The generation and subtraction of sensory expectations within cerebellum-like structures

Abstract

The generation of expectations about sensory input and the subtraction of such expectations from actual input appear to be important features of sensory processing. This paper describes the generation of sensory expectations within cerebellum-like structures of four distinct groups of fishes: Mormyridae; Rajidae; Scorpaenidae; and Apteronotidae. These structures consist of a sheet-like array of principal cells. Apical dendrites of the principal cells extend out into a molecular layer where they are contacted by parallel fibers. The basilar regions of the arrays receive primary afferent input from octavolateral endorgans, i.e., electroreceptors, mechanical lateral line neuromasts, or eighth nerve endorgans. The parallel fibers in the molecular layer convey various types of information, including corollary discharge signals associated with motor commands, sensory information from other modalities such as proprioception, and descending input from higher stages of the sensory modality that is processed by the structure. Associations between the signals conveyed by the parallel fibers and particular patterns of sensory input to the basal layers lead to the generation of a negative image of expected sensory input within the principal cell array. Addition of this negative image to actual sensory input results in the subtraction of expected from actual input, allowing the unexpected or novel input to stand out more clearly. Intracellular recording indicates that the negative image is probably generated by means of anti-Hebbian synaptic plasticity at the parallel fiber to principal cell synapse. The results are remarkably similar in the different fishes and may generalize to cerebellum-like structures in other sensory systems and taxa.