scholarly journals Asymmetric and transient properties of reciprocal activity of antagonists during the paw-shake response in the cat

2021 ◽  
Vol 17 (12) ◽  
pp. e1009677
Author(s):  
Jessica R. Parker ◽  
Alexander N. Klishko ◽  
Boris I. Prilutsky ◽  
Gennady S. Cymbalyuk

Mutually inhibitory populations of neurons, half-center oscillators (HCOs), are commonly involved in the dynamics of the central pattern generators (CPGs) driving various rhythmic movements. Previously, we developed a multifunctional, multistable symmetric HCO model which produced slow locomotor-like and fast paw-shake-like activity patterns. Here, we describe asymmetric features of paw-shake responses in a symmetric HCO model and test these predictions experimentally. We considered bursting properties of the two model half-centers during transient paw-shake-like responses to short perturbations during locomotor-like activity. We found that when a current pulse was applied during the spiking phase of one half-center, let’s call it #1, the consecutive burst durations (BDs) of that half-center increased throughout the paw-shake response, while BDs of the other half-center, let’s call it #2, only changed slightly. In contrast, the consecutive interburst intervals (IBIs) of half-center #1 changed little, while IBIs of half-center #2 increased. We demonstrated that this asymmetry between the half-centers depends on the phase of the locomotor-like rhythm at which the perturbation was applied. We suggest that the fast transient response reflects functional asymmetries of slow processes that underly the locomotor-like pattern; e.g., asymmetric levels of inactivation across the two half-centers for a slowly inactivating inward current. We compared model results with those of in-vivo paw-shake responses evoked in locomoting cats and found similar asymmetries. Electromyographic (EMG) BDs of anterior hindlimb muscles with flexor-related activity increased in consecutive paw-shake cycles, while BD of posterior muscles with extensor-related activity did not change, and vice versa for IBIs of anterior flexors and posterior extensors. We conclude that EMG activity patterns during paw-shaking are consistent with the proposed mechanism producing transient paw-shake-like bursting patterns found in our multistable HCO model. We suggest that the described asymmetry of paw-shaking responses could implicate a multifunctional CPG controlling both locomotion and paw-shaking.

2007 ◽  
Vol 97 (3) ◽  
pp. 2148-2158 ◽  
Author(s):  
Nathan P. Cramer ◽  
Ying Li ◽  
Asaf Keller

Using the rat vibrissa system, we provide evidence for a novel mechanism for the generation of movement. Like other central pattern generators (CPGs) that underlie many movements, the rhythm generator for whisking can operate without cortical inputs or sensory feedback. However, unlike conventional mammalian CPGs, vibrissa motoneurons (vMNs) actively participate in the rhythmogenesis by converting tonic serotonergic inputs into the patterned motor output responsible for movement of the vibrissae. We find that, in vitro, a serotonin receptor agonist, α-Me-5HT, facilitates a persistent inward current (PIC) and evokes rhythmic firing in vMNs. Within each motoneuron, increasing the concentration of α-Me-5HT significantly increases the both the magnitude of the PIC and the motoneuron's firing rate. Riluzole, which selectively suppresses the Na+ component of PICs at low concentrations, causes a reduction in both of these phenomena. The magnitude of this reduction is directly correlated with the concentration of riluzole. The joint effects of riluzole on PIC magnitude and firing rate in vMNs suggest that the two are causally related. In vivo we find that the tonic activity of putative serotonergic premotoneurons is positively correlated with the frequency of whisking evoked by cortical stimulation. Taken together, these results support the hypothesized novel mammalian mechanism for movement generation in the vibrissa motor system where vMNs actively participate in the rhythmogenesis in response to tonic drive from serotonergic premotoneurons.


2016 ◽  
Vol 371 (1685) ◽  
pp. 20150057 ◽  
Author(s):  
Paul S. Katz

Comparisons of rhythmic movements and the central pattern generators (CPGs) that control them uncover principles about the evolution of behaviour and neural circuits. Over the course of evolutionary history, gradual evolution of behaviours and their neural circuitry within any lineage of animals has been a predominant occurrence. Small changes in gene regulation can lead to divergence of circuit organization and corresponding changes in behaviour. However, some behavioural divergence has resulted from large-scale rewiring of the neural network. Divergence of CPG circuits has also occurred without a corresponding change in behaviour. When analogous rhythmic behaviours have evolved independently, it has generally been with different neural mechanisms. Repeated evolution of particular rhythmic behaviours has occurred within some lineages due to parallel evolution or latent CPGs. Particular motor pattern generating mechanisms have also evolved independently in separate lineages. The evolution of CPGs and rhythmic behaviours shows that although most behaviours and neural circuits are highly conserved, the nature of the behaviour does not dictate the neural mechanism and that the presence of homologous neural components does not determine the behaviour. This suggests that although behaviour is generated by neural circuits, natural selection can act separately on these two levels of biological organization.


2019 ◽  
Vol 30 (2) ◽  
pp. 107-164 ◽  
Author(s):  
Inge Steuer ◽  
Pierre A. Guertin

AbstractCentral pattern generators (CPGs) are generally defined as networks of neurons capable of enabling the production of central commands, specifically controlling stereotyped, rhythmic motor behaviors. Several CPGs localized in brainstem and spinal cord areas have been shown to underlie the expression of complex behaviors such as deglutition, mastication, respiration, defecation, micturition, ejaculation, and locomotion. Their pivotal roles have clearly been demonstrated although their organization and cellular properties remain incompletely characterized. In recent years, insightful findings about CPGs have been made mainly because (1) several complementary animal models were developed; (2) these models enabled a wide variety of techniques to be used and, hence, a plethora of characteristics to be discovered; and (3) organizations, functions, and cell properties across all models and species studied thus far were generally found to be well-preserved phylogenetically. This article aims at providing an overview for non-experts of the most important findings made on CPGs inin vivoanimal models,in vitropreparations from invertebrate and vertebrate species as well as in primates. Data about CPG functions, adaptation, organization, and cellular properties will be summarized with a special attention paid to the network for locomotion given its advanced level of characterization compared with some of the other CPGs. Similarities and differences between these networks will also be highlighted.


2008 ◽  
Vol 100 (5) ◽  
pp. 2819-2824 ◽  
Author(s):  
Olivier White ◽  
Yannick Bleyenheuft ◽  
Renaud Ronsse ◽  
Allan M. Smith ◽  
Jean-Louis Thonnard ◽  
...  

In many nonprimate species, rhythmic patterns of activity such as locomotion or respiration are generated by neural networks at the spinal level. These neural networks are called central pattern generators (CPGs). Under normal gravitational conditions, the energy efficiency and the robustness of human rhythmic movements are due to the ability of CPGs to drive the system at a pace close to its resonant frequency. This property can be compared with oscillators running at resonant frequency, for which the energy is optimally exchanged with the environment. However, the ability of the CPG to adapt the frequency of rhythmic movements to new gravitational conditions has never been studied. We show here that the frequency of a rhythmic movement of the upper limb is systematically influenced by the different gravitational conditions created in parabolic flight. The period of the arm movement is shortened with increasing gravity levels. In weightlessness, however, the period is more dependent on instructions given to the participants, suggesting a decreased influence of resonant frequency. Our results are in agreement with a computational model of a CPG coupled to a simple pendulum under the control of gravity. We demonstrate that the innate modulation of rhythmic movements by CPGs is highly flexible across gravitational contexts. This further supports the involvement of CPG mechanisms in the achievement of efficient rhythmic arm movements. Our contribution is of major interest for the study of human rhythmic activities, both in a normal Earth environment and during microgravity conditions in space.


2017 ◽  
Vol 118 (6) ◽  
pp. 2956-2974 ◽  
Author(s):  
Lea Ziskind-Conhaim ◽  
Shawn Hochman

Mapping the expression of transcription factors in the mouse spinal cord has identified ten progenitor domains, four of which are cardinal classes of molecularly defined, ventrally located interneurons that are integrated in the locomotor circuitry. This review focuses on the properties of these interneuronal populations and their contribution to hindlimb locomotor central pattern generation. Interneuronal populations are categorized based on their excitatory or inhibitory functions and their axonal projections as predictors of their role in locomotor rhythm generation and coordination. The synaptic connectivity and functions of these interneurons in the locomotor central pattern generators (CPGs) have been assessed by correlating their activity patterns with motor output responses to rhythmogenic neurochemicals and sensory and descending fibers stimulations as well as analyzing kinematic gait patterns in adult mice. The observed complex organization of interneurons in the locomotor CPG circuitry, some with seemingly similar physiological functions, reflects the intricate repertoire associated with mammalian motor control and is consistent with high transcriptional heterogeneity arising from cardinal interneuronal classes. This review discusses insights derived from recent studies to describe innovative approaches and limitations in experimental model systems and to identify missing links in current investigational enterprise.


2020 ◽  
Vol 10 (4) ◽  
pp. 215
Author(s):  
Ross Howard Sanders ◽  
Daniel J. Levitin

How does the human neurophysiological system self-organize to achieve optimal phase relationships among joints and limbs, such as in the composite rhythms of butterfly and front crawl swimming, drumming, or dancing? We conducted a systematic review of literature relating to central nervous system (CNS) control of phase among joint/limbs in continuous rhythmic activities. SCOPUS and Web of Science were searched using keywords “Phase AND Rhythm AND Coordination”. This yielded 1039 matches from which 23 papers were extracted for inclusion based on screening criteria. The empirical evidence arising from in-vivo, fictive, in-vitro, and modelling of neural control in humans, other species, and robots indicates that the control of movement is facilitated and simplified by innervating muscle synergies by way of spinal central pattern generators (CPGs). These typically behave like oscillators enabling stable repetition across cycles of movements. This approach provides a foundation to guide the design of empirical research in human swimming and other limb independent activities. For example, future research could be conducted to explore whether the Saltiel two-layer CPG model to explain locomotion in cats might also explain the complex relationships among the cyclical motions in human swimming.


2002 ◽  
Vol 82 (1) ◽  
pp. 69-83 ◽  
Author(s):  
Marilyn MacKay-Lyons

Abstract Neural networks in the spinal cord, referred to as “central pattern generators” (CPGs), are capable of producing rhythmic movements, such as swimming, walking, and hopping, even when isolated from the brain and sensory inputs. This article reviews the evidence for CPGs governing locomotion and addresses other factors, including supraspinal, sensory, and neuromodulatory influences, that interact with CPGs to shape the final motor output. Supraspinal inputs play a major role not only in initiating locomotion but also in adapting the locomotor pattern to environmental and motivational conditions. Sensory afferents involved in muscle and cutaneous reflexes have important regulatory functions in preserving balance and ensuring stable phase transitions in the locomotor cycle. Neuromodulators evoke changes in cellular and synaptic properties of CPG neurons, conferring flexibility to CPG circuits. Briefly addressed is the interaction of CPG networks to produce intersegmental coordination for locomotion. Evidence for CPGs in humans is reviewed, and although a comprehensive clinical review is not an objective, examples are provided of animal and human studies that apply knowledge of CPG mechanisms to improve locomotion. The final section deals with future directions in CPG research.


2009 ◽  
Vol 21 (5) ◽  
pp. 1335-1370 ◽  
Author(s):  
Renaud Ronsse ◽  
Dagmar Sternad ◽  
Philippe Lefèvre

Current research on discrete and rhythmic movements differs in both experimental procedures and theory, despite the ubiquitous overlap between discrete and rhythmic components in everyday behaviors. Models of rhythmic movements usually use oscillatory systems mimicking central pattern generators (CPGs). In contrast, models of discrete movements often employ optimization principles, thereby reflecting the higher-level cortical resources involved in the generation of such movements. This letter proposes a unified model for the generation of both rhythmic and discrete movements. We show that a physiologically motivated model of a CPG can not only generate simple rhythmic movements with only a small set of parameters, but can also produce discrete movements if the CPG is fed with an exponentially decaying phasic input. We further show that a particular coupling between two of these units can reproduce main findings on in-phase and antiphase stability. Finally, we propose an integrated model of combined rhythmic and discrete movements for the two hands. These movement classes are sequentially addressed in this letter with increasing model complexity. The model variations are discussed in relation to the degree of recruitment of the higher-level cortical resources, necessary for such movements.


1999 ◽  
Vol 82 (6) ◽  
pp. 3392-3405 ◽  
Author(s):  
G. E. Loeb

The mechanical actions of various ankle muscles were changed by surgically crossing or transferring the tendons in kittens. After the kittens grew to adults, both hindlimbs were implanted with multiple electromyogram (EMG) recording and cutaneous nerve stimulation electrodes to compare the activity of altered and normal muscles. The tendon transfers showed a remarkable tendency to regrow toward normal or only slightly altered mechanical action. In these animals and in the sham-operation controls, the patterns of muscle activity and reflexes were symmetrical in corresponding muscles of the two legs, although they could differ substantially between animals, particularly for the cutaneous reflexes. Eleven animals had at least some persistent alterations in muscle action. Their cutaneous reflex patterns tended to be asymmetric, in some cases quite markedly. EMG activity during unperturbed locomotion and paw-shaking was more symmetrical, but there were some changes in altered muscles and their synergists. The central pattern generators for locomotion and paw-shaking and particularly for cutaneous reflexes during locomotion appear to be at least partially malleable rather than entirely hardwired. This may provide a tool for studying their development and spinal plasticity in general.


2011 ◽  
Vol 105 (2) ◽  
pp. 601-614 ◽  
Author(s):  
Erik Zornik ◽  
Ayako Yamaguchi

Reproductive behaviors of many vertebrate species are activated in adult males by elevated androgen levels and abolished by castration. Neural and muscular components controlling these behaviors contain numerous hormone-sensitive sites including motor initiation centers (such as the basal ganglia), central pattern generators (CPGs), and muscles; therefore it is difficult to confirm the role of each hormone-activated target using behavioral assays alone. Our goal was to address this issue by determining the site of androgen-induced vocal activation using male Xenopus laevis, a species in which androgen dependence of vocal activation has been previously determined. We compared in vivo calling patterns and functionality of two in vitro preparations—the isolated larynx and an isolated brain from which fictive courtship vocalizations can be evoked—in castrated and control males. The isolated larynx allowed us to test whether castrated males were capable of transducing male-typical nerve signals into vocalizations and the fictively vocalizing brain preparation allowed us to directly examine vocal CPG function separate from the issue of vocal initiation. The results indicate that all three components—vocal initiation, CPG, and larynx—require intact gonads. Vocal production decreased dramatically in castrates and laryngeal contractile properties of castrated males were demasculinized, whereas no changes were observed in control animals. In addition, fictive calls of castrates were degraded compared with those of controls. To our knowledge, this finding represents the first demonstration of gonad-dependent maintenance of a CPG for courtship behavior in adulthood. Because previous studies showed that androgen-replacement can prevent castration-induced vocal impairments, we conclude that degradation of vocal initiation centers, larynx, and CPG function are most likely due to steroid hormone deprivation.


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