Neural Mechanisms Mediating Motion Sensitivity in Parasol Ganglion Cells of the Primate Retina

Manookin, Michael B.; Patterson, Sara S.; Linehan, Conor M.

doi:10.1016/j.neuron.2018.02.006

Cited by 76 publications

(72 citation statements)

References 108 publications

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“…In some cases, additional D-glucose (14 mmol) was added to the Ames' medium. 49 Ganglion cell spikes were measured with extracellular or loose-patch recordings using an Ames-filled borosilicate pipette. The data was sampled at 10 kHz (Multiclamp 700B, Molecular Devices), Bessel filtered at 3 kHz and digitized using an ITC-18 analog-digital board (HEKA Instruments).…”

Section: Recordingmentioning

confidence: 99%

An S-cone circuit for edge detection in the primate retina

Patterson

Kuchenbecker

Anderson

et al. 2019

Preprint

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Midget retinal ganglion cells (RGCs) are the most common RGC type in the primate retina. Their responses mediate both color and spatial vision, yet the specific links between midget RGC responses and visual perception are unclear. Previous research on the dual roles of midget RGCs has focused on those comparing long (L) vs. middle (M) wavelength sensitive cones. However, there is evidence for several other rare midget RGC subtypes receiving S-cone input, but their role in color and spatial vision is uncertain. Here, we confirm the existence of the single S-cone center OFF midget RGC circuit in the central retina of macaque monkey both structurally and functionally, by combining single cell electrophysiology with 3D electron microscopy reconstructions of the upstream circuitry. Like the well-studied L vs. M midget RGCs, the S-OFF midget RGCs have a centersurround receptive field consistent with a role in spatial vision. While spectral opponency in a primate RGC is classically assumed to contribute to hue perception, a role supporting edge detection is more consistent with the S-OFF midget RGC receptive field structure and studies of hue perception.

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Section: Recordingmentioning

confidence: 99%

An S-cone circuit for edge detection in the primate retina

Patterson

Kuchenbecker

Anderson

et al. 2019

Preprint

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“…DS neurons are found throughout the visual system, including the retina, where direction-selective ganglion cells (DSGCs) relay motion information to several downstream targets such as the superior colliculus, the dorsal lateral geniculate nucleus (dLGN) and the accessory optic system[6]. In primates, motion encoding begins in the retina[7], but also relies on higher cortical areas MT and MST[8,9]. While DS responses have been observed in mouse visual cortex[10–14], the role of these areas in motion perception is unknown.…”

Section: Introductionmentioning

confidence: 99%

A Role for Mouse Primary Visual Cortex in Motion Perception

et al. 2018

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Visual motion is an ethologically important stimulus throughout the animal kingdom. In primates, motion perception relies on specific higher-order cortical regions. Although mouse primary visual cortex (V1) and higher-order visual areas show direction-selective (DS) responses, their role in motion perception remains unknown. Here, we tested whether V1 is involved in motion perception in mice. We developed a head-fixed discrimination task in which mice must report their perceived direction of motion from random dot kinematograms (RDKs). After training, mice made around 90% correct choices for stimuli with high coherence and performed significantly above chance for 16% coherent RDKs. Accuracy increased with both stimulus duration and visual field coverage of the stimulus, suggesting that mice in this task integrate motion information in time and space. Retinal recordings showed that thalamically projecting On-Off DS ganglion cells display DS responses when stimulated with RDKs. Two-photon calcium imaging revealed that neurons in layer (L) 2/3 of V1 display strong DS tuning in response to this stimulus. Thus, RDKs engage motion-sensitive retinal circuits as well as downstream visual cortical areas. Contralateral V1 activity played a key role in this motion direction discrimination task because its reversible inactivation with muscimol led to a significant reduction in performance. Neurometric-psychometric comparisons showed that an ideal observer could solve the task with the information encoded in DS L2/3 neurons. Motion discrimination of RDKs presents a powerful behavioral tool for dissecting the role of retino-forebrain circuits in motion processing.

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“…Most physiological studies have been performed on the five numerically dominant primate RGC types, ON and OFF midget (Dacey, 1993a), ON and OFF parasol (Chichilnisky and Kalmar, 2002), and small bistratified (Chichilnisky and Baylor, 1999;Dacey, 1993b;Field et al, 2007), which make up about 75% of the visual signal. These cells are usually characterized as exhibiting classical Gaussian center-surround receptive field (RF) structure, with relatively little evidence for specialized functional properties such as those found in mouse RGCs (Crook et al, 2008;Enroth-Cugell and Robson, 1966;Kuffler, 1953;Rodieck, 1998), but see (Manookin et al, 2018). The function of visual signaling in the remaining low-density RGC types remains largely unknown .…”

Section: Introductionmentioning

confidence: 99%

Unusual physiological properties of two ganglion cell types in primate retina

Rhoades

Shah

Manookin

et al. 2018

Preprint

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The visual functions of the diverse retinal ganglion cell types in the primate retina, and the parallel visual pathways they initiate, remain poorly understood. Here, the unusual physiological and computational properties of the ON and OFF smooth monostratified (SM) ganglion cells are explored. Large-scale multi-electrode recordings from 48 macaque retinas revealed that these cells exhibited strikingly irregular receptive field structure composed of spatially segregated hotspots, quite different from the receptive fields of previously described retinal ganglion cell types. The ON and OFF SM cells are paired cell types, but OFF SM cells exhibited stronger hotspot structure than ON cells. Targeted visual stimulation and computational inference demonstrate strong nonlinear subunit properties of each hotspot that contributed to the signaling properties of SM cells. Analysis of shared inputs to neighboring SM cells indicated that each hotspot could not be explained by an individual presynaptic input. Surprisingly, visual stimulation of different hotspots produced subtly different spatiotemporal spike waveforms in the same SM cell, consistent with a dendritic contribution to hotspot structure. These findings point to a previously unreported nonlinear mechanism in the output of the primate retina that contributes to signaling spatial information. Receptive field properties of simultaneously recorded retinal ganglion cell typesTo explore the properties of poorly understood RGC types, large-scale multi-electrode recordings were used to simultaneously record the light responses of hundreds of RGCs

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Neural Mechanisms Mediating Motion Sensitivity in Parasol Ganglion Cells of the Primate Retina

Cited by 76 publications

References 108 publications

An S-cone circuit for edge detection in the primate retina

An S-cone circuit for edge detection in the primate retina

A Role for Mouse Primary Visual Cortex in Motion Perception

Unusual physiological properties of two ganglion cell types in primate retina

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