It is an important task in neuroscience to find general principles that relate neural codes to the structure of the signals they encode. The structure of sensory signals can be described in many ways, but one important categorization distinguishes continuous from transient signals. We used the communication signals of the weakly electric fish to reveal how transient signals (chirps) can be easily distinguished from the continuous signal they disrupt. These communication signals-low-frequency sinusoids interrupted by high-frequency transients-were presented to pyramidal cells of the electrosensory lateral line lobe (ELL) during in vivo recordings. We show that a specific population of electrosensory neurons encodes the occurrence of the transient signal by synchronously producing a burst of spikes, whereas bursting was neither common nor synchronous in response to the continuous signal. We also confirmed that burst can be triggered by low-frequency modulations typical of prey signals. However, these bursts are more common in a different segment of the ELL and during spatially localized stimulation. These localized stimuli will elicit synchronized bursting only in a restricted number of cells the receptive fields of which overlap the spatial extent of the stimulus. Therefore the number of cells simultaneously producing a burst and the ELL segment responding most strongly may carry the information required to disambiguate chirps from prey signals. Finally we show that the burst response to chirps is due to a biophysical mechanism previously characterized by in vitro studies of electrosensory neurons. We conclude that bursting and synchrony across cells are important mechanisms used by sensory neurons to carry the information about behaviorally relevant but transient signals.

Efficient sensory coding implies that populations of neurons should represent information-rich aspects of a signal with little redundancy. Recent studies have shown that neural heterogeneity in higher brain areas enhances the efficiency of encoding by reducing redundancy across the population. Here, we study how neural heterogeneity in the early stages of sensory processing influences the efficiency of population codes. Through the analysis of in vivo recordings, we contrast the encoding of two types of communication signals of electric fishes in the most peripheral sensory area of the CNS, the electrosensory lateral line lobe (ELL). We show that communication signals used during courtship (big chirps) and during aggressive encounters (small chirps) are encoded by different populations of ELL pyramidal cells, namely I-cells and E-cells, respectively. Most importantly, we show that the encoding strategy differs for the two signals and we argue that these differences allow these cell types to encode specifically information-rich features of the signals. Small chirps are detected, and their timing is accurately signaled through stereotyped spike bursts, whereas the shape of big chirps is accurately represented by variable increases in firing rate. Furthermore, we show that the heterogeneity across I-cells enhances the efficiency of the population code and thus permits the accurate discrimination of different quality courtship signals. Our study shows the importance of neural heterogeneity early in a sensory system and that it initiates the sparsification of sensory representation thereby contributing to the efficiency of the neural code.

For optimal sensory processing, neural circuits must extract novel, unpredictable signals from the redundant sensory input in which they are embedded, but the detailed cellular and network mechanisms that implement such selective cancellation are presently unknown. Using a combination of modeling and experiment, we characterize in detail a cerebellar circuit in weakly electric fish, showing how it can carry out this computation. We use a model incorporating the wide range of experimentally estimated parallel fiber feedback delays and a burst-induced LTD rulederivedfrominvitroexperimentstoexplaintheprecisecancellationofredundantsignalsobservedinvivo.Ourmodeldemonstrateshowthe backpropagation-dependent burst dynamics adjusts the temporal pairing width of the plasticity mechanism to precisely match the frequency of the redundant signal. The model also makes the prediction that this cerebellar feedback pathway must be composed of frequency-tuned channels; this prediction is subsequently verified in vivo, highlighting a novel and general capability of cerebellar circuitry.

Brief episodes of high-frequency firing of sensory neurons, or bursts, occur in many systems, including mammalian auditory and visual systems, and are believed to signal the occurrence of particularly important stimulus features, i.e., to function as feature detectors. However, the behavioral relevance of sensory bursts has not been established in any system. Here, we show that bursts in an identified auditory interneuron of crickets reliably signal salient stimulus features and reliably predict behavioral responses. Our results thus demonstrate the close link between sensory bursts and behavior.

The omega neuron 1 (ON1) of the cricket Teleogryllus oceanicus responds to conspecific signals (4.5 kHz) and to the ultrasonic echolocation sounds used by hunting, insectivorous bats. These signals differ in temporal structure as well as in carrier frequency. We show that ON1's temporal coding properties vary with carrier frequency, allowing it to encode both of these behaviorally important signals. Information-transfer functions show that coding of 4.5 kHz is limited to the range of amplitude-modulation components that occur in cricket songs (<32 Hz), whereas coding of 30-kHz stimuli extends to the higher pulse rates that occur in bat sounds ( approximately 100 Hz). Nonlinear coding contributes to the information content of ON1's spike train, particularly for 30-kHz stimuli with high intensities and large modulation depths. Phase locking to sinusoidal amplitude envelopes also extends to higher AM frequencies for ultrasound stimuli. ON1s frequency-specific behavior cannot be ascribed to differences in the shapes of information-transfer functions of low- and high-frequency-tuned receptor neurons, both of which are tuned more broadly to AM frequencies than ON1. Coding properties are nearly unaffected by contralateral deafferentation. ON1's role in auditory processing is to increase binaural contrast through contralateral inhibition. We hypothesize that its frequency-specific temporal coding properties optimize binaural contrast for sounds with both the spectral and temporal features of behaviorally relevant signals.