Behavioral signatures of a developing neural code

Abstract

During early life neural codes must develop to appropriately transform sensory inputs into behavioral outputs. Here we demonstrate a direct link between the maturity of neural coding in the visual brain and developmental changes in visually-guided behavior. In zebrafish larvae we show that visuallydriven hunting behavior improves from 4 to 15 days post-fertilization, becoming faster and more accurate. During the same period population activity in the optic tectum refines, leading to improved decoding and information transmission of spatial position, particularly in the representation of the frontal visual field. Remarkably, individual differences in decoding can predict each fish's hunting success. Together these results show how the neural codes required to subserve a natural behavior emerge during development.

From perception to behavior: The neural circuits underlying prey hunting in larval zebrafish

“…Bianco and Engert, 2015), and disruption of signaling in the visual pathway impairs the larva's ability to hunt (Gahtan et al, 2005;Del Bene et al, 2010;Semmelhack et al, 2014). The precise movements made by larvae during hunting are largely determined by prey location and movement; for instance initial turning speed and magnitude depend on prey location at detection (Patterson et al, 2013;Bolton et al, 2019;Avitan et al, 2020;Mearns et al, 2020), and subsequent bout selection is based on a tight stimulus-response loop (Mearns et al, 2020). Motor commands are carried downstream by the reticulospinal system, and are then translated into motor patterns via spinal cord circuitry (McLean et al, 2007;Bagnall and McLean, 2014;Berg et al, 2018).…”

“…These neurons show selectivity to stimulus size, facilitating prey selection (Del Bene et al, 2010;Preuss et al, 2014). Most tectal neurons reside in the periventricular layer (PVL) where visually-responsive neurons are tuned for different parts of the visual field in a topographic manner (Niell and Smith, 2005;Kita et al, 2015;Romano et al, 2015;Avitan et al, 2020), and show mixed selectivity to prey-related visual features (Bianco and Engert, 2015;Thompson and Scott, 2016;Helmbrecht et al, 2018). Tectal neurons project to multiple brain regions via the ipsilateral tectobulbar tract (iTB) (Henriques et al, 2019;Oldfield et al, 2020;Fernandes et al, 2021).…”

“…Hunting behavior begins at 4-5 dpf, shortly after larval zebrafish start to swim. Larval swimming motions consist of brief (≈100-180 ms) bouts of activity followed by inactivity lasting up to 1-2 s. A typical hunting event takes about 1-3 s and consists of about 1-10 bouts; the magnitude and variability of these numbers decrease over development (Avitan et al, 2020). Larval swim bouts can be clustered into roughly 7-13 specific types (Marques et al, 2018;Mearns et al, 2020).…”

“…Eye convergence serves to create a small binocular zone directly in front of the fish termed the strike zone (Gahtan et al, 2005;Bianco et al, 2011;Patterson et al, 2013). While this is clearly useful for the final bouts of the hunting sequence, why the eyes are converged for the initial bouts before the prey enters the strike zone is unclear (Avitan et al, 2020). The initial swim bouts following eye convergence act to align the larva's body toward the prey.…”

Neural encoding models for multivariate optical imaging data

“…These factors were confined to spatially localised groups of neurons concentrated in the anterior, middle, and posterior areas of the tectum, respectively (Figure 4.5B). The multiplicative factors were more spatially diffuse, although some multiplicative factors were confined to the posterior end of the tectum, possibly reflecting increased multidimensional sensitivity to visual stimuli in the rear visual field [180]. The effect of the excitatory fluctuations can be seen in Figure 4.6A for training data and Figure 4.6B for test data.…”