Somatosensory activity relevant for motor output. A summary of presentations and discussion

Several aspects of the function of receptors which contribute to somatic sensations are reviewed. First, there is evidence for a role of large-diameter cutaneous afferents in the reflex regulation of precision movements by the hand. Second, large-diameter muscle afferents from the intrinsic muscles of the hand, probably from primary muscle spindle afferents, can evoke specific sensations of finger movement. Third, the variable relationship between discharges in human C fibers from the hand and the specific sensation of pain is investigated. Activity in large-diameter cutaneous afferents can probably modify this sensation. Finally, the properties of small-diameter afferent fibers innervating joints are shown to be consistent with a role in the reflex regulation of joint integrity.     

Nutritional modulation of training-induced skeletal muscle adaptations

Skeletal muscle displays remarkable plasticity, enabling substantial adaptive modifications in its metabolic potential and functional characteristics in response to external stimuli such as mechanical loading and nutrient availability. Contraction-induced adaptations are determined largely by the mode of exercise and the volume, intensity, and frequency of the training stimulus. However, evidence is accumulating that nutrient availability serves as a potent modulator of many acute responses and chronic adaptations to both endurance and resistance exercise. Changes in macronutrient intake rapidly alter the concentration of blood-borne substrates and hormones, causing marked perturbations in the storage profile of skeletal muscle and other insulin-sensitive tissues. In turn, muscle energy status exerts profound effects on resting fuel metabolism and patterns of fuel utilization during exercise as well as acute regulatory processes underlying gene expression and cell signaling. As such, these nutrient-exercise interactions have the potential to activate or inhibit many biochemical pathways with putative roles in training adaptation. This review provides a contemporary perspective of our understanding of the molecular and cellular events that take place in skeletal muscle in response to both endurance and resistance exercise commenced after acute and/or chronic alterations in nutrient availability (carbohydrate, fat, protein, and several antioxidants). Emphasis is on the results of human studies and how nutrient provision (or lack thereof) interacts with specific contractile stimulus to modulate many of the acute responses to exercise, thereby potentially promoting or inhibiting subsequent training adaptation.     

Adaptive plasticity in the spinal stretch reflex: An accessible substrate of memory?

The study of the substrates of memory in higher vertebrates is one of the major problems of neurobiology. A simple and technically accessible experimental model is needed. Recent studies have demonstrated long-term adaptive plasticity, a form of memory, in the spinal stretch reflex (SSR). The SSR is due largely to a two-neuron monosynaptic arc, the simplest, best-defined, and most accessible pathway in the primate central nervous system (CNS). Monkeys can slowly change SSR amplitude without a change in initial muscle length or alpha motoneuron tone, when reward is made contingent on amplitude. Change occurs over weeks and months and persists for long periods. It is relatively specific to the agonist muscle and affects movement. The salient features of SSR adaptive plasticity, combined with clinical and laboratory evidence indicating spinal cord capacity for intrinsic change, suggest that SSR change eventually involves persistent segmental alteration. If this is the case, SSR plasticity should be a powerful model for studying the neuronal and synaptic substrates of memory in a primate.     

Plasticity in the nucleus tractus solitarius and its influence on lung and airway reflexes.

The nucleus tractus solitarius (NTS) is the first central nervous system (CNS) site for synaptic contact of the primary afferent fibers from the lungs and airways. The signal processing at these synapses will determine the output of the sensory information from the lungs and airways to all downstream synapses in the reflex pathways. The second-order NTS neurons bring to bear their own intrinsic and synaptic properties to temporally and spatially integrate the sensory information with inputs from local networks, higher brain regions, and circulating mediators, to orchestrate a coherent reflex output. There is growing evidence that NTS neurons share the rich repertoire of forms of plasticity demonstrated throughout the CNS. This review focuses on existing evidence for plasticity in the NTS, potential targets for plasticity in the NTS, and the impact of this plasticity on lung and airway reflexes.     

Ia presynaptic inhibition in human wrist extensor muscles: effects of motor task and cutaneous afferent activity.

The task-dependence of the presynaptic inhibition of the muscle spindle primary afferents in human forearm muscles was studied, focusing in particular on the modulation associated with the co-contraction of antagonist muscles and the activation of cutaneous afferents. The changes known to affect the motoneuron proprioceptive assistance during antagonist muscle co-activation in human leg and arm muscles were compared. The evidence available so far that these changes might reflect changes in the presynaptic inhibition of the muscle spindle afferent is briefly reviewed. The possible reasons for changes in presynaptic inhibition during the antagonist muscle co-contraction are discussed. Some new experiments on the wrist extensor muscles are briefly described. The results showed that the changes in the Ia presynaptic inhibition occurring during the co-contraction of the wrist flexor and extensor muscles while the hand cutaneous receptors were being activated (the subject's hand was clenched around a manipulandum) could be mimicked by contracting the wrist extensor muscles alone while applying extraneous stimulation to the hand cutaneous receptors. It is concluded that besides the possible contribution of inputs generated by the co-contraction of antagonist muscles and by supraspinal pathways, cutaneous inputs may play a major role in modulating the proprioceptive assistance during manipulatory movements.     

Evolution of adaptive phenotypic traits without positive Darwinian selection

Recent evidence suggests the frequent occurrence of a simple non-Darwinian (but non-Lamarckian) model for the evolution of adaptive phenotypic traits, here entitled the plasticity-relaxation-mutation (PRM) mechanism. This mechanism involves ancestral phenotypic plasticity followed by specialization in one alternative environment and thus the permanent expression of one alternative phenotype. Once this specialization occurs, purifying selection on the molecular basis of other phenotypes is relaxed. Finally, mutations that permanently eliminate the pathways leading to alternative phenotypes can be fixed by genetic drift. Although the generality of the PRM mechanism is at present unknown, I discuss evidence for its widespread occurrence, including the prevalence of exaptations in evolution, evidence that phenotypic plasticity has preceded adaptation in a number of taxa and evidence that adaptive traits have resulted from loss of alternative developmental pathways. The PRM mechanism can easily explain cases of explosive adaptive radiation, as well as recently reported cases of apparent adaptive evolution over ecological time.     

Tremor and other oscillations in neuromuscular systems

A model has been analyzed which is based on recent experimental evidence concerning the properties of muscles and the sensory feedback pathways from muscles. Damped oscillations can arise in the absence of sensory feedback due to the interaction of a muscle with inertial loads. These mechanical oscillations can have a wide range of frequencies depending on the inertial and elastic loads that are attached to the muscle. Small amounts of sensory feedback will tend to reduce deviations from a steady muscle length, but larger amounts of feedback can produce oscillations. The frequency of these reflex oscillations is determined by the properties of the muscle and feedback pathway, and is rather independent of load. If the strength of the sensory feedback is sufficient, either the mechanical oscillations or the reflex oscillations or both can grow, rather than decay, with time. The growth of these oscillations is limited by saturation non-linearities in the muscle receptors and the muscle itself, so that the oscillations approach a steady amplitude and frequency. Using typical properties of muscles and spinal reflex pathways, the frequency of reflex oscillations will be within the range 8–12 Hz found for physiological tremor. With the longer latency found for supraspinal reflexes, oscillations will occur in the range 4–6 Hz which is characteristic of Parkinson's and cerebellar diseases. The role of longer latency reflexes in the generation of these tremors is discussed.     

Changing perspectives on the functional organization of the segmental motor system

Results from a wide variety of recent studies on the architecture and innervation of skeletal muscles, the neuromechanical characteristics of motor units, and the properties and spinal reflex actions of muscle proprioceptors present a number of challenges to conventional views of the functional organization of the segmental motor system. To illustrate the nature of these challenges, studies directed toward several specific issues are reviewed. These include the functional subdivision of single muscles into two or more neuromuscular compartments; the patterns of synaptic input from peripheral afferent fibers to motoneurons innervating muscle units of different "type;" and the convergence in the segmental reflex pathways from muscle spindles and tendon organs to motoneurons.     

Afferent feedback in the control of human gait.

Sensory activity contributes to motor control in two fundamentally different ways. It may mediate 'error signals' following sudden external perturbations and it may contribute to the pre-programmed motoneuronal drive. Here we review data, which illustrate these two functions of sensory feedback in relation to human walking. When ankle plantarflexors are unloaded in the stance phase there is a sudden decrease in the sensory activity in muscle and tendon afferents from the active muscles. This decrease in sensory activity results in a drop in EMG activity recorded from the soleus muscle, which demonstrates that the sensory activity contributes importantly to the activation of the muscles. Data suggests that a spinal pathway from gr. II muscle afferents is responsible for this positive feedback contribution to the motoneuronal drive during walking.When cutaneous nerves from the foot are stimulated in the early swing phase of walking a late reflex response may be observed in the tibialis anterior muscle. This reflex may help to ensure that the foot is lifted effectively over an obstacle. Data suggest that this reflex response is at least partly mediated by a transcortical reflex pathway. It seems to be important that reactions to external perturbations are integrated at a supraspinal level during human walking.     

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation,population viability and genetic variation

An ongoing new synthesis in evolutionary theory is expanding our view of the sources of heritable variation beyond point mutations of fixed phenotypic effects to include environmentally sensitive changes in gene regulation. This expansion of the paradigm is necessary given ample evidence for a heritable ability to alter gene expression in response to environmental cues. In consequence, single genotypes are often capable of adaptively expressing different phenotypes in different environments, i.e. are adaptively plastic. We present an individual-based heuristic model to compare the adaptive dynamics of populations composed of plastic or non-plastic genotypes under a wide range of scenarios where we modify environmental variation, mutation rate and costs of plasticity. The model shows that adaptive plasticity contributes to the maintenance of genetic variation within populations, reduces bottlenecks when facing rapid environmental changes and confers an overall faster rate of adaptation. In fluctuating environments, plasticity is favoured by selection and maintained in the population. However, if the environment stabilizes and costs of plasticity are high, plasticity is reduced by selection, leading to genetic assimilation, which could result in species diversification. More broadly, our model shows that adaptive plasticity is a common consequence of selection under environmental heterogeneity, and hence a potentially common phenomenon in nature. Thus, taking adaptive plasticity into account substantially extends our view of adaptive evolution.     

Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses.

Combined V-wave and Hoffmann (H) reflex measurements were performed during maximal muscle contraction to examine the neural adaptation mechanisms induced by resistance training. The H-reflex can be used to assess the excitability of spinal alpha-motoneurons, while also reflecting transmission efficiency (i.e., presynaptic inhibition) in Ia afferent synapses. Furthermore, the V-wave reflects the overall magnitude of efferent motor output from the alpha-motoneuron pool because of activation from descending central pathways. Fourteen male subjects participated in 14 wk of resistance training that involved heavy weight-lifting exercises for the muscles of the leg. Evoked V-wave, H-reflex, and maximal M-wave (M(max)) responses were recorded before and after training in the soleus muscle during maximal isometric ramp contractions. Maximal isometric, concentric, and eccentric muscle strength was measured by use of isokinetic dynamometry. V-wave amplitude increased approximately 50% with training (P < 0.01) from 3.19 +/- 0.43 to 4.86 +/- 0.43 mV, or from 0.308 +/- 0.048 to 0.478 +/- 0.034 when expressed relative to M(max) (+/- SE). H-reflex amplitude increased approximately 20% (P < 0.05) from 5.37 +/- 0.41 to 6.24 +/- 0.49 mV, or from 0.514 +/- 0.032 to 0.609 +/- 0.025 when normalized to M(max). In contrast, resting H-reflex amplitude remained unchanged with training (0.503 +/- 0.059 vs. 0.499 +/- 0.063). Likewise, no change occurred in M(max) (10.78 +/- 0.86 vs. 10.21 +/- 0.66 mV). Maximal muscle strength increased 23-30% (P < 0.05). In conclusion, increases in evoked V-wave and H-reflex responses were observed during maximal muscle contraction after resistance training. Collectively, the present data suggest that the increase in motoneuronal output induced by resistance training may comprise both supraspinal and spinal adaptation mechanisms (i.e., increased central motor drive, elevated motoneuron excitability, reduced presynaptic inhibition).     

Reflex depression in rhythmically active monosynaptic reflex pathways

A study has been made of the depression that occurs when a monosynaptic reflex pathway is subjected to repetitive stimulation. Reflex depression has a dual origin. High frequency or early depression is postsynaptic in origin and results from subnormality in the motoneurons. Low frequency, late, or enduring depression is presynaptic in origin. The conditioning volley-test volley technique and the frequency-mean monosynaptic reflex amplitude relation yield similar information concerning reflex depression. Each method has its advantages and for some purposes one or the other of the methods necessarily must be employed. The results of a variety of experiments are consistent with the proposition that reflex depression in the monosynaptic reflex pathway originates by action in the group IA afferent fibers of muscle origin that are responsible for monosynaptic reflex transmission. Depression is present at a frequency of 0.1 per second (6 per minute) and absent at a frequency of 0.05 per second (3 per minute). Thus it is impractical for most purposes to employ repetition rates that satisfy the requirement for designation as "single shock" stimulations. The temporal course of enduring depression has been determined. It is identical with that for a number of other phenomena observable in monosynaptic reflex pathways, which suggests a common origin. The mechanism of low frequency or enduring depression is discussed in the light of this suggestion.     

Plasticity of connections underlying locomotor recovery after central and/or peripheral lesions in the adult mammals

This review discusses some aspects of plasticity of connections after spinal injury in adult animal models as a basis for functional recovery of locomotion. After reviewing some pitfalls that must be avoided when claiming functional recovery and the importance of a conceptual framework for the control of locomotion, locomotor recovery after spinal lesions, mainly in cats, is summarized. It is concluded that recovery is partly due to plastic changes within the existing spinal locomotor networks. Locomotor training appears to change the excitability of simple reflex pathways as well as more complex circuitry. The spinal cord possesses an intrinsic capacity to adapt to lesions of central tracts or peripheral nerves but, as a rule, adaptation to lesions entails changes at both spinal and supraspinal levels. A brief summary of the spinal capacity of the rat, mouse and human to express spinal locomotor patterns is given, indicating that the concepts derived mainly from work in the cat extend to other adult mammals. It is hoped that some of the issues presented will help to evaluate how plasticity of existing connections may combine with and potentiate treatments designed to promote regeneration to optimize remaining motor functions.     

Effects of peripheral inputs from hindlimb on the monosynaptic reflex of motoneurons innervating tail muscles.

The effects of group II muscle (PBSt, GS) and cutaneous afferent (Sur, SPc, Tib) inputs from the hindlimb on the monosynaptic reflexes of motoneurons innervating tail muscles were studied in lower spinalized cats. Stimulation of the cutaneous nerves at the conditioning-test stimulus interval of about 10-20 ms facilitated and inhibited the monosynaptic reflexes of ipsilateral and contralateral tail muscles, respectively. The effects of the muscle nerve stimulation were not so prominent as those elicited by cutaneous nerve stimulation. The monosynaptic reflex was also inhibited by muscle nerve stimulation at 10-50 ms intervals. The effects of conditioning stimulation of the hindlimb peripheral nerves at short intervals were depressed or blocked by section of the ipsilateral lateral funiculus at S1 spinal segment. These findings show that the neuronal pathway from hindlimb afferents to tail muscle motoneurons passed the lateral funiculus of the spinal cord and modulates the motoneuronal activity of tail muscles.     

Transmission in fractionated monosynaptic spinal reflex systems

A study has been made of conditions that support monosynaptic reflex transmission from afferent fibers of one part of a synergic muscle mass to motoneurons of another part. Heteronymous response so called can be brought on by prior tetanization of the afferent pathway and by asphyxiation to a critical stage. The response is facilitated by cooling and may appear in the cold preparation without need for prior tetanization. By appropriate asymmetrical subdivision of a monosynaptic reflex system an afferent inflow can be obtained that is sufficiently powerful to secure heteronymous transmission without the need for prior tetanization or cooling. Each junction between a monosynaptic afferent fiber and a motoneuron possesses some degree of potentiality for transmitting. Transmitter potentiality of an afferent fiber at its several junctions with motoneurons varies widely. Reasons are advanced for supposing the variation to be graded rather than stepwise, and quantitative rather than qualitative.     

Phenological plasticity will not help all species adapt to climate change

Concerns are rising about the capacity of species to adapt quickly enough to climate change. In long‐lived organisms such as trees, genetic adaptation is slow, and how much phenotypic plasticity can help them cope with climate change remains largely unknown. Here, we assess whether, where and when phenological plasticity is and will be adaptive in three major European tree species. We use a process‐based species distribution model, parameterized with extensive ecological data, and manipulate plasticity to suppress phenological variations due to interannual, geographical and trend climate variability, under current and projected climatic conditions. We show that phenological plasticity is not always adaptive and mostly affects fitness at the margins of the species' distribution and climatic niche. Under current climatic conditions, phenological plasticity constrains the northern range limit of oak and beech and the southern range limit of pine. Under future climatic conditions, phenological plasticity becomes strongly adaptive towards the trailing edges of beech and oak, but severely constrains the range and niche of pine. Our results call for caution when interpreting geographical variation in trait means as adaptive, and strongly point towards species distribution models explicitly taking phenotypic plasticity into account when forecasting species distribution under climate change scenarios.     

Spinal and supraspinal effects of activity in ligament afferents.

In this paper available knowledge on effects from joint and ligament afferents on spinal neurones and pathways are briefly reviewed, and possible functional implications discussed. Ligament afferents may contribute to joint stability, muscle coordination and proprioception through direct polysynaptic reflex effects onto ascending pathways and skeletomotoneurones, and/or indirectly via reflex actions on the gamma-muscle spindle system. Theoretical and experimental evidence indicate that ligament afferents, together with afferents from other joint structures, muscles and the skin, provide the CNS with information on movements and posture through ensemble coding mechanisms, rather than via modality specific private pathways. The existence and functional relevance of ligamentomuscular protective reflexes, that are triggered when the ligament is threatened by potentially harmful loads, has been seriously questioned. It seems more likely that peripheral sensory inputs from ligament afferents participate in a continuous control of the muscle activity through feedforward, or preprogramming, mechanisms. In line with these ideas it has been suggested that ligament mechanoreceptors have an important role in muscle coordination and in the reflex regulation of the functional joint stability, by contributing to the preprogramming of the muscle stiffness through reflex modulation of the gamma-muscle spindle system.     

Convergence in Reflex Pathways from Multiple Cutaneous Nerves Innervating the Foot Depends upon the Number of Rhythmically Active Limbs during Locomotion

Neural output from the locomotor system for each arm and leg influences the spinal motoneuronal pools directly and indirectly through interneuronal (IN) reflex networks. While well documented in other species, less is known about the functions and features of convergence in common IN reflex system from cutaneous afferents innervating different foot regions during remote arm and leg movement in humans. The purpose of the present study was to use spatial facilitation to examine possible convergence in common reflex pathways during rhythmic locomotor limb movements. Cutaneous reflexes were evoked in ipsilateral tibialis anterior muscle by stimulating (in random order) the sural nerve (SUR), the distal tibial nerve (TIB), and combined simultaneous stimulation of both nerves (TIB&SUR). Reflexes were evoked while participants performed rhythmic stepping and arm swinging movement with both arms and the leg contralateral to stimulation (ARM&LEG), with just arm movement (ARM) and with just contralateral leg movement (LEG). Stimulation intensities were just below threshold for evoking early latency (<80 ms to peak) reflexes. For each stimulus condition, rectified EMG signals were averaged while participants held static contractions in the stationary (stimulated) leg. During ARM&LEG movement, amplitudes of cutaneous reflexes evoked by combined TIB&SUR stimulation were significantly larger than simple mathematical summation of the amplitudes evoked by SUR or TIB alone. Interestingly, this extra facilitation seen during combined nerve stimulation was significantly reduced when performing ARM or LEG compared to ARM&LEG. We conclude that locomotor rhythmic limb movement induces excitation of common IN reflex pathways from cutaneous afferents innervating different foot regions. Importantly, activity in this pathway is most facilitated during ARM&LEG movement. These results suggest that transmission in IN reflex pathways is weighted according to the number of limbs directly engaged in human locomotor activity and underscores the importance of arm swing to support neuronal excitability in leg muscles.