Neuronal circuitry for stimulus selection in the visual system

Abstract

Visual objects naturally compete for the brain's attention, and selecting just one 16 of them for a behavioural response is often crucial for the animal's survival 1 . The 17 neural correlate of such stimulus prioritisation might take the form of a saliency 18 map by which responses to one target are enhanced relative to distractors in 19 other parts of the visual field 2 . Single-cell responses consistent with this type of 20 computation have been observed in the tectum of primates, birds, turtles and 21 lamprey 2-7 . However, the exact circuit implementation has remained unclear. 22Here we investigated the underlying neuronal mechanism presenting larval 23 zebrafish with two simultaneous looming stimuli, each of which was able to 24 trigger directed escapes on their own. Behaviour tracking revealed that the fish 25 respond to these competing stimuli predominantly with a winner-take-all 26 strategy. Using brain-wide functional recordings, we discovered neurons in the 27 tectum whose responses to the target stimulus were non-linearly modulated by 28 the saliency of the distractor. When the two stimuli were presented monocularly 29 in different positions of the visual field, stimulus selection was already apparent 30 in the activity of retinal ganglion cell axons, a likely consequence of antagonistic 31 mechanisms operating outside the classical receptive field 8,9 . When the two 32 stimuli were presented binocularly, i.e., on opposite sides of the fish, our 33 analysis indicates that a loop involving excitatory and inhibitory neurons in the 34 nucleus isthmi (NI) and the tectum weighed stimulus saliencies across 35 hemispheres. Consistent with focal enhancement and global suppression, 36 glutamatergic NI cells branch locally in the tectum, whereas GABAergic NI cells 37 project broadly across both tectal hemispheres. Moreover, holographic 38 optogenetic stimulation confirmed that glutamatergic NI neurons can modulate 39 visual responses in the tectum. Together, our study shows, for the first time, 40 context-dependent contributions of retinotectal and isthmotectal circuits to the 41 computation of the visual saliency map, a prerequisite for stimulus-driven, 42 bottom-up attention. 43Dark, looming stimuli are strongly aversive stimuli for zebrafish larvae 10,11 and other 44 animals 12,13 , probably mimicking an approaching predator or an object on a collision 45 course. In our setup, single looming disks presented from below and on one side of a 46 free-swimming animal were highly effective in driving an escape response to the 47GABAGABA ? Midline Excitatory tectal neurons Inhibitory tectal neurons Eye NI Tectum NI Fee bac ro ections (NI to tectum) Tectum to NI

A neural circuit basis for binasal input-enhanced chemosensory avoidance

“…These include chemosensory behaviors, alongside phototaxis, oculomotor and optokinetic responses, prey capture and various escape responses (Kalueff et al, 2013; Loring et al, 2020). With a relatively small, transparent brain that comprises a more tractable number of neurons (~10 5 ), much has been learnt about the circuitries mediating sensory processing and sensorimotor behaviors in larval zebrafish (Ahrens et al, 2012; Bahl and Engert, 2020; Chen et al, 2018; Dragomir et al, 2020; Fernandes et al, 2020; Gebhardt et al, 2019; Haesemeyer et al, 2018; Herrera et al, 2020; Kawashima et al, 2016; Knogler et al, 2017; Lacoste et al, 2015; Lovett-Barron et al, 2020; Migault et al, 2018; Naumann et al, 2016; Portugues et al, 2014; Vanwalleghem et al, 2020; Wee et al, 2019; Wolf et al, 2017; Yao et al, 2016; Zhang et al, 2017). Larval zebrafish also offers a unique opportunity for studying the brainwide organizational principles of neural circuits mediating bilateral sensory input integration.…”

Neural encoding models for multivariate optical imaging data

“…Multiplicative modulation of activity is thought to be fundamental to neural computation [9,184]. In zebrafish tectum, an example of this effect has been identified in recent work from Fernandes et al [185]. By expressing channelrhodopsin in glutamatergic cells in the nucleus isthmus, Fernandes et al could simultaneously optogenetically stimulate isthmic neurons and two-photon image tectal neurons.…”

“…The second hypothesis is that these factors correspond to afferent projections from other structures ( Figure 6.1, right). For example, glutamatergic isthmic neurons downstream of the tectum feed contextual information back to tectal neurons [185], and their persistent activity Figure 6.1: Hypothetical latent sources of spontaneous activity. Under the "recurrent circuitry" hypothesis, latent structure underlying spontaneous activity arises due to strong recurrent connections.…”

Visual learning and its underlying neural substrate in two species of teleost fish (Zebrafish and Ambon damselfish)

“…Very recent studies have described this nucleus responses to looming stimuli in larval zebrafish. These researches found that the nucleus isthmi is involved in the discriminating the most salient loom, that its optogenetic stimulatin modulates visual responses in the tectum, and that its ablation alters contrast sensitivity to looms (Fernandes et al, 2019;Henriques et al, 2019). The interconnections between the nucleus isthmi and the optic tectum are highly conserved across vertebrates (Kunzle and Schnyder, 1984;Gruberg et al, 2006;Dudkin and Gruberg, 2009), and are considered to be involved in detecting salient stimuli and in maintaining visual attention (Basso and May, 2017).…”

“…Among the structures of the tegmentum, it is likely that some of these nodes represent connections to the nucleus isthmi. This structure is reciprocally connected to the tectum, is sensitive to looms, and is related to the detection of relevant visual stimuli (Vanegas and Ito, 1983;Striedter and Northcutt, 1989;King and Schmidt, 1993;Northmore and Gallagher, 2003;Gallagher and Northmore, 2006;Fernandes et al, 2019;Henriques et al, 2019). The failure of its connections to decrease, as in the WTs, could be important to understand the behavioural effects seen in free-swimming larvae and the rest of the circuit.…”