How tightly tuned are the synaptic and intrinsic properties that give rise to neuron and circuit function? Experimental work shows that these properties vary considerably across identified neurons in different animals. Given this variability in experimental data, this review describes some of the complications of building computational models to aid in understanding how system dynamics arise from the interaction of system components. We argue that instead of trying to build a single model that captures the generic behavior of a neuron or circuit, it is beneficial to construct a population of models that captures the behavior of the population that provided the experimental data. Studying a population of models with different underlying structure and similar behaviors provides opportunities to discover unsuspected compensatory mechanisms that contribute to neuron and network function.

How different are the neuronal circuits for a given behavior across individual animals? To address this question, we measured multiple cellular and synaptic parameters within individual preparations to see how they correlate with circuit function, using neurons and synapses within the pyloric circuit of the stomatogastric ganglion (STG) of the crab Cancer borealis. There was considerable preparation-to-preparation variability in the strength of two identified synapses, in the amplitude of a modulator-evoked current, and in the expression of six ion channel genes. Nonetheless, across preparations we found strong correlations among these parameters and attributes of circuit performance. These data illustrate the importance of making multidimensional measurements from single preparations to understand how variability in circuit output is related to the variability of multiple circuit parameters.

Computational modeling and experimentation in a model system for network dynamics reveal how network phase relationships are temperature-compensated in terms of their underlying synaptic and intrinsic membrane currents.

Most neurons have large numbers of voltage-and time-dependent currents that contribute to their electrical firing patterns. Because these currents are nonlinear, it can be difficult to determine the role each current plays in determining how a neuron fires. The lateral pyloric (LP) neuron of the stomatogastric ganglion of decapod crustaceans has been studied extensively biophysically. We constructed ϳ600,000 versions of a four-compartment model of the LP neuron and distributed 11 different currents into the compartments. From these, we selected ϳ1300 models that match well the electrophysiological properties of the biological neuron. Interestingly, correlations that were seen in the expression of channel mRNA in biological studies were not found across the ϳ1300 admissible LP neuron models, suggesting that the electrical phenotype does not require these correlations. We used cubic fits of the function from maximal conductances to a series of electrophysiological properties to ask which conductances predominantly influence input conductance, resting membrane potential, resting spike rate, phasing of activity in response to rhythmic inhibition, and several other properties. In all cases, multiple conductances contribute to the measured property, and the combinations of currents that strongly influence each property differ. These methods can be used to understand how multiple currents in any candidate neuron interact to determine the cell's electrophysiological behavior.

During courtship males attract females with elaborate behaviors. In mice, these displays include ultrasonic vocalizations. Ultrasonic courtship vocalizations were previously attributed to the courting male, despite evidence that both sexes produce virtually indistinguishable vocalizations. Because of this similarity, and the difficulty of assigning vocalizations to individuals, the vocal contribution of each individual during courtship is unknown. To address this question, we developed a microphone array system to localize vocalizations from socially interacting, individual adult mice. With this system, we show that female mice vocally interact with males during courtship. Males and females jointly increased their vocalization rates during chases. Furthermore, a female's participation in these vocal interactions may function as a signal that indicates a state of increased receptivity. Our results reveal a novel form of vocal communication during mouse courtship, and lay the groundwork for a mechanistic dissection of communication during social behavior.DOI: http://dx.doi.org/10.7554/eLife.06203.001