Banded knifefish, Gymnotus carapo. Photo credit: Tiago P. Carvalho.

Banded knifefish, Gymnotus carapo. Photo credit: Tiago P. Carvalho.

You may not realise it, but in the seconds before you clicked on the link to read this article (or picked the journal off a shelf), your brain was whirling away collecting information about yourself and your surroundings prior to taking action. ‘The outcome of a voluntary decision can be predicted by brain activity even before a subject's conscious awareness,’ say James Jun and Len Maler from the University of Ottawa, Canada. They add that similar brain activity has been found in other species too. However, the relationship between the timing of the sensory brain activity and the associated voluntary activity was not clear and experiments that could be used to investigate the phenomenon tend to be invasive, leading Jun and Maler to look for an animal that makes more of a display of sensory acquisition. Electric knifefish emit mild electric pulses as they sense their surroundings through distortions in the resulting weak electric field. ‘Each pulse corresponds to a discrete active sampling event,’ says Jun, and it was this remarkable ability that the duo decided to take advantage of in order to learn more about the relationship between the fish's actions and the sensory sampling that precedes them (p. 3615).

However, before the team could begin to unravel the timing relationships, they had to be sure that the fish's movements were made of their own free will. Nothing could inadvertently startle the animals, forcing Jun to become nocturnal and conduct his experiments at night with the fish in a specially constructed light- and vibration-free sensory isolation chamber. Jun then filmed the fish's undisturbed activity while recording their electric fields to understand the relationship between their electric discharge patterns and activity, so that he could later infer the fish's activity levels directly from variation in the strength (amplitude) of the electric discharge.

Next, Jun and Maler teamed up with Andre Longtin to statistically analyse the fish's electrical discharge patterns in relation to their movements and realised that the fish existed in two distinct sensory conditions: one where the fish had a high electric field discharge rate and a second with a low rate. And when the team compared the fish's physical activity levels with their electric discharge patterns, they could see that the fish only moved when the electric discharge rate was high and had been elevated for a period prior to moving. Just like humans, the fish collect sensory information about their surroundings just before making the decision to move voluntarily. Finally, the team compared the fish's electrical discharge rates when moving freely and when startled by a loud soundand found that the discharge rate was fairly constant in the startled fish, but extremely variable in the fish that moved voluntarily.

Having confirmed that weakly electric fish are capable of making voluntary movements and that their sensory activity patterns are essentially the same as the brain patterns of freely moving humans, the team come to the startling conclusion that the ability to make voluntary movements may have been a primitive function in early vertebrate brains that predates the sophisticated cognitive abilities of humans and modern primates. Jun also hopes that it may be possible to discover which part of the fish brain triggers the burst of sensory electrical activity, saying, ‘[This] may give clues to the initiation sites of human voluntary actions.’

J. J.
Enhanced sensory sampling precedes self-initiated locomotion in an electric fish
J. Exp. Biol.