Recurrent network interactions explain tectal response variability and experience-dependent behavior

Abstract

Response variability is an essential and universal feature of sensory processing and behavior. It arises from fluctuations in the internal state of the brain, which modulate how sensory information is represented and transformed to guide behavioral actions. In part, brain state is shaped by recent network activity, fed back through recurrent connections to modulate neuronal excitability. However, the degree to which these interactions influence response variability and the spatial and temporal scales across which they operate, are poorly understood. Here, we combined population recordings and modeling to gain insights into how neuronal activity modulates network state and thereby impacts visually evoked activity and behavior. First, we performed cellular-resolution calcium imaging of the optic tectum to monitor ongoing activity, the pattern of which is both a cause and consequence of changes in network state. We developed a minimal network model incorporating fast, short range, recurrent excitation and long-lasting, activity-dependent suppression that reproduced a hallmark property of tectal activity – intermittent bursting. We next used the model to estimate the excitability state of tectal neurons based on recent activity history and found that this explained a portion of the trial-to-trial variability in visually evoked responses, as well as spatially selective response adaptation. Moreover, these dynamics also predicted behavioral trends such as selective habituation of visually evoked prey-catching. Overall, we demonstrate that a simple recurrent interaction motif can be used to estimate the effect of activity upon the incidental state of a neural network and account for experience-dependent effects on sensory encoding and visually guided behavior.

Mirror-assisted light-sheet microscopy: a simple upgrade to enable bi-directional sample excitation

“…We implemented mLSM on a custom-built digitally scanned light-sheet microscope that was in routine use in the lab (Zylbertal and Bianco, 2023). The excitation path included a 488 nm laser source with an analogue input for power modulation (OBIS 488-50 LX, Coherent, Santa Clara, California), a pair of galvanometer scan mirrors (6210H, Cambridge Technology, Bedford, Massachusetts) and objective (Plan 4X, 4x/0.1 NA, Olympus, Tokyo, Japan), with its back aperture limited to 5.5 mm using an adjustable iris (for an effective NA of ∼0.06).…”

“…The addition of a second excitation path may be undesirable as it requires additional space for a second excitation objective (EO), which hinders presentation of visual stimuli in the animal’s frontal visual field. Such stimuli are commonly used, for example, in the context of virtual hunting assays (eg Bianco and Engert, 2015; Zylbertal and Bianco, 2023).…”

“…A particularly successful application of light-sheet microscopy has been in vivo cellular-resolution functional imaging in the small, transparent brains of larval zebrafish expressing fluorescent calcium indicators (Ahrens et al ., 2013), which has provided insights into the function of distributed neuronal circuits controlling vertebrate behaviour (Keller, Ahrens and Freeman, 2015; Dragomir, Štih and Portugues, 2020; Petrucco et al ., 2023; Zylbertal and Bianco, 2023). In such experiments, the brain is illuminated from the side (laterally) and a light-sheet is formed by scanning the beam in a direction (‘y’) that corresponds to the rostrocaudal anatomical axis.…”

Attractor-like circuits improve visual decoding and behavior in zebrafish

“…In the zebrafish larva, the optic tectum plays a role in detecting the physical properties of visual stimuli, it processes them and generates goal-directed motor behaviors. The tectum’s ongoing spontaneous activity is organized according to topographically compact neuronal assemblies 16–21 . These assemblies mimic visually induced responses associated with the larva’s prey, and are organized according to the tectum’s retinotopic map 16,18 .…”

“…In the zebrafish larva, the optic tectum plays a role in detecting the physical properties of visual stimuli, it processes them and generates goal-directed motor behaviors. The tectum's ongoing spontaneous activity is organized according to topographically compact neuronal assemblies [16][17][18][19][20][21] .…”