A simple decision to move in response to touch reveals basic sensory memory and mechanisms for variable response times

Abstract

Many motor responses to sensory input, like locomotion or eye movements, are much slower than reflexes. Can simpler animals provide fundamental answers about the cellular mechanisms for motor decisions? Can we observe the 'accumulation' of excitation to threshold proposed to underlie decision making elsewhere? We explore how somatosensory touch stimulation leads to the decision to swim in hatchling Xenopus tadpoles. Delays measured to swimming in behaving and immobilised tadpoles are long and variable. Activity in their extensively studied sensory and sensory pathway neurons is too short-lived to explain these response delays. Instead, whole-cell recordings from the hindbrain reticulospinal neurons that drive swimming show that these receive prolonged, variable synaptic excitation lasting for nearly a second following a brief stimulus. They fire and initiate swimming when this excitation reaches threshold. Analysis of the summation of excitation requires us to propose extended firing in currently undefined presynaptic hindbrain neurons. Simple models show that a small excitatory recurrent-network inserted in the sensory pathway can mimic this process. We suggest that such a network may generate slow, variable summation of excitation to threshold. This excitation provides a simple memory of the sensory stimulus. It allows temporal and spatial integration of sensory inputs and explains the long, variable delays to swimming. The process resembles the 'accumulation' of excitation proposed for cortical circuits in mammals. We conclude that fundamental elements of sensory memory and decision making are present in the brainstem at a surprisingly early stage in development.

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

“…We have investigated the neurons, and networks that allow hatchling Xenopus laevis tadpoles (figure 1b) to behave and survive [20][21][22]. This has led to some surprising new discoveries about the organization of sensory systems, sensory memory and the neurons where the decisions to move are made [23][24][25].…”

The early development and physiology ofXenopus laevistadpole lateral line system

“…Other senses including ocular vision, hearing, taste and pain are not developed. The simplicity of tadpole sensory and motor systems presents the animal as an excellent model for studying sensory information integration and motor decision-making (Koutsikou S et al, 2018; Roberts A et al, 2019). In this study, we investigated the neurophysiology of the tadpole LL system.…”

Flowing from sense to action. Are neural integrators necessary?

“…A study by Koutsikou et al . () in this issue of The Journal of Physiology elegantly exposes the minimal circuitry necessary for generating such sensory memory while exploring a simple ‘touch‐and‐go’ paradigm in the tadpole. Immediately prior to swimming, a population of cells in the hindbrain called reticulospinal (RS) neurons provide the descending motor commands to drive rhythmogenesis in spinal networks necessary for swimming initiation (see Grillner () for review).…”

“…Neural circuits specialised in integrating information in time-varying signals are of critical importance -not only for memory formation -but for a variety of brain functions, in particular for motor control, navigation and decision making. A study by Koutsikou et al (2018) in this issue of The Journal of Physiology elegantly exposes the minimal circuitry necessary for generating such sensory memory while exploring a simple 'touch-and-go' paradigm in the tadpole. Immediately prior to swimming, a population of cells in the hindbrain called reticulospinal (RS) neurons provide the descending motor commands to drive rhythmogenesis in spinal networks necessary for swimming initiation (see Grillner (2003) for review).…”

“…Yet, too often too little is gained by this approach, particularly when detailed knowledge of neurons is lacking. However, the experimental settings and preparation described in Koutsikou et al (2018) grants them the necessary accessibility to perform intracellular recordings and to monitor the subthreshold processes that lead up to state transition at the level of the individual neuron. This approach enabled them to overcome the limitations associated with extracellular recordings that detect all-or-nothing states, thereby unmasking the presence of accumulating synaptic inputs that promote and prolong the excitability of 'decision-making' RS neurons.…”