Evolutionary Conservation of the Basal Ganglia as a Common Vertebrate Mechanism for Action Selection

Stephenson-Jones, Marcus; Samuelsson, Ebba; Ericsson, Johan; Robertson, Brita; Grillner, Sten

doi:10.1016/j.cub.2011.05.001

Cited by 253 publications

(271 citation statements)

References 57 publications

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“…These ascending projections are possibly involved in sensory-mediated respiratory control. Of note, like other neurophysiological features (Ericsson et al, , 2013Stephenson-Jones et al, 2011Grillner and Robertson, 2015), the general characteristics and the basic functional role of inhibitory mechanisms involved in rhythmic activities, such as respiration, appear to be highly conserved throughout evolution. New findings on the lamprey respiratory network may be useful to provide insights into the basic mechanisms of the central rhythm or pattern generators (Grillner, 2006) and hints for further investigations on this topic not only in the lamprey, but also in higher vertebrates, including mammals.…”

Section: Resultsmentioning

confidence: 95%

“…Sections were subsequently incubated with a mixture of Alexa Fluor 488 goat anti-rabbit IgG (1:200; Invitrogen) and Alexa fluor-568 conjugated streptavidin (1:1000; Invitrogen) for 3 h. For the immunohistochemical detection of glycine (double-labeling experiments), sections were incubated with rat polyclonal anti-glycine (1.5000; IG1002; ImmunoSolutions, Jesmond, New South Wales, Australia). Sections were subsequently incubated with a mixture of Alexa Fluor 488 goat anti-rat IgG (1:200; Invitrogen) and Alexa fluor-568 conjugated streptavidin (1:1000; Invitrogen) for 3 h. The specificity of the employed glutamate and glycine antibodies is known from previous studies in the lamprey (Mahmood et al, 2009;Stephenson-Jones et al, 2011;Cinelli et al, 2013). Although the rabbit anti-GABA antibody has not been previously used in the lamprey, we are confident that it is specific for GABA.…”

Section: Anatomical Experimentsmentioning

confidence: 99%

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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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Section: Resultsmentioning

confidence: 95%

Section: Anatomical Experimentsmentioning

confidence: 99%

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

et al. 2016

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“…8D) as in other species (54)(55)(56). Furthermore, the basal ganglia output nuclei instead provide tonic GABAergic inhibition to the tectal output cells in lamprey as well as in mammals (31,(57)(58)(59). This GABAergic input to the tectal output cells can serve to gate the circuit and allow activation through a temporary release from inhibition (disinhibition) (60).…”

Section: Discussionmentioning

confidence: 99%

“…To achieve this, we have developed a preparation in lamprey that maintains the eye and the midbrain intact in vitro, which has allowed us to perform whole-cell recordings from identified gaze-controlling cells in the optic tectum, while delivering natural and focal light stimuli within the visual field and monitoring and manipulating the synaptic responses. The retinotopic map in the lamprey tectum and the aligned motor map have been described in considerable detail (22,26), and the lamprey nervous system from forebrain to spinal cord is experimentally very accessible, well described, and also conserved throughout vertebrate evolution (30)(31)(32).…”

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confidence: 99%

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Kardamakis

Saitoh

Grillner

2015

Proc. Natl. Acad. Sci. U.S.A.

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132

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The optic tectum (called superior colliculus in mammals) is critical for eye-head gaze shifts as we navigate in the terrain and need to adapt our movements to the visual scene. The neuronal mechanisms underlying the tectal contribution to stimulus selection and gaze reorientation remains, however, unclear at the microcircuit level. To analyze this complex-yet phylogenetically conservedsensorimotor system, we developed a novel in vitro preparation in the lamprey that maintains the eye and midbrain intact and allows for whole-cell recordings from prelabeled tectal gaze-controlling cells in the deep layer, while visual stimuli are delivered. We found that receptive field activation of these cells provide monosynaptic retinal excitation followed by local GABAergic inhibition (feedforward). The entire remaining retina, on the other hand, elicits only inhibition (surround inhibition). If two stimuli are delivered simultaneously, one inside and one outside the receptive field, the former excitatory response is suppressed. When local inhibition is pharmacologically blocked, the suppression induced by competing stimuli is canceled. We suggest that this rivalry between visual areas across the tectal map is triggered through long-range inhibitory tectal connections. Selection commands conveyed via gazecontrolling neurons in the optic tectum are, thus, formed through synaptic integration of local retinotopic excitation and global tectal inhibition. We anticipate that this mechanism not only exists in lamprey but is also conserved throughout vertebrate evolution.optic tectum | superior colliculus | GABAergic inhibition | gaze control | evolution V isual scenes are composed of abundant stimuli, and the gaze needs continuously to be redirected toward different objectsan important task for the brain. Current models postulate that stimulus selection occurs through a process involving competitive interaction between different visual stimuli, resulting in the appropriate eye-head movement (1-5). The optic tectum (superior colliculus in mammals) has a causal role in the stimulus selection process (6-12) and not only in the control of saccades and eyehead gaze shifts (13-16). Although the collicular contribution to the selection process is of central importance, the underlying neuronal processes have remained elusive due to methodological limitations. It is our aim here to address this issue in a novel experimental model.The optic tectum is well developed in the lamprey, belonging to the oldest extant vertebrate group that evolved 560 million years ago (17), and it has remained conserved throughout vertebrate phylogeny (18)(19)(20)(21)(22). Afferents from retina provide a direct input to the superficial layers of the optic tectum, where a retinotopic map is formed (23-26). The intermediate and deep layers give rise to projections to brainstem areas and a motor map is formed that is responsible for the coordination of eye, head, and body movements (22,(27)(28)(29).To uncover the mechanisms underlying visual stimulus selection for gaz...

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“…Grillner [7] hypothesizes that the neural control system for locomotion can be traced back to the oldest known vertebrate, the lamprey, which appeared more than 500 million years ago, before any legged animal had evolved yet. Evolutionary conservation of developmental patterns [6 ] and neural core control networks [44][45][46]47 ] points to the comparative approach as a most fruitful one for the study of locomotor development [47 ,48].…”

Section: Comparative Aspectsmentioning

confidence: 99%

Development of human locomotion

Lacquaniti¹,

Ivanenko²,

Zago³

2012

Current Opinion in Neurobiology

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Neural control of locomotion in human adults involves the generation of a small set of basic patterned commands directed to the leg muscles. The commands are generated sequentially in time during each step by neural networks located in the spinal cord, called Central Pattern Generators. This review outlines recent advances in understanding how motor commands are expressed at different stages of human development. Similar commands are found in several other vertebrates, indicating that locomotion development follows common principles of organization of the control networks. Movements show a high degree of flexibility at all stages of development, which is instrumental for learning and exploration of variable interactions with the environment

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Evolutionary Conservation of the Basal Ganglia as a Common Vertebrate Mechanism for Action Selection

Cited by 253 publications

References 57 publications

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

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

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Development of human locomotion

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