Contributions of electric fish to the understanding sensory processing by reafferent systems

Abstract

Sensory systems must solve the inverse problem of determining environmental events based on patterns of neural activity in the central nervous system that are affected by those environmental events. Different environmental events can give rise to indistinguishable patterns of neural activity, so that there will often, perhaps even always, be multiple solutions to a sensory inverse problem. Imaging strategies and brain organization confine these multiple solutions within a bounded set. Three different active strategies may be employed by animals to constrain the number of solutions to the sensory inverse problem: active generation of the energy (carrier) that stimulates receptors; reorientation of the point of view; and control of signal conditioning before transduction (pre-receptor mechanisms). This paper describes how these strategies are used in sensory-motor systems, using electric fish as a paradigmatic example. Carrier generation and receptor tuning to the carrier improve signal to noise ratio. Receptor tuning to different frequency bands of the carrier spectrum allows a sensory system to evaluate different kinds of carrier modulations and to extract the different features of objects in the environment. Pre-receptor mechanisms condition the signals, optimizing their detection at a foveal region where the sensory resolution is maximum. Active orientation of the sensory surface redirects the fovea to explore in detail the source of interesting signals. Sensory input generated by these active exploration mechanisms (`reafference') has two components: one, necessary, derived from the self-generated actions and another, contingent, consisting of the information obtained from the external world. Extracting environmental information (`exafference') requires that the self generated afference be subtracted from the sensory inflow. Such subtraction is often associated with the generation and storage of expectations about sensory inputs. It can be concluded that an animal's perceptual world and its ability to transform the world are inextricably linked. Understanding sensory systems must, therefore, always require understanding the organization of motor behavior.