Neurons in the Most Superficial Lamina of the Mouse Superior Colliculus Are Highly Selective for Stimulus Direction

Abstract

The superior colliculus (SC) is a layered midbrain structure important for multimodal integration and sensorimotor transformation. Its superficial layers are purely visual and receive depth-specific projections from distinct subtypes of retinal ganglion cells. Here we use two-photon calcium imaging to characterize the response properties of neurons in the most superficial lamina of the mouse SC, an undersampled population with electrophysiology. We find that these neurons have compact receptive fields with primarily overlapping ON and OFF subregions and are highly direction selective. The high selectivity is observed in both excitatory and inhibitory neurons. These neurons do not cluster according to their direction preference and lack orientation selectivity. In addition, we perform single-unit recordings and show that direction selectivity declines with depth in the SC. Together, our experiments reveal for the first time a highly specialized lamina in the most superficial SC for movement direction, a finding that has important implications for understanding signal transformation in the early visual system.

Two Pairs of ON and OFF Retinal Ganglion Cells Are Defined by Intersectional Patterns of Transcription Factor Expression

“…It remains unclear whether direction-selective units in higher image-forming centers, such as superior colliculus, dorsal lateral geniculate nucleus, and visual cortex, inherit their selectivity from direction-selective RGCs in retina or compute it de novo (Cruz-Martín et al, 2014; Inayat et al, 2015; Marshel et al, 2012; Priebe et al, 2006; Rochefort et al, 2011). Discussions of this issue in mouse have focused on five previously identified direction-selective RGCs that project to image-forming centers: four types of ooDSGCs, which are similar in structure and physiological properties, but differ in preferred directions (ventral, dorsal, nasal and temporal; (Borst and Helmstaedter, 2015; Vaney et al, 2012) and ventrally-preferring J-RGCs, the single population of OFF direction-selective RGCs identified to date (Kim et al, 2008, 2010).…”

Functional imaging of neuronal activity of auditory cortex by using Cal-520 in anesthetized and awake mice

“…Cal-520 is a recently reported synthetic Ca 2+ indicator that has such required properties [26]. It has been used in studies of the neocortex, such as barrel and auditory cortices in anesthetized animals [26,37], subcortical regions such as the superior colliculus [38], and the cerebellum [26,39]. In cultured human neuroblastoma SH-SY5Y cells, Cal-520 has been demonstrated to be an optimal indicator for tracking localized subcellular changes, as compared with other synthetic Ca 2+ dyes including OGB-1 and fluo-8 and three GECIs (GCaMP6-slow, -medium and -fast variants) [40].…”

An NMDA receptor-dependent mechanism for subcellular segregation of sensory inputs in the tadpole optic tectum

“…This patterning motif is found in many brain structures that receive multiple sets of afferent input. For example, the different sensory inputs that are received and processed by the optic tecta of birds (Acheson et al, 1980; Yamagata et al, 1995), fish (Xiao et al, 2005; Xiao and Baier, 2007), and amphibians (Harris, 1982, 1983; Udin and Fawcett, 1988; Deeg et al, 2009; Hiramoto and Cline, 2009), and the superior colliculus of mammals (May, 2006; Wallace et al, 1993; Cang and Feldheim, 2013; Inayat et al, 2015), form distinct layers across the laminar axis of their target neuropil. In the lateral geniculate nucleus (LGN), retinal ganglion cell input is segregated into eye-specific layers (Rakic, 1976; Linden et al, 1981; Shatz, 1983), and in the hippocampus, entorhinal cortical input forms synaptic connections onto specifically the distal regions of hippocampal pyramidal neurons, while the commissural inputs from within the hippocampus synapse onto the proximal portions of the same dendrites (Supèr and Soriano, 1994).…”