Dendritic and parallel processing of visual threats in the retina control defensive responses

Abstract

Approaching predators cast expanding shadows (i.e., looming) that elicit innate defensive responses in most animals. Where looming is first detected and how critical parameters of predatory approaches are extracted are unclear. In mice, we identify a retinal interneuron (the VG3 amacrine cell) that responds robustly to looming, but not to related forms of motion. Looming-sensitive calcium transients are restricted to a specific layer of the VG3 dendrite arbor, which provides glutamatergic input to two ganglion cells (W3 and OFFα). These projection neurons combine shared excitation with dissimilar inhibition to signal approach onset and speed, respectively. Removal of VG3 amacrine cells reduces the excitation of W3 and OFFα ganglion cells and diminishes defensive responses of mice to looming without affecting other visual behaviors. Thus, the dendrites of a retinal interneuron detect visual threats, divergent circuits downstream extract critical threat parameters, and these retinal computations initiate an innate survival behavior.

Center-surround interactions underlie bipolar cell motion sensing in the mouse retina

“…Although few studies have observed BC motion sensitivity, evidence of this feature of BCs is pervasive in the literature in the form of voltage-clamp recordings of glutamatergic synaptic input to RGCs and ACs. In the mouse retina, the glutamatergic input to both SACs and VG-luT3 ACs recorded in response to looming vs. receding stimuli exhibited a strong looming preference (6,32,47), and apparent motion stimuli elicited asymmetric glutamatergic inputs in RGCs (55). In the primate retina, glutamatergic inputs to several types of RGCs were demonstrated to exhibit motion sensitivity (81,86).…”

“…In addition, there was very little directional preference for any cluster in response to stimulation across the full RF. We also found that motion origin sensitivity was not limited to the moving bar stimulus, but that motion-sensitive BCs also preferred looming stimuli to receding stimuli (Fig- 232 ure S3a), suggesting that specific BC types might be impor-233 tant for several types of motion sensing tasks that are known 234 to be performed within the retina (4,6,10). nomenon observed throughout the mammalian visual system (i.e.…”

“…Local motion sensing is of paramount importance for sighted 24 animals, enabling them to detect and capture prey (1)(2)(3)(4), as 25 well as to avoid predators (5)(6)(7)(8)(9). In mammals, multiple fea-26 tures related to motion sensing are first extracted from the first stage in the retina where visual signals diverge into parallel channels, motion detection has not yet been found to be implemented at the BC level.…”

Rod and Cone Connections With Bipolar Cells in the Rabbit Retina

“…Only a subset of OFF bipolar cells receives direct input from rods, namely types 3a, 3b, and 4 in mouse retina (Behrens et al, 2016 ). These stratify in sublamina a of the IPL, just below the cholinergic a band, well-placed to contact OFF alpha ganglion cells, which have been associated with escape behavior in mice (Münch et al, 2009 ; Kim et al, 2020 ). A looming stimulus, such as a hawk, may present as a dark approaching object against a lighter background of sky, i.e., an OFF stimulus.…”

Natural environment statistics in the upper and lower visual field are reflected in mouse retinal specializations

“…92 One recent study showed that VG3 amacrine cells, which feed into several RGC circuits, respond to expanding shadows and thus may be involved in predator detection as well. 93 Overall, this indicates that predator detection presumably relies on multiple RGC channels, including some with small and some with larger RF sizes.…”