Wiring subcortical image-forming centers: Topography, laminar targeting, and map alignment

Johnson, Kristy O.; Triplett, Jason W.

doi:10.1016/bs.ctdb.2020.10.004

Cited by 5 publications

(4 citation statements)

References 130 publications

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“…One potential source for inhibition could be GABAergic RGCs, a subset of which project to the SC (32,33). Alternatively, multiple visual cortical areas project topographically to the SC and in alignment with the retinocollicular map (34), providing one potential source of binocular input. However, studies have shown that binocular integration in the dLGN is independent of cortical feedback (23,35).…”

Section: Discussionmentioning

confidence: 99%

Diverse modes of binocular interactions in the mouse superior colliculus

Russell

Triplett

2020

Preprint

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A central role of the visual system is to integrate inputs from both eyes to form one coherent visual perception. The superior colliculus (SC) plays a central role in visual processing, gaze orientation and vergence eye movements necessary for binocular vision. Indeed, the SC receives direct inputs from both the contralateral and ipsilateral eye and binocularly-modulated neurons have been identified in the SC of multiple species. However, evidence for binocular processing in rodents, particularly mice, has not been functionally confirmed. In this study we recorded visually-evoked activity in the mouse SC while presenting visual stimuli to each eye individually or both together and reveal a surprising diversity of binocularly-modulated responses. Strikingly, we found that ~2/3 of all identified neurons in the anteromedial SC were binocularly-modulated. Furthermore, we identified four binocular subtypes based on their differential responses under varying ocularities of stimulus presentation. Interestingly, we found both orientation- and direction- selective (OS and DS, respectively) neurons in all four binocular subtypes. And, tuning properties of binocular neurons were distinct from neighboring monocular neurons, exhibiting more linear spatial summation. Together, these data suggest that binocular neurons are prevalent in the anteromedial SC of the mouse. Additionally, the distinct tuning properties of binocular neurons suggest a previously unappreciated complexity of visual processing in the SC, which may contribute to binocular perception.

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Section: Discussionmentioning

confidence: 99%

Diverse modes of binocular interactions in the mouse superior colliculus

Russell

Triplett

2020

Preprint

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“…The mechanisms underlying the development of retinotopic maps have been most intensely studied in the contra-RGC projections to the SC (Triplett and Feldheim 2012; Cang and Feldheim 2013;Johnson and Triplett 2021;Tomar et al 2023). In mice, contra-RGC axons reach the rostral end of the SC at E16 and grow across to the caudal end by P2.…”

Section: Retinotopic Organization In Scmentioning

confidence: 99%

“…Following RGC innervation and refinement in the first postnatal week, axons from layer 5 neurons in V1 reach SC starting at P6 and refine their termination zones by P12 in alignment with the retinal input map. The topographic refinement of the cortical input is instructed by the retinal projection (Johnson and Triplett 2021) and depends on ephrin-A gradients (Savier et al 2017) and activity (Triplett et al 2009). Interestingly, the refinement of V1 projections but not retinal projections to SC depends on postsynaptic NMDA receptors (Johnson et al 2023).…”

Section: Retinotopic Alignment Of Feedforward and Feedback Connection...mentioning

confidence: 99%

Mapping the Retina onto the Brain

Kerschensteiner,

Feller

2023

Cold Spring Harb Perspect Biol

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Vision begins in the retina, which extracts salient features from the environment and encodes them in the spike trains of retinal ganglion cells (RGCs), the output neurons of the eye. RGC axons innervate diverse brain areas (>50 in mice) to support perception, guide behavior, and mediate influences of light on physiology and internal states. In recent years, complete lists of RGC types (∼45 in mice) have been compiled, detailed maps of their dendritic connections drawn, and their light responses surveyed at scale. We know less about the RGCs' axonal projection patterns, which map retinal information onto the brain. However, some organizing principles have emerged. Here, we review the strategies and mechanisms that govern developing RGC axons and organize their innervation of retinorecipient brain areas.

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“…Retinal ganglion cells (RGCs) project to two main image forming regions, the superior colliculus (SC) and the dorsal lateral geniculate nucleus (dLGN), where their axon terminals are organized topographically. The establishment of topography occurs in a protracted process during the first week of postnatal life in the mouse ( Johnson and Triplett, 2021 ). Initially, diffuse terminations are refined to topographically appropriate locations in a manner dependent on a combination of molecular cues ( Feldheim and O’Leary, 2010 ), axon-axon competition ( Triplett et al, 2011 ), and neuronal activity ( McLaughlin et al, 2003 ; Pfeiffenberger et al, 2006 ).…”

Section: Introductionmentioning

confidence: 99%

NMDA Receptor Expression by Retinal Ganglion Cells Is Not Required for Retinofugal Map Formation nor Eye-Specific Segregation in the Mouse

Johnson

Smith

Goldstein³

et al. 2021

eNeuro

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Retinal ganglion cells (RGCs) project topographically to the superior colliculus (SC) and dorsal lateral geniculate nucleus (dLGN). Spontaneous activity plays a critical role in retinotopic mapping in both regions; however, the molecular mechanisms underlying activity-dependent refinement remain unclear. Previous pharmacologic studies implicate NMDA receptors (NMDARs) in the establishment of retinotopy. In other brain regions, NMDARs are expressed on both the pre-and post-synaptic side of the synapse, and recent work suggests that pre-synaptic and post-synaptic NMDARs play distinct roles in retinotectal developmental dynamics. To directly test the role of NMDARs expressed by RGCs in retinofugal map formation, we took a conditional genetic knockout approach to delete the obligate GluN1 subunit of NMDARs in RGCs. Here, we demonstrate reduced GluN1 expression in the retina of Chrnb3-Cre;GluN1 flox/flox (pre-cKO) mice without altered expression in the SC. Anatomical tracing experiments revealed no significant changes in termination zone size in the SC and dLGN of pre-cKO mice, suggesting NMDAR function in RGCs is not an absolute requirement for topographic refinement. Further, we observed no change in the eye-specific organization of retinal inputs to the SC nor dLGN. To verify that NMDA induces activity in RGC terminals, we restricted GCaMP5 expression to RGCs and confirmed induction of calcium transients in RGC terminals. Together, these findings demonstrate that NMDARs expressed by RGCs are not required for retinofugal topographic map formation nor eye-specific segregation in the mouse. 4 Significance StatementTopographic organization of retinal inputs in the brain is thought to be critical for the efficient relay of spatial information in the visual scene. Previous studies suggest NMDARs play a crucial role in establishing topography in the superior colliculus; however, these studies could not distinguish between potential pre-or post-synaptic roles. Here, we show NMDAR function in retinal ganglion cells (RGCs) is not required for the establishment of topography. Further, we find RGC NMDARs are not required to establish or maintain eye-specific laminae in retinorecipient regions.

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Wiring subcortical image-forming centers: Topography, laminar targeting, and map alignment

Cited by 5 publications

References 130 publications

Diverse modes of binocular interactions in the mouse superior colliculus

Diverse modes of binocular interactions in the mouse superior colliculus

Mapping the Retina onto the Brain

NMDA Receptor Expression by Retinal Ganglion Cells Is Not Required for Retinofugal Map Formation nor Eye-Specific Segregation in the Mouse

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