscles were recorded during three drop jumps from a 50 cm platform in each phase of the menstrual cycle. Blood assays verified sex hormone levels and cycle phase. The semitendinosus muscle exhibited onset delays (p0.006) relative to ground contact during the luteal phase, and demonstrated a significant (p0.05) difference between early and late follicular phases. Muscle timing differences between the gluteus maximus and semitendinosus were decreased (p0.05) in the luteal compared to early follicular phases. These results suggest a different co-contractive behavior between the gluteus maximus and semitendinosus, signifying a shift in neuromuscular control patterns. It appears that female recreational athletes utilize a different neuromuscular control pattern for performing a drop jump sequence when estrogen levels are high (luteal phase) compared to when they are low (early follicular phase).     

Neurotrophic control of 16S acetylcholinesterase at the vertebrate neuromuscular junction.

Endplate 16S acetylcholinesterase (16S-AChE) from rat anterior gracilis muscle was assessed, 6 hr to 10 days after denervation, by velocity sedimentation analysis on linear sucrose gradients. The innervating obturator nerve was transected either close (1--2 mm, short stump) or far (35--40 mm, long stump) from the muscle. In both instances, the activity of 16S-AChE gradually decreased and reached approximately the same level (10%--20% of control) by 6 days after denervation. However, enzymatic decay started considerably earlier in short stump (12--24 hr) as compared to long stump (4--5 days preparations, i.e., the time of onset of 16S-AChE loss depended on the length of nerve that remained attached to the muscle. Whether this result extended to other AChE molecular forms (10S, 4S) in muscle endplates could not be determined because, in contrast to 16S-AChE, these forms were also detected in red blood cells (4S) and plasma (10S). Only small amounts of 16S-AChE were found in intact obturator nerves (1/100 of that in gracilis endplate regions). Thus a faster depletion of enzyme from shorter nerve stumps after axotomy could not entirely account for the substantial effect of nerve stump length on 16S-AChE. Since muscle contraction ceases immediately following nerve transection, regardless of nerve stump length, the results can be ascribed to the lack of some neural influence other than nerve-evoked muscle activity. The present findings are consistent with the view that maintenance of 16SAChE at neuromuscular junctions primarily depends on regulatory substances which are conveyed by axonal transport and released from nerve terminals.     

Sleep, learning, and birdsong

Neuroethological research combines approaches derived from animal behavior and neurobiology to examine the neuronal mechanisms of behavior, often in the context of laboratory experiments on species chosen for particular adaptations. Typically, these species are not traditional laboratory animals yet they contribute greatly to a broad, evolutionarily diverse view of nervous system function. The surprising role of sleep in the vocal learning process of songbirds is one such example, described here. Juvenile zebra finches show sleep-dependent daytime fluctuations in their patterns of singing starting after their first exposure to tutor songs. Nighttime bursting activity in the vocal control song system also changes after the onset of tutoring, with the neuronal changes preceding the changes in objective behavior (daytime singing). After tutoring, the nighttime bursting increases and exhibits structure that depends on the particular tutor song, and the nighttime expression of these changes requires normal auditory feedback during daytime singing. These observations shed light on the information carried in neuronal activity during sleep and on the adaptive plastic mechanisms engaged during sleep. They suggest a new hypothesis of sensorimotor learning, whereby sensory memories act indirectly on sensorimotor feedback by modifying networks through plastic changes at night. Sleep may also contribute to adult song maintenance, with nighttime neuronal replay conveying information about songs produced during the day and possibly mediating daily changes in the structure of premotor bursts. Collectively, these insights contribute a comparative perspective to theories of sleep and memory, which also help to inform a developing understanding of how humans acquire and retain memories.