Afferents of the lamprey optic tectum with special reference to the GABA input: Combined tracing and immunohistochemical study

Robertson, Brita; Saitoh, Ken-ichi; Ménard, Ariane; Grillner, Sten

doi:10.1002/cne.21078

Cited by 37 publications

(52 citation statements)

References 81 publications

(91 reference statements)

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“…3 G and H). This confirms previous studies showing that the GPh does not project to the tectum or MLR (18,19). The major projections of the GPh neurons are, therefore, to the homolog of the lateral habenula.…”

Section: Gph and Gpi/gpe Neurons Differ In Their Electrophysiologicalsupporting

confidence: 91%

“…In contrast, pallidal neurons that project to the thalamus and brainstem motor regions are situated more caudally in the lamprey homolog of the GPi/GPe (Fig. 1A) (11,18,19). Both the GPi/GPe and GPh receive input from the striatum (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The major projections of the GPh neurons are, therefore, to the homolog of the lateral habenula. These results indicate that, as with the input, the output circuitry of the GPh is completely distinct from the GPi/GPe, which projects to the thalamus and brainstem motor regions (11,(18)(19)(20). tegmental area (VTA) and the matriosomes that preferentially express calbindin along with a range of other neurotransmitterrelated substances (21)(22)(23).…”

Section: Gph and Gpi/gpe Neurons Differ In Their Electrophysiologicalmentioning

confidence: 95%

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Independent circuits in the basal ganglia for the evaluation and selection of actions

Stephenson-Jones

Kardamakis

Robertson

et al. 2013

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

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116

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The basal ganglia are critical for selecting actions and evaluating their outcome. Although the circuitry for selection is well understood, how these nuclei evaluate the outcome of actions is unknown. Here, we show in lamprey that a separate evaluation circuit, which regulates the habenula-projecting globus pallidus (GPh) neurons, exists within the basal ganglia. The GPh neurons are glutamatergic and can drive the activity of the lateral habenula, which, in turn, provides an indirect inhibitory influence on midbrain dopamine neurons. We show that GPh neurons receive inhibitory input from the striosomal compartment of the striatum. The striosomal input can reduce the excitatory drive to the lateral habenula and, consequently, decrease the inhibition onto the dopaminergic system. Dopaminergic neurons, in turn, provide feedback that inhibits the GPh. In addition, GPh neurons receive direct projections from the pallium (cortex in mammals), which can increase the GPh activity to drive the lateral habenula to increase the inhibition of the neuromodulatory systems. This circuitry, thus, differs markedly from the "direct" and "indirect" pathways that regulate the pallidal (e.g., globus pallidus) output nuclei involved in the control of motion. Our results show that a distinct reward-evaluation circuit exists within the basal ganglia, in parallel to the direct and indirect pathways, which select actions. Our results suggest that these circuits are part of the fundamental blueprint that all vertebrates use to select actions and evaluate their outcome.striosomes | reward/aversion | pallium/cortex | evolution T o achieve a goal, animals need to select actions and evaluate their outcome to determine whether their goal was achieved. In mammals, the basal ganglia play a key role in the selection of actions (1-3) and have more recently been suggested to additionally contribute to predicting and evaluating the outcome of the selected actions (4-8).The so-called "direct" and "indirect" pathways through the basal ganglia are present in all vertebrates and act together to select actions by decreasing tonic inhibition of the basal ganglia output nuclei [globus pallidus interna (GPi) and substantia nigra pars reticulata (SNr)] on a selected motor program and increasing the inhibition onto other competing actions. The output of these selection circuits target brainstem and thalamic motor areas, and neurons within this circuit are modulated by various aspect of movement kinetics related to the initiation and modulation of ongoing actions.In addition to the output neurons that project to motor areas, a separate subpopulation of pallidal neurons projects to the lateral habenula (9-12), a structure involved in evaluating and predicting the motivational value of actions. Recent in vivo recordings in primates have shown that the activity of these habenula-projecting pallidal neurons is modulated by the cues that predict the availability of reward (13,14) and not by aspects of movements. The majority of these pallidal neurons, as with latera...

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Section: Gph and Gpi/gpe Neurons Differ In Their Electrophysiologicalsupporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Gph and Gpi/gpe Neurons Differ In Their Electrophysiologicalmentioning

confidence: 95%

See 1 more Smart Citation

Independent circuits in the basal ganglia for the evaluation and selection of actions

Stephenson-Jones

Kardamakis

Robertson

et al. 2013

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

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116

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“…Although most mammalian studies have focused on the role of the retinotopic excitatory circuits that mediate signal transmission between the superficial layer and the deeper layers (33)(34)(35)(36), only more recent studies have emphasized the role of GABAergic circuits in the collicular control of gaze (37)(38)(39)(40)(41)(42)(43)(44)(45). The question how collicular GABAergic systems affect stimulus selection for gaze motor action has, however, remained unanswered because most studies have relied on extracellular recordings in vivo and therefore have not allowed an analysis of the synaptic basis for these inhibitory interactions.…”

mentioning

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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“…We have constructed a model representing lamprey pallidal neuron [2] based on a previously published GPe/STN model neuron [3]. The model was re-implemented in GENESIS and tuned to replicate passive membrane properties of a lamprey pallidal neuron.…”

Section: Modelmentioning

confidence: 99%

Exploration of the lamprey pallidal neurons – a combined computational and experimental study

2009

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Afferents of the lamprey optic tectum with special reference to the GABA input: Combined tracing and immunohistochemical study

Cited by 37 publications

References 81 publications

Independent circuits in the basal ganglia for the evaluation and selection of actions

Independent circuits in the basal ganglia for the evaluation and selection of actions

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Exploration of the lamprey pallidal neurons – a combined computational and experimental study

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