Shin-ichi Sekizawa

Frequency response functions and information capacities of paired spider mechanoreceptor neurons

Abstract. Pseudorandom white-noise stimulation followed by direct spectral estimation was used to obtain linear frequency response and coherence functions from paired, but dynamically different, spider mechanosensory neurons. The dynamic properties of the two neuron types were similar with either mechanical or electrical stimulation, showing that action potential encoding dominates the dynamics. Phase-lag data indicated that action potential initiation occurs more rapidly during mechanical stimulation, probably in the distal sensory dendrites. Total information capacity, calculated from coherence, as well as information per action potential, were both similar in the two types of neurons, and similar to the few available estimates from other spiking neurons. However, information capacity and information per action potential both depended strongly on neuronal firing rate, which has not been reported before.

Peripheral GABAergic inhibition of spider mechanosensory afferents

Spider mechanosensory neurons receive an extensive network of efferent synapses onto their sensory dendrites, somata and distal axonal regions. The function of these synapses is unknown. Peripheral synapses are also found on crustacean stretch‐receptor neurons but not on mechanosensory afferents of other species, although inhibitory GABAergic synapses are a common feature of centrally located axon terminals. Here we investigated the effects of GABA receptor agonists and antagonists on one group of spider mechanosensory neurons, the slit sense organ VS‐3, which are accessible to current‐ and voltage‐clamp recordings. Bath application of GABA activated an inward current that depolarized the membrane and increased the membrane conductance leading to impulse inhibition. VS‐3 neuron GABA receptors were activated by muscimol and inhibited by picrotoxin but not bicuculline, and their dose–response relationship had an EC50 of 103.4 µm, features typical for insect ionotropic GABA receptors. Voltage‐ and current‐clamp analysis confirmed that, while the Na+ channel inhibition resulting from depolarization can lead to impulse inhibition, the increase in membrane conductance (i.e. ‘shunting’) completely inhibited impulse propagation. This result argues against previous findings from other preparations that GABA‐mediated inhibition is caused by a depolarization that inactivates Na+ conductance, and it supports those findings that assign this role to membrane shunting. Our results show that GABA can rapidly and selectively inhibit specific mechanoreceptors in the periphery. This type of peripheral inhibition may provide spiders with a mechanism for distinguishing between signals from potential prey, predators or mates, and responding with appropriate behaviour to each signal.

Predicting the responses of mechanoreceptor neurons to physiological inputs by nonlinear system identification.

AbstractThe nonlinear dynamic properties of action potential encoding were studied in mechanosensory neurons innervating the slits of a slit-sense organ in the tropical wandering spider, Cupiennius salei. The organ contains two types of neurons that are morphologically similar but have different dynamic properties. Type A neurons produce only one or two action potentials in response to a mechanical or electrical stimulus of any suprathreshold amplitude, while type B neurons can fire prolonged bursts of action potentials in response to similar stimuli. Neurons were stimulated with pseudorandomly modulated intracellular current while recording the resultant fluctuations in membrane potential and action potentials. A parallel cascade method was used to estimate a third-order Volterra series to describe the nonlinear dynamic relationship between membrane potential and action potentials. Kernels measured for the two types of neurons had reproducible forms that showed differences between the two neuron types. The measured kernels were able to predict the responses of the neurons to novel pseudorandomly modulated inputs with reasonable fidelity. However, the Volterra series did not adequately predict the difference in responses to step depolarizations.

A Novel Postsynaptic Group II Metabotropic Glutamate Receptor Role in Modulating Baroreceptor Signal Transmission

The nucleus tractus solitarius (NTS) is essential for orchestrating baroreflex control of blood pressure. When a change in blood pressure occurs, the information is transmitted by baroreceptor afferent fibers to the central network by glutamate binding to ionotropic glutamate receptors on second-order baroreceptor neurons. Glutamate also activates presynaptic group II and III metabotropic glutamate receptors (mGluRs), depressing both glutamate and GABA release to modulate baroreceptor signal transmission. Here we present a novel role for postsynaptic group II mGluRs to further fine-tune baroreceptor signal transmission at the first central synapses. In a brainstem slice with ionotropic glutamate and GABA receptors blocked, whole-cell patch-clamp recordings of second-order baroreceptor neurons revealed that two group II mGluR agonists evoked concentration-dependent membrane hyperpolarizations. The hyperpolarization remained when a presynaptic contribution was prevented with Cd2+, was blocked by a postsynaptic intervention of intracellular dialysis of the G-protein signaling inhibitor, was mimicked by endogenous release of glutamate by tractus solitarius stimulation, and was prevented by a group II mGluR antagonist. Postsynaptic localization of group II mGluRs was confirmed by fluorescent confocal immunohistochemistry and light microscopy. Group II mGluR induced-currents consisted of voltage-dependent outward and inward components, prevented by tetraethylammonium chloride and tetrodotoxin, respectively. In contrast to group II mGluR-induced hyperpolarization, there was no effect on intrinsic excitability as determined by action potential shape or firing in response to depolarizing current injections. The data suggest a novel mechanism for postsynaptic group II mGluRs to fine-tune baroreceptor signal transmission in the NTS.

A context-free data compression approach to measuring information transmission by action potentials

Action potentials allow nervous systems to transmit information rapidly and efficiently over considerable distances, but what is the information they carry and how much can be carried by one neuron? Often, qualitative and vague descriptions are used, such as the firing rate representing intensity. Recent attempts to quantify information transmission by action potentials have concentrated on treating neurons as communication channels, whose information capacity can be estimated from their signal-to-noise ratios. However, this only indicates how much information could theoretically be carried, not the actual amount at any given time, and the ratio itself depends on assumptions about information coding. Here we introduce a different approach based on the concept of data compression, which has become familiar with the widespread use of digital computers and networks. Compression takes advantage of redundancy in a sequence of numbers to reduce its size, but allows it to be reconstructed later without error. We show that data compression by a context-free grammar can quantitatively estimate the real information content of action potential signals without any prior assumptions about coding, or knowledge of neural inputs. Measurements of information coding by mechanosensory neurons are used as examples, but a major advantage of this approach is its generality. It can estimate information transmission by any neuron whose output can be measured, regardless of neuronal type, connectivity or function.