Responses of the antennal bimodal hygroreceptor neurons to innocuous and noxious high temperatures in the carabid beetle,Pterostichus oblongopunctatus

Electrophysiological responses of thermo- and hygroreceptor neurons from antennal dome-shaped sensilla of the carabid beetle Pterostichus oblongopunctatus to different levels of steady temperature ranging from 20 to 35 °C and rapid step-changes in it were measured and analysed at both constant relative and absolute ambient air humidity conditions. It appeared that both hygroreceptor neurons respond to temperature which means that they are bimodal. For the first time in arthropods, the ability of antennal dry and moist neurons to produce high temperature induced spike bursts is documented. Burstiness of the spike trains is temperature dependent and increases with temperature increase. Threshold temperatures at which the two neurons switch from regular spiking to spike bursting are lower compared to that of the cold neuron, differ and approximately coincide with the upper limit of preferred temperatures of the species. We emphasise that, in contrast to various sensory systems studied, the hygroreceptor neurons of P. oblongopunctatus have stable and continuous burst trains, no temporal information is encoded in the timing of the bursts. We hypothesise that temperature dependent spike bursts produced by the antennal thermo- and hygroreceptor neurons may be responsible for detection of noxious high temperatures important in behavioural thermoregulation of carabid beetles.     

Coherence resonance for neuronal bursting with spike undershoot

Although the bursting patterns with spike undershoot are involved with the achievement of physiological or cognitive functions of brain with synaptic noise, noise induced-coherence resonance (CR) from resting state or subthreshold oscillations instead of bursting has been widely identified to play positive roles in information process. Instead, in the present paper, CR characterized by the increase firstly and then decease of peak value of power spectrum of spike trains is evoked from a bursting pattern with spike undershoot, which means that the minimal membrane potential within burst is lower than that of the subthreshold oscillations between bursts, while CR cannot be evoked from the bursting pattern without spike undershoot. With bifurcations and fast-slow variable dissection method, the bursting patterns with and without spike undershoot are classified into “Sub-Hopf/Fold” bursting and “Fold/Homoclinic” bursting, respectively. For the bursting with spike undershoot, the trajectory of the subthreshold oscillations is very close to that of the spikes within burst. Therefore, noise can induce more spikes from the subthreshold oscillations and modulate the bursting regularity, which leads to the appearance of CR. For the bursting pattern without spike undershoot, the trajectory of the quiescent state is not close to that of the spikes within burst, and noise cannot induce spikes from the quiescent state between bursts, which is cause for non-CR. The result provides a novel case of CR phenomenon and extends the scopes of CR concept, presents that noise can enhance rather than suppress information of the bursting patterns with spike undershoot, which are helpful for understanding the dynamics and the potential physiological or cognitive functions of the nerve fiber or brain neurons with such bursting patterns.     

The structure and size of sensory bursts encode stimulus information but only size affects behavior

Cricket ultrasound avoidance is a classic model system for neuroethology. Avoidance steering is triggered by high-firing-rate bursts of spikes in the auditory command neuron AN2. Although bursting is common among sensory neurons, and although the detailed structure of bursts may encode information about the stimulus, it is as yet unclear whether this information is decoded. We address this question in two ways: from an information coding point of view, by showing the relationship between stimulus and burst structure; and also from a functional point of view by showing the relationship between burst structure and behavior. We conclude that the burst structure carries detailed temporal information about the stimulus but that this has little impact on the behavioral response, which is affected mainly by burst size.     

Effects of temperan a central synapse between identified motor neurons in the locust

Summary Changing the temperature from 10–40 °C modifies the transmission at an established monosynaptic connection between the fast extensor tibiae (FETi) and flexor tibiae motor neurons in the metathoracic ganglion of the locustSchistocerca gregaria (Forskål). Striking changes occur to the shape of the spikes, to membrane resistance, to the synaptic delay, and to the evoked synaptic potentials.In the presynaptic FETi motor neuron, raising the temperature reduces the amplitude of an antidromic spike recorded in the soma by a factor of 10 (40 mV to 4 mV), reduces the time taken to reach peak amplitude by 5 (3.5 to 0.7 ms) and decreases the duration at half maximum amplitude by 0.5. The conduction velocity of the spike in the axon is increased by 50% from 10 °C to 40 °C. Orthodromic spikes are affected by temperature in a similar way to the antidromic spikes.The membrane resistance of both pre- and postsynaptic motor neurons falls as the temperature is raised. The membrane resistance of FETi falls by a factor of 4 (about 4 M at 10 °C to 1 M at 40 °C). A contributory component to this fall could be the increase in the frequency of synaptic potentials generated as a result of inputs from other neurons. No temperature dependence could be demonstrated on the voltage threshold relative to resting potential for evoking orthodromic spikes, but because the resistance changes, the current needed to achieve this voltage must be increased at higher temperatures.The latency measured from the peak of the spike in the soma of FETi to the start of the EPSP in the soma of a flexor motor neuron decreases by a factor of 20 (10 ms at 10 °C to 0.5 ms at 40 °C).In a postsynaptic flexor tibiae motor neuron, the amplitude of the evoked synaptic potential increases by a factor of 3.4 (5 mV to 17 mV), its duration at half maximum amplitude decreases by 3 (7 ms at 12 °C to 2.3 ms at 32 °C) and its rate of rise increases by 3. An increased likelihood that spikes will occur in the flexor contributes to the enhanced amplitude of the compound EPSP at temperatures above 20 °C.Abbreviation FETi fast extensor tibiae motor neuron     

Complex evolution of spike patterns during burst propagation through feed-forward networks

Stable signal transmission is crucial for information processing by the brain. Synfire-chains, defined as feed-forward networks of spiking neurons, are a well-studied class of circuit structure that can propagate a packet of single spikes while maintaining a fixed packet profile. Here, we studied the stable propagation of spike bursts, rather than single spike activities, in a feed-forward network of a general class of excitable bursting neurons. In contrast to single spikes, bursts can propagate stably without converging to any fixed profiles. Spike timings of bursts continue to change cyclically or irregularly during propagation depending on intrinsic properties of the neurons and the coupling strength of the network. To find the conditions under which bursts lose fixed profiles, we propose an analysis based on timing shifts of burst spikes similar to the phase response analysis of limit-cycle oscillators.     

Intrinsic bursting enhances the robustness of a neural network model of sequence generation by avian brain area HVC

Avian brain area HVC is known to be important for the production of birdsong. In zebra finches, each RA-projecting neuron in HVC emits a single burst of spikes during a song motif. The population of neurons is activated in a precisely timed, stereotyped sequence. We propose a model of these burst sequences that relies on two hypotheses. First, we hypothesize that the sequential order of bursting is reflected in the excitatory synaptic connections between neurons. Second, we propose that the neurons are intrinsically bursting, so that burst duration is set by cellular properties. Our model generates burst sequences similar to those observed in HVC. If intrinsic bursting is removed from the model, burst sequences can also be produced. However, they require more fine-tuning of synaptic strengths, and are therefore less robust. In our model, intrinsic bursting is caused by dendritic calcium spikes, and strong spike frequency adaptation in the soma contributes to burst termination.     

On the dynamics of the spontaneous activity in neuronal networks

Most neuronal networks, even in the absence of external stimuli, produce spontaneous bursts of spikes separated by periods of reduced activity. The origin and functional role of these neuronal events are still unclear. The present work shows that the spontaneous activity of two very different networks, intact leech ganglia and dissociated cultures of rat hippocampal neurons, share several features. Indeed, in both networks: i) the inter-spike intervals distribution of the spontaneous firing of single neurons is either regular or periodic or bursting, with the fraction of bursting neurons depending on the network activity; ii) bursts of spontaneous spikes have the same broad distributions of size and duration; iii) the degree of correlated activity increases with the bin width, and the power spectrum of the network firing rate has a 1/f behavior at low frequencies, indicating the existence of long-range temporal correlations; iv) the activity of excitatory synaptic pathways mediated by NMDA receptors is necessary for the onset of the long-range correlations and for the presence of large bursts; v) blockage of inhibitory synaptic pathways mediated by GABA(A) receptors causes instead an increase in the correlation among neurons and leads to a burst distribution composed only of very small and very large bursts. These results suggest that the spontaneous electrical activity in neuronal networks with different architectures and functions can have very similar properties and common dynamics.     

Bursts and isolated spikes code for opposite movement directions in midbrain electrosensory neurons

Directional selectivity, in which neurons respond strongly to an object moving in a given direction but weakly or not at all to the same object moving in the opposite direction, is a crucial computation that is thought to provide a neural correlate of motion perception. However, directional selectivity has been traditionally quantified by using the full spike train, which does not take into account particular action potential patterns. We investigated how different action potential patterns, namely bursts (i.e. packets of action potentials followed by quiescence) and isolated spikes, contribute to movement direction coding in a mathematical model of midbrain electrosensory neurons. We found that bursts and isolated spikes could be selectively elicited when the same object moved in opposite directions. In particular, it was possible to find parameter values for which our model neuron did not display directional selectivity when the full spike train was considered but displayed strong directional selectivity when bursts or isolated spikes were instead considered. Further analysis of our model revealed that an intrinsic burst mechanism based on subthreshold T-type calcium channels was not required to observe parameter regimes for which bursts and isolated spikes code for opposite movement directions. However, this burst mechanism enhanced the range of parameter values for which such regimes were observed. Experimental recordings from midbrain neurons confirmed our modeling prediction that bursts and isolated spikes can indeed code for opposite movement directions. Finally, we quantified the performance of a plausible neural circuit and found that it could respond more or less selectively to isolated spikes for a wide range of parameter values when compared with an interspike interval threshold. Our results thus show for the first time that different action potential patterns can differentially encode movement and that traditional measures of directional selectivity need to be revised in such cases.     

Conversion of Phase Information into a Spike-Count Code by Bursting Neurons

Single neurons in the cerebral cortex are immersed in a fluctuating electric field, the local field potential (LFP), which mainly originates from synchronous synaptic input into the local neural neighborhood. As shown by recent studies in visual and auditory cortices, the angular phase of the LFP at the time of spike generation adds significant extra information about the external world, beyond the one contained in the firing rate alone. However, no biologically plausible mechanism has yet been suggested that allows downstream neurons to infer the phase of the LFP at the soma of their pre-synaptic afferents. Therefore, so far there is no evidence that the nervous system can process phase information. Here we study a model of a bursting pyramidal neuron, driven by a time-dependent stimulus. We show that the number of spikes per burst varies systematically with the phase of the fluctuating input at the time of burst onset. The mapping between input phase and number of spikes per burst is a robust response feature for a broad range of stimulus statistics. Our results suggest that cortical bursting neurons could play a crucial role in translating LFP phase information into an easily decodable spike count code.     

Noise-induced burst and spike synchronizations in an inhibitory small-world network of subthreshold bursting neurons

We are interested in noise-induced firings of subthreshold neurons which may be used for encoding environmental stimuli. Noise-induced population synchronization was previously studied only for the case of global coupling, unlike the case of subthreshold spiking neurons. Hence, we investigate the effect of complex network architecture on noise-induced synchronization in an inhibitory population of subthreshold bursting Hindmarsh–Rose neurons. For modeling complex synaptic connectivity, we consider the Watts–Strogatz small-world network which interpolates between regular lattice and random network via rewiring, and investigate the effect of small-world connectivity on emergence of noise-induced population synchronization. Thus, noise-induced burst synchronization (synchrony on the slow bursting time scale) and spike synchronization (synchrony on the fast spike time scale) are found to appear in a synchronized region of the J–D plane (J: synaptic inhibition strength and D: noise intensity). As the rewiring probability p is decreased from 1 (random network) to 0 (regular lattice), the region of spike synchronization shrinks rapidly in the J–D plane, while the region of the burst synchronization decreases slowly. We separate the slow bursting and the fast spiking time scales via frequency filtering, and characterize the noise-induced burst and spike synchronizations by employing realistic order parameters and statistical-mechanical measures introduced in our recent work. Thus, the bursting and spiking thresholds for the burst and spike synchronization transitions are determined in terms of the bursting and spiking order parameters, respectively. Furthermore, we also measure the degrees of burst and spike synchronizations in terms of the statistical-mechanical bursting and spiking measures, respectively.     

Vibration receptive sensilla on the wing margins of the silkworm moth Bombyx mori

Bristles along the wing margins (wm-bristles) of the silkworm moth, Bombyx mori, were studied morphologically and electrophysiologically. The male moth has ca. 50 wm-bristles on each forewing and hindwing. Scanning electron microscopy revealed that these wm-bristles are typical mechanosensilla. Leuco-methylene blue staining demonstrated that each wm-bristle has a single receptor neuron, which is also characteristic of the mechanosensillum. The receptor neuron responded to vibrating air currents but did not respond to a constant air current. The wm-bristles showed clear directional sensitivity to vibrating air currents. The wm-bristles were classified into two types, type I and type II, by their response patterns to sinusoidal movements of the bristle. The neuron in type I discharged bursting spikes immediately following stimulation onset and also discharged a single spike for each sinusoidal cycle for frequencies less than ca. 60 Hz. The neuron in type II only responded to vibrations over 40 Hz and, specifically at 75 Hz, discharged a single spike for each sinusoidal cycle throughout the stimulation period. These results suggest that the two types of wm-bristles are highly tuned in different ways to detect vibrations due to the wing beat. The roles of the wm-bristles in the wing beat are discussed.     

Thermal response and reversibility of prolonged larval diapause in the chestnut weevil, Curculio sikkimensis

Curculio sikkimensis undergoes prolonged larval diapause that is terminated by chilling and warming cycles. To examine the effects of warming temperatures and their duration on diapause termination, we exposed diapause larvae that had not been reactivated after chilling at 5 °C to 20 or 25 °C and chilled them again before incubation at 20 °C. With increasing warming duration at 20 °C, diapause termination after chilling increased and shorter chilling durations became effective. In contrast, few or no larvae warmed at 25 °C terminated diapause after chilling, irrespective of the warming duration. To investigate the effect of warming temperature on diapause intensity, larvae with diapause weakened by initial incubation at 20 °C after the first chilling were subsequently incubated at 15, 20, or 25 °C, then chilled at 5 °C before incubation at 20 °C. Diapause termination increased significantly after the larvae were treated at 15 or 20 °C but decreased significantly after they were treated at 25 °C. The intensification of prolonged diapause at 25 °C was reversed when the larvae were transferred to 20 °C. Diapause intensity in C. sikkimensis therefore decreases at 20 °C, increases at 25 °C, and can be reversed by alternately exposing diapause larvae to 20 and 25 °C. In C. sikkimensis, prolonged diapause does not always proceed in one direction, and its intensity fluctuates in response to ambient temperature conditions.     

Bursting as an Effective Relay Mode in a Minimal Thalamic Model

In recent years, accumulating evidence indicates that thalamic bursts are present during wakefulness and participate in information transmission as an effective relay mode with distinctive properties from the tonic activity. Thalamic bursts originate from activation of the low threshold calcium cannels via a local feedback inhibition, exerted by the thalamic reticular neurons upon the relay neurons. This article, examines if this simple mechanism is sufficient to explain the distinctive properties of thalamic bursting as an effective relay mode. A minimal model of thalamic circuit composed of a retinal spike train, a relay neuron and a reticular neuron is simulated to generate the tonic and burst firing modes. The integrate-and-fire-or-burst model is used to simulate the neurons. After discriminating the burst events with criteria based on inter-spike-intervals, statistical indices show that the bursts of the minimal model are stereotypic events. The relation between the rate of bursts and the parameters of the input spike train demonstrates marked nonlinearities. Burst response is shown to be selective to spike-silence-spike sequences in the input spike train. Moreover, burst events represent the input more reliably than the tonic spike in a considerable range of the parameters of the model. In conclusion, many of the distinctive properties of thalamic bursts such as stereotypy, nonlinear dependence on the sensory stimulus, feature selectivity and reliability are reproducible in the minimal model. Furthermore, the minimal model predicts that while the bursts are more frequent in the spike train of the off-center X relay neurons (corresponding to off-center X retinal ganglion cells), they are more reliable when generated by the on-center ones (corresponding to on-center X ganglion cells).     

Ionic mechanisms underlying spontaneous CA1 neuronal firing in Ca2+-free solution

Hippocampal CA1 neurons exposed to zero-[Ca(2+)] solutions can generate periodic spontaneous synchronized activity in the absence of synaptic function. Experiments using hippocampal slices showed that, after exposure to zero-[Ca(2+)](0) solution, CA1 pyramidal cells depolarized 5-10 mV and started firing spontaneous action potentials. Spontaneous single neuron activity appeared in singlets or was grouped into bursts of two or three action potentials. A 16-compartment, 23-variable cable model of a CA1 pyramidal neuron was developed to study mechanisms of spontaneous neuronal bursting in a calcium-free extracellular solution. In the model, five active currents (a fast sodium current, a persistent sodium current, an A-type transient potassium current, a delayed rectifier potassium current, and a muscarinic potassium current) are included in the somatic compartment. The model simulates the spontaneous bursting behavior of neurons in calcium-free solutions. The mechanisms underlying several aspects of bursting are studied, including the generation of triplet bursts, spike duration, burst termination, after-depolarization behavior, and the prolonged inactive period between bursts. We show that the small persistent sodium current can play a key role in spontaneous CA1 activity in zero-calcium solutions. In particular, it is necessary for the generation of an after-depolarizing potential and prolongs both individual bursts and the interburst interval.     

Efficient inhibition of bursts by bursts in the auditory system of crickets

In crickets, auditory information about ultrasound is carried bilaterally to the brain by the AN2 neurons. The ON1 neuron provides contralateral inhibitory input to AN2, thereby enhancing bilateral contrast between the left and right AN2s, an important cue for sound localization. We examine how the structures of the spike trains of these neurons affect this inhibitory interaction. As previously shown for AN2, ON1 responds to salient peaks in stimulus amplitude with bursts of spikes. Spike bursts, but not isolated spikes, reliably signal the occurrence of specific features of the stimulus. ON1 and AN2 burst at similar times relative to the amplitude envelope of the stimulus, and bursts are more tightly time-locked to stimulus feature than the isolated spikes. As a consequence, spikes that, in the absence of contralateral inhibition, would occur within AN2 bursts are more likely to be preceded by spikes in ON1 (mainly also in bursts) than are isolated AN2 spikes. This leads to a large decrease in the burst rate of the inhibited AN2. We conclude that the match in coding properties of ON1 and AN2 allows contralateral inhibition to be most efficient for those portions of the response that carry the behaviourally relevant information, i.e. for bursts. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Amplitude variability and extracellular low-pass filtering of neuronal spikes

The influence of neural morphology and passive electrical parameters on the width and amplitude of extracellular spikes is investigated by combined analytical and numerical investigations of idealized and anatomically reconstructed pyramidal and stellate neuron models. The main results are: 1), All models yield a low-pass filtering effect, that is, a spike-width increase with increasing distance from soma. 2), A neuron's extracellular spike amplitude is seen to be approximately proportional to the sum of the dendritic cross-sectional areas of all dendritic branches connected to the soma. Thus, neurons with many, thick dendrites connected to soma will produce large amplitude spikes, and therefore have the largest radius of visibility. 3), The spike shape and amplitude are found to be dependent on the membrane capacitance and axial resistivity, but not on the membrane resistivity. 4), The spike-amplitude decay with distance r is found to depend on dendritic morphology, and is decaying as 1/rⁿ with 1 ≤ n ≤ 2 close to soma and n ≥ 2 far away.     

Electrical activity of neurons in the cat cortex during cooling

Changes of the activity of cortical neurons were studied in the posterior crucial gyrus and in the middle parts of the suprasylvian and ectosylvian gyri on cooling the brain to 18°C and below. In exact experiments it was noted that cooling the cortex to 18.8–21.8° causes a complete cessation of neuron activity. The kinetics of the change of activity under these conditions follows a definite order: first an increase of the frequency of spike discharges is observed (31–27°), then a decrease of their amplitude (at 25–22°), and finally a complete disappearance of neuron activity (at 21.8–18.8°). Discontinuation of the cooling leads to restoration of the activity of the nerve cells in inverse order: low-amplitude high-frequency discharges manifest (at 23–26°), the amplitude of the spikes increases (at 29–31°) and then the initial activity is restored (at 31–32°). The decrease of neuron activity depends on the rate of temperature drop in the cortex. The faster the cortex is cooled, the lower is the temperature at which the neurons cease to function. And conversely, slow cooling of the cortex causes an inactivation of the spike potentials at a higher temperature.S. M. Kirov Gorki State Medical Institute. Translated from Neirofiziologiya, Vol. 2, No. 1, pp. 59–63, January–February, 1970.     

Linking dynamical and functional properties of intrinsically bursting neurons

Several studies have shown that bursting neurons can encode information in the number of spikes per burst: As the stimulus varies, so does the length of individual bursts.Therepresented stimuli, however, vary substantially among different sensory modalities and different neurons.The goal of this paper is to determine which kind of stimulus features can be encoded in burst length, and how those features depend on the mathematical properties of the underlying dynamical system.We show that the initiation and termination of each burst is triggered by specific stimulus features whose temporal characteristsics are determined by the types of bifurcations that initiate and terminate firing in each burst. As only a few bifurcations are possible, only a restricted number of encoded features exists. Here we focus specifically on describing parabolic, square-wave and elliptic bursters. We find that parabolic bursters, whose firing is initiated and terminated by saddle-node bifurcations, behave as prototypical integrators: Firing is triggered by depolarizing stimuli, and lasts for as long as excitation is prolonged. Elliptic bursters, contrastingly, constitute prototypical resonators, since both the initiating and terminating bifurcations possess well-defined oscillation time scales. Firing is therefore triggered by stimulus stretches of matching frequency and terminated by a phase-inversion in the oscillation. The behavior of square-wave bursters is somewhat intermediate, since they are triggered by a fold bifurcation of cycles of well-defined frequency but are terminated by a homoclinic bifurcation lacking an oscillating time scale. These correspondences show that stimulus selectivity is determined by the type of bifurcations. By testing several neuron models, we also demonstrate that additional biological properties that do not modify the bifurcation structure play a minor role in stimulus encoding. Moreover, we show that burst-length variability (and thereby, the capacity to transmit information) depends on a trade-off between the variance of the external signal driving the cell and the strength of the slow internal currents modulating bursts. Thus, our work explicitly links the computational properties of bursting neurons to the mathematical properties of the underlying dynamical systems.     

Temperature limits to early development of the New Zealand sea urchin Evechinus chloroticus (Valenciennes, 1846)

Seawater temperature is an important environmental factor for the early life stages of marine invertebrates. In this study we evaluated and described the effects of temperature during early development of E. chloroticus, identifying the optimum temperature range and upper thermal limit for successful development. The temperature range evaluated was between 15–24 °C which included the normal seawater temperatures during the spawning season in northern New Zealand, as well as the highest temperature projected by the IPCC for this region due to global warming (1–3 °C by the year 2100). Gametes from several females and males were used in the experiment. Fertilization was carried out at different temperatures and development was monitored at different time points after fertilization in each temperature. The development rate of E. chloroticus increased with an increase in seawater temperature. However, at temperatures higher than 21.5 °C the amount of abnormal development reached ∼30%. The optimum temperature for early development was between 15–21 °C, whereas the upper thermal limit was ∼24 °C. Therefore, early development of E. chloroticus is negatively affected by an increase in seawater temperature of ∼3–4 °C above current seawater temperature levels in northern New Zealand. The thermal sensitivity of early life stages of E. chloroticus could affect survival rates during early development of this species in a global warming scenario, which could impair recruitment in populations which are exposed to higher temperatures, leading to possible distributional shifts of this species.