Patch-clamp recordings in slices of telencephalon, diencephalon and rhombencephalon of salamanders

Trends in Neurosciences

Simon

Ijspeert

2020

Self Cite

How do four-legged animals adapt their locomotion to the environment? How do central and peripheral mechanisms interact within the spinal cord to produce adaptive locomotion and how is locomotion recovered when spinal circuits are perturbed? Salamanders are the only tetrapods that regenerate voluntary locomotion after full spinal transection. Given their evolutionary position, they provide a unique opportunity to bridge discoveries made in fish and mammalian models. Genetic dissection of salamander neural circuits is becoming feasible with new methods for precise manipulation, elimination, and visualisation of cells. These approaches can be combined with classical tools in neuroscience and with modelling and a robotic environment. We propose that salamanders provide a blueprint of the function, evolution, and regeneration of tetrapod locomotor circuits. Salamanders as a Model Organism for Studying Locomotion Two major challenges in neuroscience are to decipher how the interplay between central and peripheral mechanisms controls locomotion in four-legged animals (tetrapods) and to delineate the reorganisation of motor circuits after spinal lesion. In this review, we outline the reasons why salamanders are ideally suited to address these two problems. First, salamanders are the only tetrapods capable of regenerating their locomotor circuits after full transection at adult stage [1-3]. Second, they are the closest extant representatives of the first tetrapods that transitioned from aquatic to terrestrial life [4]. This key evolutionary position makes salamanders ideal to provide a bridge between discoveries in fish (such as zebrafish) and mammals (such as mouse). Salamanders swim underwater and walk on ground [4], allowing researchers to investigate to what extent body dynamics and sensory feedback shape these locomotor patterns. Third, high precision dissection of their neural circuits is becoming possible thanks to new tools that will allow visualisation and optogenetic and chemogenetic manipulations that can be combined with classical neuroscience tools and advanced modelling and robotic environments. It is thus timely to highlight the recent advances in salamander research at the intersection of genomics, systems neuroscience, modelling, and robotics, which altogether provide a unique opportunity to decode locomotor control in the intact and regenerated tetrapod nervous system. In this review, we systematically place these approaches and recent results into a cross-species comparative setting, with a special focus on zebrafish and mouse as comparative models for which most data on the genetic identity of locomotor circuits are available. For closer examination of the locomotor circuitries of other related animal models such as lamprey, cat, and Xenopus embryo, we refer readers to prior reviews (lamprey: [5], cat: [6], Xenopus embryo: [7]). The Salamander Nervous System: A Bridge between Fish and Mammalian Models Salamander locomotor circuits include the main features found in all vertebrates (Figure 1A,C). Their...

Section: Pkd2l1: Polycystin 2 Like 1 Transientmentioning

confidence: 77%

Section: Zebrafishmentioning

confidence: 92%

Walking with Salamanders: From Molecules to Biorobotics

Trends in Neurosciences

Simon

Ijspeert

2020

Self Cite

“…To record the tectum cells projecting to the mRN, the tracer Ca 2+ green was injected at the level of the mRN bilaterally and the preparation was pinned down in a cold (10°C) oxygenated chamber overnight. The next day, transverse slices were obtained as previously described (Flaive & Ryczko 2020). Briefly, the brain was glued onto the specimen disk at the level of a transverse section made rostral to the optic nerve, and placed in the slicing chamber of a VT1000S vibrating‐blade microtome (also called vibratome, Leica) filled with the ice‐cold sucrose‐based solution (in mM: 3 KCl, 1.25 KH 2 PO 4 , 4 MgSO 4 , 26 NaHCO 3 , 10 dextrose, 0.2 CaCl 2 , 219 sucrose, pH 7.3–7.4, 300–320 mOsmol/kg) bubbled with 95% O 2 and 5% CO 2 , with the vibratome blade facing the dorsal side of the brain.…”

Section: Methodsmentioning

confidence: 99%

From retina to motoneurons: A substrate for visuomotor transformation in salamanders

Flaive

J of Comparative Neurology

2022

Self Cite

The transformation of visual input into motor output is essential to approach a target or avoid a predator. In salamanders, visually guided orientation behaviors have been extensively studied during prey capture. However, the neural circuitry involved is not resolved. Using salamander brain preparations, calcium imaging and tracing experiments, we describe a neural substrate through which retinal input is transformed into spinal motor output. We found that retina stimulation evoked responses in reticulospinal neurons of the middle reticular nucleus, known to control steering movements in salamanders. Microinjection of glutamatergic antagonists in the optic tectum (superior colliculus in mammals) decreased the reticulospinal responses. Using tracing, we found that retina projected to the dorsal layers of the contralateral tectum, where the dendrites of neurons projecting to the middle reticular nucleus were located.In slices, stimulation of the tectal dorsal layers evoked glutamatergic responses in deep tectal neurons retrogradely labeled from the middle reticular nucleus. We then examined how tectum activation translated into spinal motor output. Tectum stimulation evoked motoneuronal responses, which were decreased by microinjections of glutamatergic antagonists in the contralateral middle reticular nucleus. Reticulospinal fibers anterogradely labeled from tracer injection in the middle reticular nucleus were preferentially distributed in proximity with the dendrites of ipsilateral motoneurons. Our work establishes a neural substrate linking visual and motor centers in salamanders. This retino-tecto-reticulo-spinal circuitry is well positioned to control orienting behaviors. Our study bridges the gap between the behavioral studies and the neural mechanisms involved in the transformation of visual input into motor output in salamanders.

“…To record the tectum cells projecting to the mRN, the tracer Ca 2+ green was injected at the level of the mRN bilaterally and pinned down in a cold (10°C degrees) oxygenated chamber overnight. The next day, coronal slices were obtained as previously described (Flaive and Ryczko 2020). Briefly, the brain was glued at the level of the transverse section rostral to the optic nerve onto the specimen disk and placed in the slicing chamber of a VT1000S vibrating-blade microtome (also called vibratome, Leica) filled with the ice-cold sucrose-based solution.…”

Section: Methodsmentioning

confidence: 99%

From retina to motoneurons: a substrate for visuomotor transformation in salamanders

Flaive

2022

Preprint

Self Cite

The transformation of visual input into motor output is essential to approach a target or avoid a predator. In salamanders, visually-guided orientation behaviors have been extensively studied during prey capture. However, the neural circuitry involved is not resolved. Using salamander brain preparations, calcium imaging and tracing experiments, we describe a neural substrate through which retinal input is transformed into spinal motor output. We found that retina stimulation evoked responses in reticulospinal neurons of the middle reticular nucleus, known to control steering movements in salamanders. Microinjection of glutamatergic antagonists in the optic tectum (superior colliculus in mammals) decreased the reticulospinal responses. Using tracing we found that retina projected to the dorsal layers of the contralateral tectum, where the dendrites of neurons projecting to the middle reticular nucleus were located. In slices, stimulation of the tectal dorsal layers evoked glutamatergic responses in deep tectal neurons retrogradely labelled from the middle reticular nucleus. We then examined how tectum activation translated into spinal motor output. Tectum stimulation evoked motoneuronal responses, which were decreased by microinjections of glutamatergic antagonists in the contralateral middle reticular nucleus. Reticulospinal fibers anterogradely labelled from tracer injection in the middle reticular nucleus were preferentially distributed in proximity with the dendrites of ipsilateral motoneurons. Our work establishes a neural substrate linking visual and motor centers in salamanders. This retino-tecto-reticulo-spinal circuitry is well positioned to control orienting behaviors. Our study bridges the gap between the behavioral studies and the neural mechanisms involved in the transformation of visual input into motor output in salamanders.