Static frequency tuning accounts for changes in neural synchrony evoked by transient communication signals.

Although communication signals often vary continuously on the underlying signal parameter, they are perceived as distinct categories. We here report the opposite case where an electrocommunication signal is encoded in four distinct regimes, although the behavior described to date does not show distinct categories. In particular, we studied the encoding of chirps by P-unit afferents in the weakly electric fish Apteronotus leptorhynchus. These fish generate an electric organ discharge that oscillates at a certain individual-specific frequency. The interaction of two fish in communication contexts leads to the emergence of a beating amplitude modulation (AM) at the frequency difference between the two individual signals. This frequency difference represents the social context of the encounter. Chirps are transient increases of the fish's frequency leading to transient changes in the frequency of the AM. We stimulated the cells with the same chirp on different, naturally occurring backgrounds beats. The P-units responded either by synchronization or desynchronization depending on the background. Although the duration of a chirp is often shorter than a full cycle of the AM it elicits, the distinct responses of the P-units to the chirp can be predicted solely from the frequency of the AM based on the static frequency tuning of the cells.

The neuroethology of electrocommunication: how signal background influences sensory encoding and behaviour in Apteronotus leptorhynchus.

Weakly-electric fish are a well-established model system for neuroethological studies on communication and aggression. Sensory encoding of their electric communication signals, as well as behavioural responses to these signals, have been investigated in great detail under laboratory conditions. In the wave-type brown ghost knifefish, Apteronotus leptorhynchus, transient increases in the frequency of the generated electric field, called chirps, are particularly well-studied, since they can be readily evoked by stimulating a fish with artificial signals mimicking conspecifics. When two fish interact, both their quasi-sinusoidal electric fields (called electric organ discharge, EOD) superimpose, resulting in a beat, an amplitude modulation at the frequency difference between the two EODs. Although chirps themselves are highly stereotyped signals, the shape of the amplitude modulation resulting from a chirp superimposed on a beat background depends on a number of parameters, such as the beat frequency, modulation depth, and beat phase at which the chirp is emitted. Here we review the influence of these beat parameters on chirp encoding in the three primary stages of the electrosensory pathway: electroreceptor afferents, the hindbrain electrosensory lateral line lobe, and midbrain torus semicircularis. We then examine the role of these parameters, which represent specific features of various social contexts, on the behavioural responses of A. leptorhynchus. Some aspects of the behaviour may be explained by the coding properties of early sensory neurons to chirp stimuli. However, the complexity and diversity of behavioural responses to chirps in the context of different background parameters cannot be explained solely on the basis of the sensory responses and thus suggest that critical roles are played by higher processing stages.