Responses of Reticulospinal Neurons in the Lamprey to Lateral Turns (original) (raw)
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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...
Vestibular control of swimming in lamprey
Experimental Brain Research, 1992
A method has been developed for recording the response of single neurons in the lamprey brainstem in vitro to natural stimulation of vestibular receptors. The brainstem dissected together with the intact vestibular apparatus could be rotated in space, in two perpendicular planes (transverse, the roll tilt, and sagittal, the pitch tilt), in one of them up to 360°, and in
Postural Control in the Lamprey: A Study With a Neuro-Mechanical Model
Journal of Neurophysiology, 2000
The swimming lamprey normally maintains the dorsal-side-up orientation due to activity of the postural control system driven by vestibular organs. Commands for postural corrections are transmitted from the brain stem to the spinal cord mainly by the reticulospinal (RS) pathways. As shown in previous studies, RS neurons are activated by contralateral roll tilt, they exhibit a strong dynamic response, but much weaker static response. Here we test a hypothesis that decoding of these commands in the spinal cord is based on the subtraction of signals in the left and right RS pathways. In this study, we used a neuro-mechanical model. An intact lamprey was mounted on a platform that restrained its postural activity but allowed lateral locomotor undulations to occur. The activity in the left and right RS pathways was recorded by implanted electrodes. These natural biological signals were then used to control an electrical motor rotating the animal around its longitudinal axis toward the str...
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...
Brain Research, 1989
Lamprey reticulospinal neurons are rhythmically modulated during fictive swimming. The present study examines the possibility that this modulation may originate from the spinal cord locomotor networks rather than from the brainstem. To test this, the in vitro preparation of the lamprey brainstem-spinal cord was separated into two compartments which could be exposed to different chemical environments. Locomotor activity was induced pharmacologically in the caudal spinal cord compartment and reticulospinal (RS) neurons from the posterior rhombencephalic reticular nucleus (PRRN) were recorded intracellularly in the rostral compartment containing normal lamprey Ringer. Under these conditions, the membrane potential of RS neurons showed clear rhythmic oscillations which are correlated with the ongoing locomotor activity in the caudal spinal cord bath, although no locomotor discharges were present in the ventral roots of the rostral bath. Such oscillations were not present in the absence of locomotion. These results indicate that the spinal cord locomotor networks can contribute to the rhythmic oscillations which occur in RS neurons during fictive locomotion. Moreover, the latter oscillations of membrane potential are due to both phasic excitation and Cl- -dependent inhibition in the opposite phase.
Visual Potentiation of Vestibular Responses in Lamprey Reticulospinal Neurons
European Journal of Neuroscience, 1996
The lamprey normally swims with the dorsal side up. Illumination of one eye shifts the set-point of the vestibular roll control system, however, so that the animal swims with a roll tilt towards the source of light (the dorsal light response). A tilted orientation is often maintained for up to 1 min after the stimulation. In present study, the basis for this behaviour was investigated at the neuronal level. The middle rhombencephalic reticular nucleus (MRRN) is considered a main nucleus for the control of roll orientation in lampreys. Practically all MRRN neurons receive vestibular and visual input and project to the spinal cord. Earlier extracellular experiments had shown that optic nerve stimulation potentiates the response to vestibular stimulation in the ipsilateral MRRN. This most likely represents a neural correlate of the dorsal light response. Experiments were carried out in vitro on the isolated brainstem of the silver lamprey (Ichthyomyzon unicuspis). MRRN cells were recorded intracellularly, and the overall activity of descending systems was monitored with bilateral extracellular electrodes. The responses to 10 Hz optic nerve stimulation and 1 Hz vestibular nerve stimulation, and the influence of optic nerve stimulation on the vestibular responses, were investigated. In most preparations, optic nerve stimulation excited practically all ipsilateral MRRN cells. After stimulation, the cell was typically depolarized and showed an increased level of synaptic noise for up to 80 s. In contralateral MRRN neurons, optic nerve stimulation usually evoked hyperpolarization or no response. Vestibular nerve stimulation evoked compound excitatory postsynaptic potentials (EPSPs) or spikes in approximately 90% of the cells, both ipsilaterally and contralaterally. A smaller subpopulation of MRRN cells (approximately 10%) received vestibular inhibition. In 26 of 48 recorded MRRN cells, the response to vestibular stimulation was potentiated after ipsilateral optic nerve stimulation. The potentiation was seen in cells receiving either excitatory or inhibitory vestibular input as an increase in EPSP amplitude/spiking (85%) and a decrease in inhibitory postsynaptic potential amplitude (15%) respectively. In most cases the vestibular responses did not return to control levels during the testing period (10-30 min), and thus the visual stimulation most likely induced long-lasting changes in the functional connectivity of the role control network, in addition to the short-lasting afteractivity. In four of the 11 cells recorded contralateral to the stimulated optic nerve, a depression of the vestibular response could be seen. In potentiated cells, single vestibular pulses often evoked longer episodes of large synaptic noise and sometimes spiking. In the latter case, the action potentials appeared with highly variable latency after each stimulation pulse. This indicates that an important mechanism underlying the potentiation may be a long-lasting increase in excitability in a pool of unidentified interneurons located either upstream of the MRRN cells, relaying vestibular and visual inputs, or downstream, providing positive feedback.
Intraspinal stretch receptor neurons mediate different motor responses along the body in lamprey
Journal of Comparative Neurology, 2013
Different species maintain a basic body posture due to the activity of the postural control system. An efficient control of the body orientation, as well as the body configuration, is important for standing and during locomotion. A general goal of the present study was to analyze neuronal feedback mechanisms contributing to stabilization of the trunk orientation in space, as well as those controlling the body configuration. Two animal models of different complexity, the lamprey (a lower vertebrate) and the rabbit (a mammal), were used. Neuronal mechanisms underlying lateral stability were analyzed in rabbits. The dorsalside-up trunk orientation in standing quadrupeds is maintained by the postural system driven mainly by somatosensory inputs from the limbs. Postural limb reflexes (PLRs) represent a substantial component of this system. To characterize spinal neurons of the postural networks, in decerebrate rabbit, activity of individual spinal neurons in L4-L6 was recorded during PLRs caused by lateral tilts of the supporting platform. Spinal neurons mediating PLRs have been revealed, and different parameters of their activity were characterized. All neurons were classified into four types according to the combination of tilt-related sensory inputs to a neuron from the ipsi-and contralateral limb (determining the modulation of a neuron). A hypothesis about the role of different types of PLR-related neurons for trunk stabilization in different planes has been proposed. To reveal contribution of supraspinal influences to modulation of PLR-related neurons, the activity of individual spinal neurons was recorded during stimulation causing PLRs under two conditions: (i) when spinal neurons received supraspinal influences, and (ii) when these influences were temporarily abolished by a cold block of spike propagation in spinal pathways at T12 ("reversible spinalization"). The effects of reversible spinalization on individual neurons were diverse. Neurons, which did not receive supraspinal influences, were located mainly in the dorsal horn, whereas most neurons, receiving excitatory supraspinal influences were located in the intermediate zone and ventral horn. The population of PLRrelated neurons presumably responsible for disappearance of muscle tone and PLRs after spinalization was revealed. The effects of manipulation with the tonic supraspinal drive (by means of binaural galvanic vestibular stimulation, GVS) on the postural system were studied. GVS creates asymmetry in tonic supraspinal drive, resulting in a lateral body sway towards the anode. This new body orientation is actively stabilized. To reveal the underlying mechanisms, spinal neurons were recorded during PLRs with and without GVS. It was found that GVS enhanced PLRs on the cathode side and reduced them on the anode side. It was suggested that GVS changes the set-point of the postural system through the change of the gain in antagonistic PLRs. Two subgroups of PLR-related neurons presumably mediating the effect of GVS on PLRs were found. An artificial feedback system was formed in which GVS-caused body sway was used to counteract the lateral body sway resulting from a mechanical perturbation of posture. It was demonstrated that the GVS-based artificial feedback was able to restore the postural function in rabbits with postural deficit. We suggested that such a control system could compensate for the loss of lateral stability of different etiology. Neuronal mechanisms underlying control of body configuration were analyzed in lampreys. The lamprey is capable of different forms of motor behavior: fast forward swimming (FFS), slow forward swimming (SFS), backward swimming (BS), forward and backward crawling, and lateral turns (LT). The amplitude of the body flexion (characterizing the body configuration) differs in different forms of motor behavior. In the lamprey, signals about the body configuration are provided by intraspinal stretch receptor neurons (SRNs). To clarify whether the networks generating different forms of motor behavior are located in the spinal cord, in chronic spinal lampreys, electrical stimulation of the spinal cord was performed. It was demonstrated that all forms of motor behavior are generated by the spinal networks. To study SRN-mediated reflexes and their contribution to the control of body configuration in different motor behaviors, in the in vitro preparation we recorded responses of reticulospinal (RS) neurons and motoneurons (MNs) to bending of the spinal cord in different planes and at different rostro-caudal levels during different forms of fictive motor behavior Bending in the pitch plane during FFS caused SRN-mediated reflexes. MNs on the convex side were activated by pitch bending in the mid-body region. These reflexes will reduce the bend, thus contributing to maintenance of rectilinear body axis in the pitch plane during FFS. It was found that bending in the yaw plane activated MNs on the convex side during FFS, but on the concave side during different forms of escape behavior (SFS, BS, LT). It was demonstrated that a reversal of reflex responses was due to ipsilateral supraspinal commands causing modifications of the spinal network located in the ipsi-hemicord. A population of RS neurons (residing in the middle rhombencephalic reticular nuclei) presumably transmitting these commands has been revealed. We suggest that modifications of SRN-mediated reflex responses will result in the decrease and increase of the lateral bending amplitude during FFS and escape behaviors, respectively, thus reinforcing movements generated in each specific behavior. Thus in the present study, for the first time, some neuronal mechanisms underlying reflex reversal in vertebrate animals have been revealed.
Journal of Neurophysiology, 2003
In the lamprey (a lower vertebrate), motor commands from the brain to the spinal cord are transmitted through the reticulospinal (RS) and vestibulospinal (VS) pathways. The axons of larger RS neurons reach the most caudal of approximately 100 spinal segments, whereas the VS pathway does not descend below the 15th segment. This study was carried out to compare functional projections of RS and VS neurons in the rostral spinal segments that the neurons innervate together. To reveal these projections, individual RS or VS neurons were stimulated, and the responses of different groups of spinal motoneurons were recorded in ventral root branches to dorsal and ventral parts of myotomes. The responses were detected using a spike-triggered averaging technique on the background of ongoing motoneuronal activity. Individual RS and VS neurons exerted uniform effects on segmental motor output within this rostral part of the spinal cord. The effects of VS neurons on different groups of motoneurons ...
Pattern of Motor Coordination Underlying Backward Swimming in the Lamprey
Journal of Neurophysiology, 2006
Islam, Salma S., Pavel V. Zelenin, Grigori N. Orlovsky, Sten Grillner, and Tatiana G. Deliagina. Pattern of motor coordination underlying backward swimming in the lamprey. . The main form of locomotion in the lamprey (a lower vertebrate, cyclostome) is forward swimming (FS) based on periodical waves of lateral body flexion propagating from head to tail. The lamprey is also capable of backward swimming (BS).