Direction selectivity in the larval zebrafish tectum is mediated by asymmetric inhibition

Abstract

The extraction of the direction of motion is an important computation performed by many sensory systems and in particular, the mechanism by which direction-selective retinal ganglion cells (DS-RGCs) in the retina acquire their selective properties, has been studied extensively. However, whether DS-RGCs simply relay this information to downstream areas or whether additional and potentially de novo processing occurs in these recipient structures is a matter of great interest. Neurons in the larval zebrafish tectum, the largest retino-recipent area in this animal, show direction-selective (DS) responses to moving visual stimuli but how these properties are acquired is still unknown. In order to study this, we first used two-photon calcium imaging to classify the population responses of tectal cells to bars moving at different speeds and in different directions. Subsequently, we performed in vivo whole cell electrophysiology on these DS tectal neurons and we found that their inhibitory inputs were strongly biased toward the null direction of motion, whereas the excitatory inputs showed little selectivity. In addition, we found that excitatory currents evoked by a stimulus moving in the preferred direction occurred before the inhibitory currents whereas a stimulus moving in the null direction evoked currents in the reverse temporal order. The membrane potential modulations resulting from these currents were enhanced by the spike generation mechanism to generate amplified direction selectivity in the spike output. Thus, our results implicate a local inhibitory circuit in generating direction selectivity in tectal neurons.

Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish

“…The OT, by far the largest contiguous larval visual brain structure, is recurrently connected across its laminar architecture and receives direct input from the majority of retinal projections (Burrill and Easter, 1994) in addition to indirect input from accessory visual areas (Vanegas and Ito, 1983). Neurons in the OT show direction, orientation, speed, and size selectivity (Gabriel et al, 2012; Grama and Engert, 2012; Hunter et al, 2013; Niell and Smith, 2005) and respond to aversive (predator-like) and appetitive (prey-like) visual cues in many animals (Dean et al, 1989; Ewert, 1997; Muto et al, 2013). Furthermore, OT neurons in birds (Winkowski and Knudsen, 2008), tadpoles (Khakhalin et al, 2014), frogs (Baranauskas et al, 2012), and fish (Niell and Smith, 2005) respond to looming stimuli.…”

Visually guided gradation of prey capture movements in larval zebrafish

“…This suggests a pre-calculated gradation in behavior based on the perceived distance of the prey item. There are certainly computational mechanisms that could accomplish this, such as the direction, orientation and size selectivity of tectal neurons (Del Bene et al, 2010;Gabriel et al, 2012;Grama and Engert, 2012;Niell and Smith, 2005;. How these mechanisms help calculate distance or direction of travel of paramecia is unknown.…”

Anatomical and functional analysis of non-retinal tectal afferents in larval zebrafish

“…These stimuli were presented in different contrasts, sizes, and directions, to determine whether there was any selectivity in how neurons in the thalamus responded to these parameters. This mirrors similar work previously done for the tectum (Gabriel et al, 2012;Grama and Engert, 2012;Hunter et al, 2013;Abbas and Meyer, 2014). These data show strong responses among thalamic neurons to a dark-on-light loom stimulus, with few if any responses to other stimuli (Figure 4.2).…”