Insights into neural mechanisms and evolution of behaviour from electric fish

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Abstract
Behaviour and its neural control can be studied at proximate and ultimate levels. Much progress has been made in determining how neural circuits control behavior, but comparatively little is understood about why these particular solutions have arisen. This question can be addressed through comparative studies, aimed at understanding how neural circuits are modified during the evolution of new behaviours. Comparative studies in electrosensory systems provide insights into the neural mechanisms and evolution of behaviour. The jamming avoidance response (JAR) is a behaviour in which fish change their frequency of electric organ discharge (EOD) to increase the difference in frequency between their own EOD and that of a neighbour. The JAR evolved convergently in electric fishes. The algorithm for the control of jamming avoidance behavior is complex, involving concurrent analyses of signal amplitude and timing differences across the receptor array, similar to those that underlie sound localization. Interestingly, this solution seems to have been utilized in at least three independent instances of evolution of this behaviour. The hypothesis that this computation is an ancestral trait is supported by its presence in a family of fishes that have some ancestral features of South American electric fishes, but lack a JAR. These comparative data indicate that concurrent analyses of changes in signal amplitude and timing difference serve diverse functions in electrosensory species, and served as a preadaptation for the evolution of JARs. Analyses of the neural control of JARs strongly support the notion that this type of behaviour has evolved independently several times, and that subtle changes in neural circuitry were sufficient for its evolution. Across three groups of fishes that have independently evolved electrosensory systems — skates, South American and African electric fishes — adaptive cancellation of expected sensory information is mediated by a common plasticity mechanism. First-order central electrosensory neurons gradually become less responsive to electrosensory input that is repeatedly associated in time with motor commands, or reliable correlates of those commands. This cancellation process results from the integration of this afferent input with a modifiable 'negative image' of the expected input. In all three cases, generation of this negative image involves plasticity at the parallel-fibre interface between primary sensory and cerebellar structures. Cerebellar circuits are both phylogenetically very old and highly conserved. It seems that plasticity at parallel fibre synapses has had historic importance for adjusting the gain of neural responses. Because this role of cerebellar circuits predated the evolution of most electrosensory systems, it is likely that this plasticity mechanism served as a preadaptation for the convergent evolution of adaptive cancellation processes in these different electrosensory systems. Together, these comparative findings support the idea that the structural and physiological organization of the nervous system cannot be understood with respect to current function alone; historical factors and the constraints they impose on systems must also be considered. Comparative studies provide an opportunity to study the neural control of behaviour at both the proximate and ultimate levels.