Visual Threat Assessment and Reticulospinal Encoding of Calibrated Responses in Larval Zebrafish

Abstract

Summary All visual animals must decide whether approaching objects are a threat. Our current understanding of this process has identified a proximity-based mechanism where an evasive maneuver is triggered when a looming stimulus passes a subtended visual angle threshold. However, some escape strategies are more costly than others and so it would be beneficial to additionally encode the level of threat conveyed by the predator's approach rate to select the most appropriate response. Here, using naturalistic rates of looming visual stimuli while simultaneously monitoring escape behavior and the recruitment of multiple reticulospinal neurons, we find that larval zebrafish do indeed perform a calibrated assessment of threat. While all fish generate evasive maneuvers at the same subtended visual angle, lower approach rates evoke slower, more kinematically variable escape responses with relatively long latencies as well as the unilateral recruitment of ventral spinal projecting nuclei (vSPNs) implicated in turning. In contrast, higher approach rates evoke faster, more kinematically stereotyped responses with relatively short latencies, as well as bilateral recruitment of vSPNs and unilateral recruitment of giant fiber neurons in fish and amphibians called Mauthner cells. In addition to the higher proportion of more costly, shorter latency Mauthner-active responses to greater perceived threats, we observe a higher incidence of freezing behavior at higher approach rates. Our results provide a new framework to understand how behavioral flexibility is grounded in the appropriate balancing of trade-offs between fast and slow movements when deciding to respond to a visually perceived threat.

The shift from life in water to life on land advantaged planning in visually-guided behavior

“…These findings suggest that with terrestrialization, there would be reduced need for specialized circuits in the vertebrate brain to generate habitual predator-avoidance maneuvers. The Mauthner system, which reduces the delay time between detection of a predator and the generation of an escape, is perhaps the best characterized of such circuits 65 , and is only known to be present in vertebrates up through amphibians 66…”

Neural circuits mediating visual stabilization during active motion in zebrafish

“…The advantage of zebrafish is the translucent brain that enables optical imaging (Ahrens et al, 2012) and optogenetic manipulations (Arrenberg et al, 2009;Goncalves et al, 2014) with the help of genetic tools (Neuhauss, 2003;Renninger et al, 2011). Several neural circuits related with internal model have been explored, e.g., motor adaptation (Ahrens et al, 2012), threat assessment and prey detection (Barker and Baier, 2015;Bhattacharyya et al, 2017;Del Bene et al, 2010;Dunn et al, 2016;Semmelhack et al, 2014;Temizer et al, 2015), behavioral context of short-term memory (Daie et al, 2015), sensory motor integration (Knogler et al, 2017;Koyama et al, 2011;Mu et al, 2012;Schoonheim et al, 2010;Wolf et al, 2017;Yao et al, 2016), OKR (Kubo et al, 2014;Portugues et al, 2014), VPNI (Goncalves et al, 2014;Miri et al, 2011), motion after effect (Perez-Schuster et al, 2016), and internal rhythm (Kaneko et al, 2006;Romano et al, 2015;Sumbre et al, 2008;Warp et al, 2012;Wyart et al, 2009). With the advancement of optical imaging methods, the current study contributes a small yet important piece of the neural representation of the internal model: the role of efference copy on the tail-OKR interaction and a push-pull mechanisms in hindbrain to support it.…”

Concepts, goals and the control of survival-related behaviors

“…These creatures are approximately 5mm long, virtually experience-free, and are heavily preyed upon. When faced with a predator, a freely-swimming larval zebrafish is capable of producing a suite of overlaid escape behaviors, modulating its response according to predator nearness inferred from several sensory sources with different temporal dynamics, the quickest being changes in the electrosensory environment and longer processing times for the amount and rate of visual field occlusion [23, 24]. Zebrafish, like most fish, have “Mauthner neurons” in a premotor system within their brainstem, which integrates multiple sources of sensory information to produce an extremely rapid escape flip opposite the direction of occlusion (called a C-bend escape maneuver); in response to looming stimuli, zebrafish execute a C-bend flip in under 25msec.…”