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.

Keywords: decisions; locomotion; response times; sensory memory.

Figure 1.

A simple theory for cortical decision circuits and tadpole responses to a brief skin stimulus. (a) Diagram to illustrate general theory for variable delay generation (based on [3]). (b) A resting hatchling Xenopus tadpole, 5 mm long, hangs from mucus secreted by its cement gland (arrow). (c) Video frames of tadpole (dorsal view) flexing (arrowhead), then swimming following a current pulse to the right trunk (*). (d,e) RTs to the first flexion of swimming and first motor nerve activity of fictive swimming in immobilized tadpoles. (Online version in colour.)

Figure 2.

Organization of neuronal pathways from head and trunk skin stimulation to swimming in the hatchling frog tadpole. The boxes represent populations of similar excitatory neurons in the five functional levels between a skin stimulus and a motor response. Arrows show direct excitatory synaptic connections established by recording from pre- and post-synaptic neurons. Dashed boxes and arrows are populations and connections proposed to explain current evidence. For simplicity, the pathways are only shown for one side of the body and inhibitory neurons are omitted. Letters near boxes are the abbreviations of neuron names they contain. (Online version in colour.)

Figure 3.

Recordings show the activity and connections of neurons in the swimming response pathway: (a) current injection into a sensory RB neuron leads to an action potential (*) and direct excitation of a sensory pathway dlc neuron (excitatory post-synaptic potential (EPSP) starts at arrow) which then evokes an action potential in the dlc (*). (b,c) Paired recordings showing responses to a 1 ms head skin current stimulus which evoked swimming. (b) A sensory pathway tIN responds with a single spike. The excitation from this and other tIN spikes excites the hdIN on the same side which depolarizes smoothly to threshold (dashed arrow) and fires a spike. (c) A rostral dlc on the right side also fires a single spike but this cannot explain the slow, noisy build-up of excitation (arrowheads) to threshold (dashed arrow) and firing in the hdIN on the opposite side. (d–f) Trunk skin stimulation also leads to variable excitation of hdINs. (d) A stronger stimulus leads to two jumps (arrowheads) in hdIN which reach threshold (arrow) and firing is followed by rhythmic firing during swimming. (e) Two examples of responses subthreshold for swimming show noisy excitation (arrowheads) summing but not reaching firing threshold. (f) The long duration of subthreshold excitation in hdINs is revealed by averaging five recordings at a slower time-scale. (g) Two examples of responses of a possible sensory processing neuron (exN) in the hindbrain to a trunk skin stimulus (at arrow). Each record shows an early spike and variable later firing. (Online version in colour.)