Barayeu, A. | bioRxiv Science

bioRxiv2024

Weakly nonlinear responses at low intrinsic noise levels in two types of electrosensory primary afferents

Spiking thresholds in neurons or rectification at synapses are essential for neuronal computations rendering neuronal processing inherently nonlinear. Nevertheless, linear response theory has been instrumental for understanding, for example, the impact of noise or neuronal synchrony on signal transmission, or the emergence of oscillatory activity, but is valid only at low stimulus amplitudes or large levels of intrinsic noise. At higher signal-to-noise ratios, however, nonlinear response components become relevant. Theoretical results for leaky integrate-and-fire neurons in the weakly nonlinear regime suggest strong responses at the sum of two input frequencies if one of these frequencies or their sum match the neurons baseline firing rate. We here analyze nonlinear responses in two types of primary electroreceptor afferents, the P-units of the active and the ampullary cells of the passive electrosensory system of the wave-type electric fish Apteronotus leptorhynchus of either sex. In our combined experimental and modeling approach we identify these predicted nonlinear responses in those 31 out of 172 P-units that are characterized by low intrinsic noise. In contrast, the majority (22 out of 30) ampullary cells show nonlinear responses. Our results provide experimental evidence for nonlinear responses of spike generators in the weakly nonlinear regime. We conclude that such nonlinear responses occur in any sensory neuron that operates in similar regimes particularly at near-threshold stimulus conditions. Significance statementThe generation of action potentials involves a strong threshold nonlinearity. Nevertheless, the encoding of stimuli with small amplitudes by neurons with sufficient intrinsic noise can be well described as a linear system. As the stimulus amplitude is increased, new spectral components start to appear in the so called weakly nonlinear regime. Theory predicts nonlinear interactions whenever one or the sum of two stimulus frequencies matches the neurons baseline firing rate. Indeed, we find these interactions in a large set of electrophysiological recordings from primary electroreceptive afferents of a weakly electric fish. The non-linear response components could boost sensory responses to weak signals emitted, for example, by distant conspecifics.

neuroscience↗

bioRxiv2024

Bursts boost nonlinear encoding in electroreceptor afferents

Nonlinear mechanisms are at the heart of neuronal information processing, for example to fire an action potential, the membrane voltage must exceed a threshold nonlinearity. Even though, linear encoding schemes are commonly used and often successfully describe large parts of sensory encoding nonlinear mechanisms such as thresholds and saturations are well known to be crucial to encode behaviorally relevant features in the stimulus space not captured by linear methods. Here we analyze the role of bursts in p-type electroreceptor afferents (P-units) in the weakly electric fish Apteronotus leptorhynchus. It is long known that subpopulations of these cells fire bursts of action potentials while others do not. Previous research suggests, that the non-bursting cells are better at encoding the stimulus time-course while bursting neurons are better suited to encode special features in the stimulus. We here show, based on the analysis of experimental data and modeling, that bursts affect the linear as well as the nonlinear encoding. Theoretical work predicts that in simple leaky-integrate-and-fire model neurons, two periodic stimuli interact nonlinearly when the sum of the two frequencies matches the neurons baseline firing rate as quantified by the second-order susceptibility. Indeed, such nonlinear responses have been found in non-bursting P-units when stimulated by two beats simultaneously but only in those cells, that exhibit very low levels of intrinsic noise. In this study, we found that bursts strongly enhance these nonlinear responses which may play a critical role in the detection of weak intruder signals in the presence of a strong female signal, i.e. an electrosensory cocktail party.

neuroscience↗