Encoding and decoding of reticulospinal commands

doi:10.1016/S0165-0173(02)00199-6

Brain Research Reviews

Volume 40, Issues 1–3, October 2002, Pages 166-177

https://doi.org/10.1016/S0165-0173(02)00199-6 Get rights and content

Abstract

In the lamprey, the reticulospinal (RS) system is the main descending system transmitting commands to the spinal cord. We investigated these commands and their effect on the spinal mechanisms. The RS commands were studied by recording responses of RS neurons to sensory stimuli eliciting different motor behaviors. Initiation of locomotion was associated with symmetrical bilateral massive activation of RS neurons, whereas turns in different planes were associated with asymmetrical activation of corresponding neuronal groups. The sub-populations of RS neurons causing different motor behaviors partly overlap. We suggest that commands for initiation of locomotion and regulation of its vigour, encoded as the value of bilateral RS activity, are decoded in the spinal cord by integrating all RS signals arriving at the segmental locomotor networks. Commands for turns in different planes, encoded as an asymmetry in the activities of specific groups of RS neurons, are decoded by comparing the activities of those groups. This hypothesis was supported by the experiments on a neuro-mechanical model, where the difference between the activities in the left and right RS pathways was used to control a motor rotating the animal in the roll plane. Transformation of the descending commands into the motor responses was investigated by recording the effects of individual RS neurons on the motor output. Twenty patterns of influences have been found. This great diversity of the patterns allows the RS system to evoke body flexion in any plane. Since most neurons have asymmetrical projections we suggest that, for rectilinear swimming, RS neurons with opposite asymmetrical effects are co-activated.

Introduction

The reticulospinal (RS) system plays an important role in the control of locomotion, steering and posture in vertebrates [23]. In higher vertebrates, the specific contribution of the RS system to the control of motor behavior is difficult to assess since this system operates along with other descending systems, the corticospinal, rubrospinal, and vestibulospinal ones. We have been studying the RS system in the lamprey (a lower vertebrate, cyclostome). This animal has a general organization of the CNS similar to that in higher vertebrates [19]. In contrast to higher vertebrates, however, the RS system in the lamprey is practically the only descending system transmitting commands to the spinal cord and responsible for the initiation of locomotion, for steering, and for postural corrections. The bilateral RS pathways originate from ∼2400 neurons located in four reticular nuclei: the mesencephalic reticular nucleus, and the anterior, middle and posterior rhombencephalic reticular nuclei [1], [4], [26], [28]. RS neurons project ipsilaterally over long distances and affect different classes of spinal neurons [2], [20], [27].

In the present study we first investigated, the commands for different forms of motor activity in the lamprey transmitted by RS neurons. Secondly, we tried to understand how these commands affect the spinal mechanisms.

Section snippets

Commands transmitted by RS neurons

The RS commands were studied by recording the responses of individual RS neurons to various sensory stimuli in the intact lamprey [6], [11], in the semi-intact preparation [10], [16], and in the in vitro preparation [7], [8], [9]. These stimuli evoke different motor behaviors such as locomotion, steering, and postural corrections.

Overlap of descending command systems

The RS system in the lamprey is practically the only descending system to transmit different motor commands to the spinal cord. This raises two questions.

(1) When the same motor pattern is used in different behavioral contexts, or is evoked by different sensory stimuli, are the corresponding motor commands transmitted by the same sub-population of RS neurons or by different sub-populations? An answer to this question for one particular case has been obtained in recent experiments [6]. It was

Decoding of RS commands

We suggest that decoding of RS commands in the spinal cord is based on two principles. (1) The commands for initiation of locomotion and regulation of its vigour, encoded as the value of bilateral RS activity, are decoded by integrating all RS signals arriving to the spinal locomotor networks, so that their integrated value determines the level of activity of these networks. (2) The commands for turns in different planes, encoded as an asymmetry in the activities of specific subdivisions of the

Motor effects of individual RS neurons

A weakness of our models of postural control is that the motor effect of RS neurons was hypothesized rather than determined experimentally. The effects of signals transmitted from the brain to the spinal networks by a population of RS neurons are determined by specific functional projections of individual neurons. In higher vertebrates, these projections are difficult to reveal [13]. We have found that, in the lamprey, motor effects of individual RS neurons can be detected by averaging the

Acknowledgements

This work was supported by grants to T.G.D. from Royal Swedish Academy of Sciences (Research Grant for Swedish–Russian scientific co-operation), Swedish Medical Research Council (no. 11554), and Curt Nilsson Foundation. P.V.Z. was supported by the Wenner-Gren Foundation.

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ReviewEncoding and decoding of reticulospinal commands

Abstract

Introduction

Section snippets

Commands transmitted by RS neurons

Overlap of descending command systems

Decoding of RS commands

Motor effects of individual RS neurons

Acknowledgements

Brain Res.

Brain Res.

Reticulospinal neurons in lamprey: transmitters, synaptic interactions and their role during locomotion

Arch. Ital. Biol.

Activities of identified interneurons, motoneurons, and muscle fibers during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation

J. Neurophysiol.

Ueber Bau und Funktion des Petromyzonlabyrinthes

Acta Oto-laryngol. (Suppl.)

Vestibular compensation in lampreys: impairment and recovery of equilibrium control during locomotion

J. Exp. Biol.

Responses of reticulospinal neurons in intact lamprey to vestibular and visual inputs

J. Neurophysiol.

Vestibular control of swimming in lamprey. 2. Characteristics of spatial sensitivity of reticulospinal neurons

Exp. Brain Res.

Vestibular control of swimming in lamprey. 3. Activity of vestibular afferents. Convergence of vestibular inputs on reticulospinal neurons

Exp. Brain Res.

Visual input affects the response to roll in reticulospinal neurons of the lamprey

Exp. Brain Res.

Initiation of locomotion in larval and adult lamprey by stimulation of lateral line photoreceptors

J. Exp. Biol.

Activity of reticulospinal neurons during locomotion in the freely behaving lamprey

J. Neurophysiol.

Functional organization within the medullary reticular formation of the intact unanaesthetized cat. III. Microstimulatiom during locomotion

J. Neurophysiol.

Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill

J. Neurophysiol.

Crossed reciprocal inhibition evoked by electrical stimulation of the lamprey spinal cord

Exp. Brain Res.

Lateral turns in the lamprey. II. Activity of reticulospinal neurons during the generation of fictive turns

J. Neurophysiol.

Review
Encoding and decoding of reticulospinal commands