Initiation of locomotion by lateral line photoreceptors in lamprey:behavioural and neurophysiological studies

Deliagina, T. G.; Ullén, Fredrik; González, Marı́a José; Ehrsson, H. Henrik; Orlovsky, G. N.; Grillner, Sten

doi:10.1242/jeb.036244

Cited by 16 publications

(12 citation statements)

References 31 publications

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“…Forward swimming appeared either spontaneously or was evoked by different sensory stimuli, i.e., pinching the head or the tail, illuminating the eye or tail photoreceptors (Ullén et al 1993;Deliagina et al 1995). The lamprey swam freely for periods of 20 to 100 s, randomly turning in different planes and changing the frequency of body oscillations.…”

Section: Methodsmentioning

confidence: 99%

Reticulospinal neurons controlling forward and backward swimming in the lamprey

Zelenin

2011

Journal of Neurophysiology

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Zelenin PV. Reticulospinal neurons controlling forward and backward swimming in the lamprey. J Neurophysiol 105: 1361-1371, 2011. First published January, 19, 2011 doi:10.1152 doi:10. /jn.00887.2010brates 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 intensity. RS activity was phasically modulated by the locomotor rhythm during FS (20% of neurons), during BS (29%), or during both FS and BS (16%). The majority of RS neurons responding to vestibular stimulation (and presumably involved in control of body orientation) were active mainly during FS. This explains the absence of stabilization of the body orientation observed during BS. We discuss possible functions of different groups of RS neurons, i.e., activation of the spinal locomotor CPG, inversion of the direction of propagation of locomotor waves, and postural control. supraspinal commands; reticulospinal system; backward locomotion; forward locomotion; posture

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Section: Methodsmentioning

confidence: 99%

Reticulospinal neurons controlling forward and backward swimming in the lamprey

Zelenin

2011

Journal of Neurophysiology

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“…In addition to visual input, nonvisual sensory information reaches the pretectum directly from the lateral line receptors via the octavolateral area and indirectly through the torus semicircularis, a midbrain area that functions as a multisensory integration center (Bodznick and Northcutt, 1981;Gonz alez et al, 1999). The lateral line system is a sensory organ specialized for detecting vibrations conveyed through the water (Akoev and Muraveiko, 1984;Rovainen, 1982), photoreception from the skin (Young, 1935;Deliagina et al, 1995), and electroreception (Bodznick and Northcutt, 1981). For survival, integration of different types of sensory information from the surrounding world is critical.…”

Section: Pretectal Sensory Inputmentioning

confidence: 99%

The pretectal connectome in lamprey

Capantini

Twickel

Robertson

et al. 2016

J of Comparative Neurology

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In vertebrates, the pretectum and optic tectum (superior colliculus in mammals) are visuomotor areas that process sensory information and shape motor responses. Whereas the tectum has been investigated in great detail, the pretectum has received far less attention. The present study provides a detailed analysis of the connectivity and neuronal properties of lamprey pretectal cells. The pretectum can be subdivided roughly into three areas based on cellular location and projection pattern: superficial, central, and periventricular. Three different types of pretectal cells could be distinguished based on neuronal firing patterns. One type, the rapid spike-inactivation cells, preferentially lie within the periventricular zone; the other cell types are distributed more generally. In terms of afferentation, the pretectum receives electro- and mechanoreceptive inputs in addition to retinal input. Histological data reveal that a large number of pretectal cells in the superficial and central areas extend dendrites into the optic tract, suggesting a predominant retinal influence even outside of the normal retinal terminal areas. The pretectum receives inhibitory input from the basal ganglia, and input from the pallium (cortex in mammals) and torus semicircularis. In addition, the pretectum is reciprocally connected with the thalamus, tectum, octavolateral area, and habenula. The main pretectal output is to the reticulospinal nuclei, and thus the pretectum indirectly affects the control of movement. Efference copies of some of this output are relayed to the thalamus and tectum. Overall, its extensive circuitry-especially the reciprocal connectivity with other retinorecipient areas-underlines the importance of the pretectum for sensory integration and visuomotor functions. J. Comp. Neurol. 525:753-772, 2017. © 2016 Wiley Periodicals, Inc.

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“…Interestingly, it has been reported that afferent projections of the glossopharyngeal and vagal nerves terminate in the OLA, especially in its medial and ventral nuclei (Koyama, 2005). Furthermore, the OLA receives information from light receptors of the tail and is involved in the initiation of locomotion evoked by tail illumination (Ulle´n et al, 1993;Deliagina et al, 1995). A study on the primary projections of the lateral line nerves, known to mediate photoreception, electroreception and mechanoreception, reported that some fibers were observed within areas other than the OLA and, in particular, within the vagal motoneuron region (Koyama et al, 1990).…”

Section: Functional Considerationsmentioning

confidence: 99%

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

et al. 2016

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Abstract-Neurons within the vagal motoneuron region of the lamprey have been shown to modulate respiratory activity via ascending excitatory projections to the paratrigeminal respiratory group (pTRG), the proposed respiratory rhythm generator. The present study was performed on in vitro brainstem preparations of the lamprey to provide a characterization of ascending projections within the whole respiratory motoneuron column with regard to the distribution of neurons projecting to the pTRG and related neurochemical markers. Injections of Neurobiotin were performed into the pTRG and the presence of glutamate, GABA and glycine immunoreactivity was investigated by doublelabeling experiments. Interestingly, retrogradely labeled neurons were found not only in the vagal region, but also in the facial and glossopharyngeal motoneuron regions. They were also present within the sensory octavolateral area (OLA). The results show for the first time that neurons projecting to the pTRG are immunoreactive for glutamate, surrounded by GABA-immunoreactive structures and associated with the presence of glycinergic cells. Consistently, GABA A or glycine receptor blockade within the investigated regions increased the respiratory frequency. Furthermore, microinjections of agonists and antagonists of ionotropic glutamate receptors and of the GABA A receptor agonist muscimol showed that OLA neurons do not contribute to respiratory rhythm generation. The results provide evidence that glutamatergic ascending pathways to the pTRG are subject to a potent inhibitory control and suggest that disinhibition is one important mechanism subserving their function. The general characteristics of inhibitory control involved in rhythmic activities, such as respiration, appear to be highly conserved throughout vertebrate evolution.

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Initiation of locomotion by lateral line photoreceptors in lamprey:behavioural and neurophysiological studies

Cited by 16 publications

References 31 publications

Reticulospinal neurons controlling forward and backward swimming in the lamprey

Reticulospinal neurons controlling forward and backward swimming in the lamprey

The pretectal connectome in lamprey

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

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