The decision to move: response times, neuronal circuits and sensory memory in a simple vertebrate

Abstract

All animals use sensory systems to monitor external events and have to decide whether to move. Response times are long and variable compared to reflexes, and fast escape movements. The complexity of adult vertebrate brains makes it difficult to trace the neuronal circuits underlying basic decisions to move. To simplify the problem, we investigate the nervous system and responses of hatchling frog tadpoles which swim when their skin is stimulated. Studying the neuron-by-neuron pathway from sensory to hindbrain neurons, where the decision to swim is made, has revealed two simple pathways generating excitation which sums to threshold in these neurons to initiate swimming. The direct pathway leads to short, and reliable delays like an escape response. The other includes a population of sensory processing neurons which extend firing to introduce noise and delay into responses. These neurons provide a brief, sensory memory of the stimulus, that allows tadpoles to integrate stimuli occurring within a second or so of each other. We relate these findings to other studies and conclude that sensory memory makes a fundamental contribution to simple decisions and is present in the brainstem of a basic vertebrate at a surprisingly early stage in development.

In vivo photocontrol of microtubule dynamics and integrity, migration and mitosis, by the potent GFP-imaging-compatible photoswitchable reagents SBTubA4P and SBTub2M

“…We also tested interfering with development at the later blastula stage (>64 cells) by a similar protocol. While subsequent morphological development was normal under lit and dark conditions (Fig S9b-c), sensorimotor responses to mechanical stimulation 48 were suppressed by lit SBTubA4P only (Fig S9e, Movie S12). Interestingly, the tubulin-inhibiting azobenzene photoswitch PST-1P (Fig S9e ) light-independently suppresses sensorimotor responses.…”

Novel and highly distributed classes of hindbrain neuronal activity contribute to sensory processing and motor control in the Xenopus laevis tadpole

“…It has been shown that the hatchling Xenopus laevis tadpole responds to trunk skin stimuli by initiating swimming with a delay of 50-150ms (26)(27)(28). We demonstrated that this long and variable delay resembles the accumulation of excitation proposed for complex brain circuits active during motor decision-making (29,30), in contrast to quick reflexes (e.g the quick C-start response; (31)), thus concluding that sensory processing and motor decision mechanisms are present even at this early developmental stage.…”

“…The sensory (Rohon-Beard cells, RB) and sensory pathway neurons (dorsolateral ascending and dorsolateral commissural neurons, dla and dlc, respectively), which transmit the sensory information from the periphery to the tadpole's brain, are very well-known (19,20). Their firing, early in response to stimulation, cannot explain neither the variability, nor the delay detected in dINs' firing latencies and swim initiation (27). Indeed, the variable and long process of accumulation of excitation recorded in dINs could be mimicked through modelling only by inserting an excitatory recurrent network within the brainstem sensory pathway (26).…”

Whole animal modelling reveals neuronal mechanisms of decision-making and reproduces unpredictable swimming in frog tadpoles

“…Frog tadpoles, one of the most numerous vertebrate animals on earth, are simple, vulnerable animals that rely on swimming to escape from predators. The simplicity of the hatchling Xenopus tadpole and its nervous system presents a rare opportunity for experimental and computational studies (Roberts et al, 2014; Roberts et al, 2010b) where detailed information is available on behaviour, sensory systems, the central nervous system ( CNS ) (Roberts et al, 2019), body components and their properties as well as body-water interaction (Hoff and Wassersug, 2000).…”