Gating of steering signals through phasic modulation of reticulospinal neurons during locomotion (original) (raw)

Reticulospinal neurons controlling forward and backward swimming in the lamprey

Journal of Neurophysiology, 2011

Most vertebrates are capable of two forms of locomotion, forward and backward, strongly differing in the patterns of motor coordination. Basic mechanisms generating these patterns are located in the spinal cord; they are activated and regulated by supraspinal commands. In the lamprey, these commands are transmitted by reticulospinal (RS) neurons. The aim of this study was to reveal groups of RS neurons controlling different aspects of forward (FS) and backward (BS) swimming in the lamprey. Activity of individual larger RS neurons in intact lampreys was recorded during FS and BS by chronically implanted electrodes. It was found that among the neurons activated during locomotion, 27% were active only during FS, 3% only during BS, and 70% during both FS and BS. In a portion of RS neurons, their mean firing frequency was correlated with frequency of body undulations during FS (8%), during BS (34%), or during both FS and BS (22%), suggesting their involvement in control of locomotion int...

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Physiological Reviews, 2019

The vertebrate control of locomotion involves all levels of the nervous system from cortex to the spinal cord. Here, we aim to cover all main aspects of this complex behavior, from the operation of the microcircuits in the spinal cord to the systems and behavioral levels and extend from mammalian locomotion to the basic undulatory movements of lamprey and fish. The cellular basis of propulsion represents the core of the control system, and it involves the spinal central pattern generator networks (CPGs) controlling the timing of different muscles, the sensory compensation for perturbations, and the brain stem command systems controlling the level of activity of the CPGs and the speed of locomotion. The forebrain and in particular the basal ganglia are involved in determining which motor programs should be recruited at a given point of time and can both initiate and stop locomotor activity. The propulsive control system needs to be integrated with the postural control system to maint...

Simple cellular and network control principles govern complex patterns of motor behavior

Proceedings of the National Academy of Sciences, 2009

The vertebrate central nervous system is organized in modules that independently execute sophisticated tasks. Such modules are flexibly controlled and operate with a considerable degree of autonomy. One example is locomotion generated by spinal central pattern generator networks (CPGs) that shape the detailed motor output. The level of activity is controlled from brainstem locomotor command centers, which in turn, are under the control of the basal ganglia. By using a biophysically detailed, full-scale computational model of the lamprey CPG (10,000 neurons) and its brainstem/forebrain control, we demonstrate general control principles that can adapt the network to different demands. Forward or backward locomotion and steering can be flexibly controlled by local synaptic effects limited to only the very rostral part of the network. Variability in response properties within each neuronal population is an essential feature and assures a constant phase delay along the cord for different locomotor speeds.

Activity of Reticulospinal Neurons During Locomotion in the Freely Behaving Lamprey

Journal of Neurophysiology, 2000

The reticulospinal (RS) system is the main descending system transmitting commands from the brain to the spinal cord in the lamprey. It is responsible for initiation of locomotion, steering, and equilibrium control. In the present study, we characterize the commands that are sent by the brain to the spinal cord in intact animals via the reticulospinal pathways during locomotion. We have developed a method for recording the activity of larger RS axons in the spinal cord in freely behaving lampreys by means of chronically implanted macroelectrodes. In this paper, the mass activity in the right and left RS pathways is described and the correlations of this activity with different aspects of locomotion are discussed. In quiescent animals, the RS neurons had a low level of activity. A mild activation of RS neurons occurred in response to different sensory stimuli. Unilateral eye illumination evoked activation of the ipsilateral RS neurons. Unilateral illumination of the tail dermal photo...

Modeling of the Spinal Neuronal Circuitry Underlying Locomotion in a Lower Vertebratea

Annals of the New York Academy of Sciences, 1998

The neural circuitry generating lamprey undulatory swimming is among the most accessible and best known of the vertebrate neuronal locomotor systems. It therefore serves as an experimental model for such systems. Modeling and computer simulation of this system was initiated at a point when a significant part of the network had been identified, although much detail was still lacking. The model has been further developed over 10 years in close interaction with experiments. The local burst generating circuitry is formed by ipsilateral excitatory neurons and crossed reciprocal inhibitory neurons. Early models also incorporated an off-switch lateral interneuron (L), the connectivity of which suggested it could contribute to burst termination at moderate to high bursting frequencies. Later examination of this model suggested, however, that the L interneuron was not of primary importance for burst termination, and this was later verified experimentally. Further, early models explained the effects of 5-HT on bursting frequency, spike frequency, and burst duration as being due to its modulatory action on the spike frequency adaptation of lamprey premotor interneurons. In current network models, accumulated adaptation is in addition the main burst terminating factor. Drive-related modulation of adaptation is explored as a mechanism for control of burst duration. This produces an adequate burst frequency range and a constant burst proportion within each cycle. It further allows for hemisegmental bursting, which has been observed experimentally. The local burst generator forms the basis of a network model of the distributed pattern generator that extends along the spinal cord. Phase constancy and flexibility of intersegmental coordination has been studied in such a simulated network. Current modeling work focuses on neuromodulator circuitry and action, network responses to input transients, how to model the intact versus an isolated piece of spinal cord, as well as on improving an earlier neuromechanical model of lamprey swimming.

Interaction between the caudal brainstem and the lamprey central pattern generator for locomotion

Neuroscience, 1996

Because of its remarkable simplicity and the robustness of the isolated preparation, the lamprey has been used as a model system to study locomotion and its central pattern generator. The function of the spinal cord is relatively well understood in this context, but the role of the brain or even the caudal brainstem remains less so. We here present a study of the interaction between the caudal brainstem and the spinal pattern generator for locomotion. We show that the interaction is highly complex, with both feedforward input from the brainstem to spinal cord and feedback input from the spinal cord to brainstem playing a significant role in the motor output during locomotion. The brainstem, when diffusely stimulated pharmacologically, can initiate fictive locomotion, or it can disrupt or alter the ongoing D-glutamate initiated motor output. The nature of the disruptions vary greatly, and can induce generalized irregularity, while the alterations can include accelerating or decelerating of the bursting. All behaviors are displayed with spectrograms of the motor nerve discharge. We also show that the unstimulated brainstem can disrupt as well as slow the bursting, but in a complex fashion. Finally, a slow episodic behavior initiated from the caudal brainstem is also described. This can be elicited either by D-glutamate to the brainstem or by ascending activity from the spinal cord pattern generator. Thus, we demonstrate that the interaction between the brainstem and the spinal cord during the production of locomotion is highly complex. The locomotion that is exhibited by the combined brainstem-spinal cord preparation is extremely variable. This is in striking contrast to the variability of the locomotor output pharmacologically induced in the spinal cord alone. The latter preparation exhibits remarkable regularity, or upon occasion, irregularity, but not the routine irregularity or the systematic up and down changes in frequency seen with the brainstem present. However, the pattern of frequency changes induced by the brainstem is not predictable, and remains to be understood.

Mathematical Analysis and Simulations of the Neural Circuit for Locomotion in Lampreys

Physical Review Letters, 2004

We analyze the dynamics of the neural circuit of the lamprey central pattern generator (CPG) This analysis provides insights into how neural interactions form oscillators and enable spontaneous oscillations in a network of damped oscillators, which were not apparent in previous simulations or abstract phase oscillator models. We also show how the different behaviour regimes (characterized by phase and amplitude relationships between oscillators) of forward/backward swimming, and turning, can be controlled using the neural connection strengths and external inputs.

Responses of Reticulospinal Neurons in the Lamprey to Lateral Turns

Journal of Neurophysiology, 2007

When swimming, the lamprey maintains a definite orientation of its body in the vertical planes, in relation to the gravity vector, as the result of postural vestibular reflexes. Do the vestibular-driven mechanisms also play a role in the control of the direction of swimming in the horizontal (yaw) plane, in which the gravity cannot be used as a reference direction? In the present study, we addressed this question by recording responses to lateral turns in reticulospinal (RS) neurons mediating vestibulospinal reflexes. In intact lampreys, the activity of axons of RS neurons was recorded in the spinal cord by implanted electrodes. Vestibular stimulation was performed by periodical turns of the animal in the yaw plane (60° peak to peak). It was found that the majority of responding RS neurons were activated by the contralateral turn. By removing one labyrinth, we found that yaw responses in RS neurons were driven mainly by input from the contralateral labyrinth. We suggest that these n...

Modeling a vertebrate motor system: pattern generation, steering and control of body orientation

Progress in brain research, 2007

The lamprey is one of the few vertebrates in which the neural control system for goal-directed locomotion including steering and control of body orientation is well described at a cellular level. In this report we review the modeling of the central pattern-generating network, which has been carried out based on detailed experimentation. In the same way the modeling of the control system for steering and control of body orientation is reviewed, including neuromechanical simulations and robotic devices.