Receptive-field organization of monkey superior colliculus.

Cynader, Max S.; Berman, Nancy E.J.

doi:10.1152/jn.1972.35.2.187

Cited by 504 publications

(313 citation statements)

References 26 publications

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“…On the other hand, while CGP injection did not affect the peak firing rate (predrug, 115.4 ± 19.2 Hz vs. CGP, 143.4 ± 25.9 Hz, n = 5; P = 0.124; Fig. 4C1-3 (Dräger and Hubel, 1975;Rhoades and Chalupa, 1977;Wang et al, 2010), cats Cynader, 1972, 1975), and monkeys (Schiller and Koerner, 1971;Cynader and Berman, 1972;Goldberg and Wurtz, 1972;Marrocco and Li, 1977;Moors and Vendrik, 1979), although they did not explicitly describe the pause between the ON and OFF responses. With the use of juxtacellular labeling, we revealed that the ON + Pause + OFF responses were observed in a variety of morphological types of sSC neurons.…”

Section: Gaba a And Gaba B Receptors Cooperatively Generate The Pausementioning

confidence: 96%

“…The majority of sSC neurons reportedly exhibit both ON and OFF responses in response to a static visual stimulus (Schiller and Koerner, 1971; Cynader, 1972, 1975;Cynader and Berman, 1972;Goldberg and Wurtz, 1972;Dräger and Hubel, 1975;Marrocco and Li, 1977;Rhoades and Chalupa, 1977;Moors and Vendrik, 1979;Wang et al, 2010).…”

Section: The Majority Of Ssc Neurons Exhibit On + Pause + Off Responsesmentioning

confidence: 99%

“…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).…”

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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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Section: Gaba a And Gaba B Receptors Cooperatively Generate The Pausementioning

confidence: 96%

Section: The Majority Of Ssc Neurons Exhibit On + Pause + Off Responsesmentioning

confidence: 99%

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confidence: 99%

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

Kaneda

Isa

2013

Neuroscience

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“…Afferents from retina provide a direct input to the superficial layers of the optic tectum, where a retinotopic map is formed (23)(24)(25)(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).…”

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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.

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 recorded from cats under conditions of reversible intubation (2)(3)(4). The responses of 98 units in two cats studied during a total of five recording sessions were compared with those of 248 units in the visual cortex of nine normally reared cats.…”

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confidence: 99%

Cats Reared in Stroboscopic Illumination: Effects on Receptive Fields in Visual Cortex

Cynader¹,

Berman²,

Hein³

1973

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

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Cats were reared in a light-tight box in which the only source of illumination was a 9-psec strobe flash every 2 sec. This allowed them to experience visual form but they did not experience visual movement.Receptive-field properties of single units in area 17 of the visual cortex of cats reared in stroboscopic illumination (strobe-reared) were compared with properties of units in area 17 of normally reared cats. In strobe-reared cats both direction selectivity and orientation selectivity were greatly reduced relative to normally reared cats, and some units in the strobe-reared cats responded only to strobe flashes.

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Receptive-field organization of monkey superior colliculus.

Cited by 504 publications

References 26 publications

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

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

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Cats Reared in Stroboscopic Illumination: Effects on Receptive Fields in Visual Cortex

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