Descending Inputs and the Decoding of Temporally Encoded Sensory Information

Sensory information is often acquired through active exploration. Knowledge of the world is gained by exploring a complex surface with hands or a visual scene with eyes. Yet relatively little is known about how neurons encode sensory stimuli in the context of natural patterns of sensing behavior, or about how sensory processing regions in the brain distinguish properties of the external world from the sensory consequences of the animal's own behavior.

A particularly clear example of active sensing is found in mormyrid electric fish. Electric fish use an electrical sense to navigate and find prey in the dark by probing the environment by emitting brief electric organ discharge (EOD) pulses. Nearby objects perturb the electric field around the fish, and these perturbations are detected by electroreceptors in the fish's skin. Each receptor encodes changes in local field strength as small shifts in the precise timing of individual action potentials following the EOD. The fish thus obtains a sequence of 'snapshots' of the world, in which information about surrounding objects is encoded in the timing of action potentials.

In nature, the frequency and regularity of this sequence of snapshots varies depending on the behavioral context, whether the fish is probing objects, foraging, or quietly resting. Interestingly, the frequency chosen by the fish has a clear effect on the timing of electroreceptor action potentials within each snapshot: higher rates shift spikes later, and lower rates shift spikes earlier. The size of these effects is comparable to the effects of small invertebrate prey on which these fish feed. How does the fish detect and capture prey when its own sensing behavior has such a strong effect on the sensory input?

This study provides opportunity to explore how sensory processing regions of the fish's brain resolves the ambiguity, and whether a change in the input from electroreceptors is due to an external stimulus or to the animal's own sensing behavior. Neurons at the first stage of electrosensory processing integrate input from electroreceptors with signals from other areas of the fish's brain linked to the motor command that evokes the EOD. Such motor command signals could, in principal, 'undo' the effects of EOD rate on electroreceptor input.

The research is expected to lead to a better understanding of how animals use internal knowledge of their actions to distinguish properties of the external world from the sensory consequences of their own behavior. At a more cellular level, the experiements are also expected to lead to a better understanding of how information contained in the precise timing of action potentials is decoded or interpreted by neural circuits.