A nonlinear cascade model for action potential encoding in an insect sensory neuron.

Action potential encoding in the cockroach tactile spine neuron can be represented as a single-input single-output nonlinear dynamic process. We have used a new functional expansion method to characterize the nonlinear behavior of the neural encoder. This method, which yields similar kernels to the Wiener method, is more accurate than the latter and is efficient enough to obtain reasonable kernels in less than 15 min using a personal computer. The input stimulus was band-limited white Gaussian noise and the output consisted of the resulting train of action potentials, which were unitized to give binary values. The kernels and the system input-output signals were used to identify a model for encoding comprising a cascade of dynamic linear, static nonlinear, and dynamic linear components. The two dynamic linear components had repeatable and distinctive forms with the first being low-pass and the second being high-pass. The static nonlinearity was fitted with a fifth-order polynomial function over several input amplitude ranges and had the form of a half-wave rectifier. The complete model gave a good approximation to the output of the neuron when both were subjected to the same novel white noise input signal.     

Kernel and nonlinear canonical correlation analysis

We review a neural implementation of the statistical technique of Canonical Correlation Analysis (CCA) and extend it to nonlinear CCA. We then derive the method of kernel-based CCA and compare these two methods on real and artificial data sets before using both on the Blind Separation of Sources.     

Dynamics and metamorphosis of an identifiable peptidergic neuron in an insect

Eclosion hormone (EH) is a 7000 Da peptide that triggers ecdysis behavior in insects. In the moth, Manduca sexta, EH is found in two pairs of ventromedial (VM) cells in the brain which send their axons down the ventral nerve cord to a neurohemal site in the proctodeal nerve in the larva and pupa. During adult development, these cells send axon collaterals to the corpora cardiaca where they form a new release site used for adult eclosion. Studies of bioassayable peptide during the 5th larval instar and the larval-pupal transformation revealed that after depletion at ecdysis, the VM cells showed a transient increase in EH found in their cell bodies and axons. By contrast, their terminals in the proctodeal nerve showed a gradual accumulation of peptide followed by a release of over 90% of the stored material at pupal ecdysis. In situ hybridization analysis on whole mounts of the brains showed that the VM cells always contained EH mRNA with increased accumulation during the larval and pupal molting periods with a slight decline just before ecdysis. High levels of EH mRNA were found in brains of diapausing pupae. During the first two-thirds of adult development, mRNA accumulated to high levels, then slowly declined until ecdysis. EH mRNA levels up to 3 days after adult eclosion. At no time was EH mRNA found in the lateral neurosecretory cell cluster previously reported to produce EH for adult eclosion. 1994 John Wiley & Sons, Inc.     

Removal of rapid sensory adaptation from an insect mechanoreceptor neuron by oxidizing agents which affect sodium channel inactivation

1. The femoral tactile spine of the cockroach is a mechanoreceptor with a single sensory neuron. The response to a step movement is a burst of action potentials which decays to zero in about 1 s. This rapid adaptation is a property of the action potential initiating region of the neuron. 2. The oxidizing agents chloramine-T and N-chlorosuccinimide selectively and irreversibly remove sodium channel inactivation from neurons in several preparations and are believed to act by oxidation of methionine or cysteine residues in the proteins of the sodium channel. 3. Chloramine-T and N-chlorosuccinimide, applied for a controlled time period, eliminated the rapid adaptation of the tactile spine neuron to an electrical depolarization. After treatment it fired tonically in response to a steady current stimulus. Longer applications of the agents eventually raised the threshold for action potential initiation. 4. Threshold behavior in the tactile spine neuron was characterized by measuring strength-duration relationships for stimulation with extracellular current pulses at the action potential initiating region. The two oxidizing agents caused a voltage-dependent modification of the dynamic threshold properties which led to the change from rapidly adapting to tonic behavior. 5. Two stronger oxidizing agents, N-bromoacetamide and N-bromosuccinimide, raised the threshold of the neuron without removing rapid adaptation. These two agents act similarly to chloramine-T and N-chlorosuccinimide on sodium inactivation in other neurons but are believed to oxidize the tryptophan, tyrosine and histidine residues of proteins in addition to cysteine and methionine.(ABSTRACT TRUNCATED AT 250 WORDS)     

Sensory transduction in an insect mechanoreceptor: Linear and nonlinear properties

Mechanotransduction in the femoral tactile spine of the cockroach, Periplaneta americana, was examined as a function of displacement of the spine axially in its socket. Linear behaviour was analyzed by measurement of the frequency response function between displacement and action potential output using sinusoidal stimulation and random noise stimulation. The measured frequency response functions can be well fitted by a relationship which is a fractional power of complex frequency. This power was close to 0.5 for all experiments. To distinguish between the effects of nonlinearity and of inherent variability, the averaged responses of the preparation to repeated sequences of pseudorandom noise were compared to those from experiments in which continuous pseudorandom noise were used. The lack of sensitivity of the coherence function to these two methods of measurement suggests that mechanical stimuli are encoded into action potentials with a large signal-to-noise ratio. The low value of the coherence function which is characteristics of insect mechanoreceptors is therefore due to the strong non-linearity of their responses. To investigate the nonlinear properties of transduction, the second-order frequency response function of the tactile spine was measured for random noise stimulation experiments. Two models of the transduction process were considered in which a linear element with memory was cascaded with a nonlinear element without memory in the two possible configurations. Comparison of the experimental second-order frequency response functions with predictions based upon these two models and the measured first-order frequency response suggests that the transduction mechanism can be modelled by a linear element, which may be associated with the viscoelastic properties of the dendritic tubular body, and a zeromemory nonlinearity, which is most likely to be rectification by the dendritic membrane.     

Auditory change detection by a single neuron in an insect

The detection of novel signals in the auditory scene is an elementary task of any hearing system. In Neoconocephalus katydids, a primary auditory interneuron (TN-1) with broad spectral sensitivity, responded preferentially to rare deviant pulses (7 pulses/s repetition rate) embedded among common standard pulses (140 pulses/s repetition rate). Eliminating inhibitory input did not affect the detection of the deviant pulses. Detection thresholds for deviant pulses increased significantly with increasing amplitude of standard pulses. Responses to deviant pulses occurred when the carrier frequencies of deviant and standard were sufficiently different, both when the deviant had a higher or lower carrier frequency than the standard. Recordings from receptor neurons revealed that TN-1 responses to the deviant pulses did not depend on the population response strength of the receptors, but on the distribution of the receptor cell activity. TN-1 responses to the deviant pulse occurred only when the standard and deviant pulses were transmitted by different groups of receptor cells. TN-1 responses parallel stimulus specific adaptation (SSA) described in mammalian auditory system. The results support the hypothesis that the mechanisms underlying SSA and change-detection are located in the TN-1 dendrite, rather than the receptor cells.     

Location and dynamic properties of the spike generator in an insect mechanosensory neuron

1.The cereal bristle hairs of the cockroach, Periplaneta americana, are each innervated by one mechanosensory cell and 1–5 chemosensory cells. In transepithelial recordings, chemo- and mechanosensory spikes could be discriminated from each other by their relative amplitude. 2. When current steps were applied via the sensory hair, trains of impulses were triggered whatever the polarity of the current. 3. All responses adapted to the current, but the time course of adaptation was fitted by a power law for outward currents and an exponential law for inward currents. 4. During application of outward currents, the spikes showed a negative initial phase on which a small positive component was superimposed; strong polarizations produced purely negative spikes. More classical spikes with a positive initial phase were induced by inward currents. 5. The present work supports the hypothesis of a direct excitability of the apical dendrite in cereal bristle mechanoreceptors and confirms previous results suggesting that spikes are normally triggered within that region during mechanical stimulations. It is also established, for the first time, that adaptation to currents may be different in the apical dendrite and in more basal regions of the same mechanosensory neuron.Abbreviation RP receptor potential - TEV transepithelial voltage - TTX tetrodotoxin     

Dynamic properties of the action potential encoder in an insect mechanosensory neuron

A variety of sensory receptors show adaptation to dynamic stimuli that can be well characterized as fractional differentiation of the input signal. The cause of this behavior is unknown, but because it can be represented by linear systems theory, it has been assumed to arise during early linear processes of transduction or adaptation, rather than during the nonlinear process of action potential encoding. I measured the action potential encoding properties of an insect mechanoreceptor by direct electrical stimulation of the sensory cell axon and found a dynamic response that is identical to the response given by mechanical stimulation. This indicates that the fractional differentiation is a property of the encoder rather than the transducer.     

Ionic events following GABA receptor activation in an identified insect motor neuron

The ionic events underlying gamma-aminobutyric acid (GABA) receptor activation on the cell body of a cockroach identified motor neuron were investigated by using current-clamp and voltage-clamp techniques. The reversal potential for GABA-induced hyperpolarization was -77.0 +/- 2.4 mV (mean +/- s.e.m.; n = 22). The reversal potential for GABA was highly sensitive to changes in external chloride, only weakly affected by changes in external potassium, and independent of changes in either sodium or calcium ion concentration. Intracellular ion-sensitive microelectrodes confirmed that an influx of chloride ions mediated the GABA response. Intracellular injection of acetate, citrate, sulphate, fluoride or ammonium caused no change in the reversal potential for GABA. Intracellular injection of chloride, bromide, chlorate, bromate, or methyl sulphate shifted the reversal potential for GABA to values more positive than resting membrane potential. Evidence for chloride accumulating and for extrusion mechanisms was examined by using putative inhibitors. However, internal application of ammonium ions, and external application of 4-acetamido-4'-isothiocyanatostilbene-2,2'-disulphonic acid (SITS), 4,4'-diisothiocyanatostilbene-2,2'-disulphonic acid (DIDS), acetazolamide, furosemide, ammonium, zinc and copper ions, were all without effect on the reversal potential for GABA.     

Action cascade of an insect gonadotropin,testis ecdysiotropin,in male Lepidoptera

Summary

Testis sheaths from late last instar larvae and mid-developing pupae of Heliothis virescens and Lymantria dispar synthesize ecdysteroid in vitro. Gonadal ecdysteroid can stimulate the production of growth factors from the sheaths which, in turn, promote the growth and development of the genital tract. Ongoing basal synthesis is controlled by positive feedback to exogenous ecdysteroid; titers of this hormone approaching those of molting last instar larvae and developing pupae effect maximum synthesis. These findings suggest that circulating titers of ecdysteroid hormone promote gonadal ecdysteroidogenesis, and thus coordinate the actions of the gonads with metamorphic events in the whole animal. Synthesis of ecdysteroid by testes is initiated, however, by a brain neuropeptide, testis ecdysiotropin (TE). TE is a 21 amino acid peptide of molecular weight 2472 Da. TE boosts basal steroid synthesis by pupal testis sheaths as well. It acts primarily via G_i protein and second messengers diacyl glycerol and low calcium influx, resulting in stimulation of phosphokinase C. G_s protein and its resultant messenger, cyclic AMP, also play roles in activation and inhibition of ecdysteroidogenesis. The interplay of controlling systems probably serves to fine tune a system essential to gonadal development and function.     

Steroid control of neuron and muscle development during the metamorphosis of an insect

Insect metamorphosis is controlled by a small ensemble of developmental hormones including a class of steroids--the ecdysteroids. In the tobacco hornworm, Manduca sexta, the progression from the larval to pupal to adult stages is controlled by the relative blood titers of ecdysteroids and juvenile hormone (JH). The cellular events in the nervous and muscular systems which accompany metamorphosis resemble those of embryonic development, but they occur in an animal which is larger and experimentally more tractable than an embryo. In this paper we review the role of ecdysteroids in directing the metamorphosis of the nervous and muscular systems in Manduca, and how JH modifies the cellular responses to the steroids. In particular, we describe how these hormones control muscle degeneration, changes in the structure and function of identified neurons, and programmed neuron death. One general finding is that interactions between cells (e.g., neurons and their target muscles) are not involved in their hormonal responses, but rather the hormones act independently and in parallel at the different sites. Another key finding is that the critical periods and hormonal requirements for the commitment to a particular differentiative pathway, and the phenotypic expression of that pathway, can differ, and are therefore experimentally separable. Finally, we find that the significance of a hormonal signal (e.g., a rise in blood ecdysteroids) is interpreted differently depending upon the previous history of hormone exposure of a neuron or muscle. This progressive change in the interpretation of hormonal signals is a major mechanism by which a limited number of hormones can orchestrate a complicated phenomenon such as metamorphosis.     

GABA receptors on the cell-body membrane of an identified insect motor neuron

The pharmacology of a gamma-aminobutyric acid (GABA) receptor on the cell body of an identified motor neuron of the cockroach (Periplaneta americana) was investigated by current-clamp and voltage-clamp methods. Iontophoretic application of GABA increased membrane conductance to chloride ions, and prolonged application resulted in desensitization. Hill coefficients, determined from dose-response data, indicated that binding of at least two GABA molecules was required to activate the chloride channel. Differences between vertebrate GABAA receptors and insect neuronal GABA receptors were detected. For the GABA receptor of motor neuron Df, the following rank order of potency was observed: isoguvacine greater than muscimol greater than or equal to GABA greater than 3-aminopropanesulphonic acid. The GABAB receptor agonist baclofen was inactive. Of the potent vertebrate GABA receptor antagonists (bicuculline, pitrazepin, RU5135 and picrotoxin), only picrotoxin (10(-7) M) produced a potent, reversible block of the response to GABA of motor neuron Df. Both picrotoxinin and picrotin also blocked GABA-induced currents. Bicuculline hydrochloride (10(-4) M) and bicuculline methiodide (10(-4) M) were both ineffective when applied at resting membrane potential (-65 mV), although at hyperpolarized levels partial block of GABA-induced current was sometimes observed. Pitrazepin (10(-4) M) caused a partial, voltage-independent block of GABA-induced current. The steroid derivative RU5135 was inactive at 10(-5) M. In contrast to the potent competitive blockade of vertebrate GABAA receptors by bicuculline, pitrazepin and RU5135, none of the weak antagonism caused by these drugs on the insect GABA receptor was competitive. Flunitrazepam (10(-6) M) potentiated GABA responses, providing evidence for a benzodiazepine site on an insect GABA-receptor-chloride-channel complex.