Electrosensory maps form a substrate for the distributed and parallel control of behavioral responses in weakly electric fish

Abstract

Electroreceptors, distributed over the body surface of weakly electric fish, code the local amplitude and phase, or timing of zerocrossing, of the animal's electric signals. These signals are generated by rhythmic discharges of the electric organ and form a dipole-like field around the animal. This field is perturbed by interference with electric fields of other fish as well as by the appearance of objects electrically different from water. The spatial and temporal structure of such perturbations can be interpreted as the electric image of interfering fields and moving objects. This strategy of assessing the environment is called 'electrolocation', a form of 'seeing' with the body surface. Electric images are analyzed in somatotopically ordered strata of neurons within the central nervous system. Primary electrosensory afferents project to somatotopically ordered layers of higher-order neurons in the electrosensory lateral line lobe (ELL) of the hindbrain. Phase and amplitude information are processed in separate layers of the ELL. The phase of the signal in a given region of the body surface is coded by the timing of spikes of spherical cells marking the zerocrossings of the electric signal. This phase information is relayed to lamina 6 of the torus semicircularis of the midbrain. Rises and falls in local amplitude are coded by the activity of different pyramidal cell types, E- and I-units, which project to various laminae of the torus above and below lamina 6. The somatotopic organization of the torus allows for computations of spatial patterns in electrosensory information. Within lamina 6, differences in the phase of signals from different parts of the body surface are computed. Differential-phase information is then relayed to deeper laminae of the torus and remains in topographic register with amplitude information. This organization allows for joint evaluation of spatially related patterns of amplitude and phase modulations on the animal's body surface within local neuronal circuits of the torus. A topographic projection of the torus relays amplitude and differential-phase information to the optic tectum where a further joint evaluation of amplitude and phase serves to control behavioral responses. The control of a particular behavioral performance, the 'jamming avoidance response', is of a distributed nature in that the representations of individual sites on the body surface contribute cumulatively to shift the electric organ pacemaker frequency.(ABSTRACT TRUNCATED AT 400 WORDS)