Role of intrinsic synaptic circuitry in collicular sensorimotor integration

Lee, Psyche H.; Helms, Matthew C.; Augustine, George J; Hall, William C.

doi:10.1073/pnas.94.24.13299

Cited by 117 publications

(111 citation statements)

References 39 publications

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“…3A, dotted red line). Such an integration mechanism is compatible with the neuroanatomical structure of the SC with well characterized sensory and motor layers and a functional connection (Lee et al, 1997).…”

Section: Resultsmentioning

confidence: 61%

Computational Modeling of Collicular Integration of Perceptual Responses and Attention in Microsaccades

Engbert

2012

Journal of Neuroscience

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During visual fixation on a target object, our eyes are not motionless but generate slow fixational eye movements and microsaccades. Effects of visual attention have been observed in both microsaccade rates and spatial directions. Experimental results, however, range from early (Ͻ200 ms) to late (Ͼ600 ms) effects combined with cue-congruent as well as cue-incongruent microsaccade directions. On the basis of well characterized neural circuitry in superior colliculus, we construct a dynamical model of neural activation that is modulated by perceptual input and visual attention. Our results show that additive integration of low-level perceptual responses and visual attention can explain microsaccade rate and direction effects across a range of visual cueing tasks. These findings suggest that the patterns of microsaccade direction observed in experiments are compatible with a single dynamical mechanism. The basic principles of the model are highly relevant to the general problem of integration of low-level perception and top-down selective attention.

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Section: Resultsmentioning

confidence: 61%

Computational Modeling of Collicular Integration of Perceptual Responses and Attention in Microsaccades

Engbert

2012

Journal of Neuroscience

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“…The in vitro studies did show that single-pulse stimulation of the sSC induces synaptic responses in dSC neurons that are amplified into strong bursting spike responses and long-lasting depolarization when GABA A -mediated inhibition is suppressed (Lee et al, 1997(Lee et al, , 2001Isa et al, 1998;Saito and Isa, 2003).…”

Section: Introductionmentioning

confidence: 99%

“…The circuits that organize this activity have been studied in vitro in slice preparations (for review, see Isa and Saito, 2001;Grantyn et al, 1984;Lee et al, 1997Lee et al, , 2007Isa et al, 1998;Meredith and Ramoa, 1998;Lo and Mize, 2000;Schmidt et al, 2001;Isa, 2002;Isa and Sparks, 2006;Neale and Salt, 2006;Kaneda et al, 2008). Furthermore, profiles of field potential responses at different depths evoked by sSC stimulation were measured by single-electrode recordings in anesthetized rats (Katsuta and Isa, 2003) and monkeys (Nikitin and Isa, 2004).…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal Profiles of Field Potentials in Mouse Superior Colliculus Analyzed by Multichannel Recording

Phongphanphanee¹,

Kaneda²,

Isa³

2008

J. Neurosci.

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The onset and vector of orienting behaviors, such as saccades, are controlled by commands that descend from a population of neurons in deep layers of the superior colliculus (dSC). In this study, to characterize the role of the collicular local circuitry that generates the spatiotemporal pattern of command activity in the dSC neuronal population, responses evoked by single-pulse electrical stimulation in superficial layers of the superior colliculus (sSC) were analyzed by a 64-channel field potential recording system (planar electrode, 8 ϫ 8 pattern; 150 m interelectrode spacing) in slices obtained from 16-to 22-d-old mice. A negative field potential with short latency and short duration spatially restricted to the recording sites in sSC was evoked adjacent to the stimulation site. After bath application of 10 M bicuculline, the same stimulus induced a large negative field response with long duration that spread from sSC to dSC. The dSC potential initially showed a positive response, presumably because of reversal of the negative potential that originated in sSC, and then a long negative response that spread horizontally as far as 1 mm. These responses disappeared after application of an NMDA receptor antagonist, 2-amino-5-phosphonovelarate, indicating that NMDA receptors have an important role in the generation of these responses. Simultaneous whole-cell patch-clamp recordings showed that the long-lasting negative field potentials corresponded to the depolarization accompanying burst spike activity of SC neurons. The present study revealed an extensive excitatory network in the dSC that may contribute to the generation of activity by a large population of neurons that discharge before a saccade.

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“…This is probably due to the high percentage of GABAergic neurons in the sSC (Okada, 1974). Thus, it is most likely that both excitatory and inhibitory neurons were included in the experiments of (Lee et al, 1997;Isa et al, 1998;Kaneda et al, 2008).…”

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confidence: 99%

GABAergic mechanisms for shaping transient visual responses in the mouse superior colliculus

Kaneda

Isa

2013

Neuroscience

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An object that suddenly appears in the visual field should be quickly detected and responded to because it could be beneficial or harmful. The superficial layer of the superior colliculus (sSC) is a brain structure capable of such functions, as sSC neurons exhibit sharp transient spike discharges with short latency in response to the appearance of a visual stimulus.However, how transient activity is generated in the sSC is poorly understood. Here, we show that inhibitory inputs actively shape transient activity in the sSC. Juxtacellular recordings from anesthetized mice demonstrate that almost all types of sSC neurons, which were identified by post hoc histochemistry, show transient spike discharges, i.e., ON activity, immediately after visual stimulus onset. ON activity was followed by a pause before the visual stimulus was turned off. To determine whether the pause reflected the absence of excitatory drive or inhibitory conductance, we injected depolarizing currents juxtasomally, which enabled us to observe inhibition as decreased discharges. The pause was observed even under this condition, suggesting that inhibitory input caused the pause. We further found that local application of a mixture of gamma aminobutyric acid (GABA) A and GABA B receptor antagonists additively diminished the pause. These results indicate that GABAergic inputs produce transient ON responses by attenuating excitatory activity through the cooperative activation of GABA A and GABA B receptors, allowing sSC neurons to act as a saliency detector. Detecting an object that suddenly appears in the visual field is crucial for animals because their survival may depend on whether the object is beneficial or harmful. Transient, but not persistent, spike discharges in the sensory systems should encode the detection of the appearance. One of the candidate nuclei for this function is the superior colliculus (SC), a midbrain structure that is critical for visuomotor information processing (Sparks, 1986;Isa and Sparks, 2006). The superficial layer of the SC (sSC) receives visual inputs from the retina and the primary visual cortex (V1) in a retinotopically organized manner (Dräger and Hubel, 1976;May, 2006). sSC neurons exhibit transient spike discharges, called ON responses, immediately after the appearance of a visual stimulus (Schiller and Koerner, 1971; Cynader, 1972, 1975;Cynader and Berman, 1972;Goldberg and Wurtz, 1972;Dräger and Hubel, 1975;Rhoades and Chalupa, 1977;Marrocco and Li, 1977;Moors and Vendrik, 1979;Wang et al., 2010), implying that the sSC could detect the appearance of the object. Indeed, lesions or inactivation of the SC cause a detection deficit of visual stimuli (Butter et al., 1978;Overton and Dean, 1988;Fitzmaurice et al., 2003).The sSC consists of several cell types, including excitatory and inhibitory neurons (Mize, 1992;Endo et al., 2003Endo et al., , 2005May, 2006;Kaneda et al., 2008). Previous intracellular recording and labeling studies elucidated that some sSC neurons responded to moving or static visual stim...

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Role of intrinsic synaptic circuitry in collicular sensorimotor integration

Cited by 117 publications

References 39 publications

Computational Modeling of Collicular Integration of Perceptual Responses and Attention in Microsaccades

Computational Modeling of Collicular Integration of Perceptual Responses and Attention in Microsaccades

Spatiotemporal Profiles of Field Potentials in Mouse Superior Colliculus Analyzed by Multichannel Recording

GABAergic mechanisms for shaping transient visual responses in the mouse superior colliculus

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