Nigral Inhibition of GABAergic Neurons in Mouse Superior Colliculus

Kaneda, Katsuyuki; Isa, Kaoru; Yanagawa, Yuchio; Isa, Tadashi

doi:10.1523/jneurosci.3263-08.2008

Cited by 83 publications

(66 citation statements)

References 52 publications

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“…Since electrical activity in the SC is regulated by GABA (Chevalier et al, 1985; Chevalier and Deniau, 1990; Hall and Lee, 1993; Lee et al, 2001, 2007; Behan et al, 2002; Kaneda et al, 2008; Isa and Hall, 2009), we tested the actions of two GABA A receptor antagonists, bicuculline (50 μ m) and gabazine (SR95531, 5 μ m) (bicuculline and gabazine were used interchangeably and the results combined). These drugs generally increased the amplitude of optical signals, but had the greatest effects on after-depolarizations (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…However, the after-depolarization is shaped by GABA A receptor mediated inhibition and it is likely that prolonged bursting by GABAergic horizontal cells curtails prolonged bursting of narrow-field and wide-field vertical cells. Previous studies have shown enhanced excitatory responses in the SC following GABA A receptor blockade (Isa et al, 1998; Özen et al, 2000; Saito and Isa, 2003; Kaneda et al, 2008; Phongphanphanee et al, 2008). Our results are consistent with these results, but indicate that each temporal component of the optical signal is modulated by GABA A receptors differently.…”

Section: Discussionmentioning

confidence: 98%

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Intralaminar and Interlaminar Activity within the Rodent Superior Colliculus Visualized with Voltage Imaging

Vokoun¹,

Jackson²,

Basso³

2010

J. Neurosci.

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The superior colliculus (SC) is a midbrain structure that plays a role in converting sensation into action. Most SC research focuses on either in vivo extracellular recordings from behaving monkeys or patch-clamp recordings from smaller mammals in vitro. However, the activity of neuronal circuits is necessary to generate behavior, and neither of these approaches measures the simultaneous activity of large populations of neurons that make up circuits. Here, we describe experiments in which we measured changes in membrane potential across the SC map using voltage imaging of the rat SC in vitro. Our results provide the first high temporal and spatial resolution images of activity within the SC. Electrical stimulation of the SC evoked a characteristic two-component optical response containing a short latency initial-spike and a longer latency after-depolarization. Single-pulse stimulation in the superficial SC evoked a pattern of intralaminar and interlaminar spread that was distinct from the spread evoked by the same stimulus applied to the intermediate SC. Intermediate layer stimulation produced a more extensive and more ventrally located activation of the superficial layers than did stimulation in the superficial SC. Together, these results indicate the recruitment of dissimilar subpopulations of circuitry depending on the layer stimulated. Field potential recordings, pharmacological manipulations, and timing analyses indicate that the patterns of activity were physiologically relevant and largely synaptically driven. Therefore, voltage imaging is a powerful technique for the study of spatiotemporal dynamics of electrical signaling across neuronal populations, providing insight into neural circuits that underlie behavior.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 98%

Intralaminar and Interlaminar Activity within the Rodent Superior Colliculus Visualized with Voltage Imaging

Vokoun¹,

Jackson²,

Basso³

2010

J. Neurosci.

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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%

“…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). In rodents, it has also been shown that GABAergic neurons in the deep layer of tectum/colliculus are under nigral inhibition and that this inhibition is topographically organized in register (58,61). To what extent the basal ganglia influence processing in tectum by disinhibition of local GABAergic neurons is as yet not clear.…”

Section: Discussionmentioning

confidence: 99%

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Kardamakis

Saitoh

Grillner

2015

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

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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“…These models have argued that disinhibition of target nuclei is critical to movement, consistent with targeting of nigral projections to excitatory projection neurons in the colliculus (Jiang et al, 2003). However, a recent study has demonstrated that nigral projection neurons may also synapse on inhibitory neurons in the superior colliculus (Kaneda et al, 2008), thus complicating a simple disinhibition model (Basso and Sommer, 2011).…”

Section: Projections From the Substantia Nigra Pars Reticulatamentioning

confidence: 97%