Giant polyfunctional neuron of the edible snail

The structure of the receptive field of LPa3 neurone and its connection with the periphery were studied on semi-intact preparations of the snail Helix pomatia. It was found that: 1) The mechano-sensitive receptive field (excitatory) of the LPa3 neurone occupies nearly the whole surface of the snail's skin and internal organs. But latencies of LPa3 reactions to mechanical stimulation, the whole field may be divided into four zones: 50 to 60 ms, 100 ms, 130 to 140 ms and 200 to 250 ms. 2) Blockade of synaptic transmission with magnesium or cobalt has shown that relaying of the signal from the mantle receptors to the LPa3 neurone takes place in the peripheral nervous system. 3) Cobalt ionophoresis showed that the LPa3 neurone gives off processes to the right and left pallial nerves, the anal nerve and, occasionally, to the cutaneous nerve. During simultaneous intracellular recording from the LPa3 neurone and extracellular from the above nerves, action potentials are in every case recorded at first in the neurone body, and then, with a 20 to 30 ms delay, in the nerves. This means that the LPa3 neurone processes joining the nerves are axons. It is suggested that the sensory inputs and wide branching structures output of the LPa3 neurone axons make it an integrating polyfunctional system.     

The monosynaptic connection: the modulating effect of opioid peptides on the plasticity of presynaptic neurons and identified synapses]

Study of opioid peptides (leucine-enkephalin and methionine-enkephalin) action on plastic properties of the system of monosynaptically connected neurones LPa7--LPa3, PPa3 and LPa8--LPa3, PPa3 was conducted in the snail brain. It has been shown that all three links in the system studied (presynaptic neurone, postsynaptic neurone and synapse) manifest one and the same type of plasticity--habituation to rhythmic stimulation. Enkephalins have a modulating action on plastic properties of the presynaptic neurone and synapse: they retard the habituation of the presynaptic neurone to intracellular stimulation and retard the development of habituation at synaptic level. However, changes in the character of postsynaptic response in the presence of enkephalins are not a direct consequence of their influence on plastic properties of the presynaptic neurone. Besides, enkephalines reduce the effectiveness of synaptic transmission in the given system: they reduce EPSP duration in the postsynaptic neurone.     

Disinhibition as a mechanism of tuning of cross-like figures in the visual cortex neurons

A discrete neural net was used for simulation of cross-sensitivity in 40% of neurones of the cat visual cortex' area 17th. It is based on disinhibition of the end-stopping inhibition in receptive field from the side-disinhibitory zone. Highly selective or invariant sensitivity of the simulated neurone in respect to shape and orientation of a cross-like figure was observed under changes of location, size and weight of the receptive field zones. The disinhibitory mechanism seems to be critically involved in the selection of the second-order features of the images in the primary visual cortex.     

Postsynaptic mechanism of withdrawal reflex sensitization in the snail

Repeated tactile stimulation of the skin evoked sensitization and subsequent habituation of a behavioral avoidance reaction of pneumostome closure in the land snail, Helix lucorum L. Spike responses in putative command neurons for avoidance behavior increased and subsequently decreased parallel to behavioral events. Decrease of spike responses in command neurons was due to decreased synaptic input evoked by repeated tactile stimulation. Intracellular investigation of the increase in the spike response in command neurons for pneumostome closure, which underlies behavioral sensitization, revealed a synpatically-evoked, long-lasting depolarization. No conductance changes during this depolarization were found, but neuronal excitability was altered.     

Induction of plastic changes in the excitability of neuronal electrogenic membranes during habituation

Habituation of the postsynaptic response of a turtle cortical neurone to an orthodromic stimulus, induces enhanced excitability of the electro-excitable membrane which does not generate action potentials during habituation. Single excitation of the electro-excitable membrane by intracellular stimulation during this period, facilitates transmitter sensitivity of the chemoreceptor membrane. Habituation of the action potential to the intracellular electrical stimulus induces enhanced sensitivity of the chemoreceptor membrane. Single excitation of the chemoreceptor membrane during this period results in enhanced excitability of the electro-excitable membrane. Plastic changes during habituation involve the whole neurone membrane, although the monotonous stimulus activates only its local area.     

Configurational pattern discrimination responsible for dishabituation in common toads Bufo bufo (L.): Behavioral tests of the predictions of a neural model

Summary Recently, a neural model of visual pattern discrimination for stimulus-specific habituation was developed, based on previous behavioral studies which demonstrated that toads exhibit a dishabituation hierarchy for different worm-like stimuli. The model suggests that visual objects are represented by temporal coding and predicts that the dishabituation hierarchy changes when the stimulus/background contrast direction is reversed or the stimulus size is varied. The behavioral experiments reported in this paper were designed to test these predictions, (1) For a pair of stimuli from the contrast reversal prediction, the experimental results validated the theory. (2) For a pair of stimuli from the size reduction prediction, the experimental results failed to validate the theory. Further experiments concerning size effects suggest that configurai visual pattern discrimination in toads exhibits size invariance. (3) Inspired by the Groves-Thompson account of habituation, we found that dishabituation by a second stimulus has a separate process from habituation to a first stimulus. This paper serves as an example of a fruitful dialogue between experimentation and modeling, crucial for understanding brain functions.Abbreviations a-h worm-like stimulus patterns - AT anterior thalamus - ERF excitatory receptive field - IRF inhibitory receptive field - RF receptive field - R2 to R4 retinal ganglion cell types - vMP posterior ventromedial pallium     

Effect of enkephalins on the plasticity of pond snail

The effects of introduction of leu- and met-enkephalins (LE and ME) into the perfusion medium on the characteristics of electrical activity, spontaneous firing and habituation of single neurones to repeated intracellular electrical stimulation were studied on isolated CNS of molluscs. The character, speed, and degree of development of endoneuronal habituation changed significantly after application of LE in 67 per cent of the neurones studied and in 25 per cent of neurones after ME application. As a rule the changes of habituation dynamics occurred at constant levels of membrane potential, excitability, and reactivity of the neurone. LE and ME exerted different modulating effects on the initial electrical activity in 60 per cent of neurones. The obtained data on the independence of the effects of enkephalins on different parameters of activity of one and the same neurone give evidence of a mosaic character of excitable neuronal membrane. A suggestion is made about the possible role of the revealed opiate dependence of the endoneuronal functional plasticity in realization of opiate influences at the behavioural level.     

Responses of high-frequency movement detector neurons in dragonfly larvae to motion of complex patterns

Neurons of the class described respond by a discharge with a frequency of 150–200/sec to the appearance and motion of single dark objects in a new part of the large receptive field. Movement of a complex pattern induces a weak initial response. Repeated movements of a complex pattern evoke habituation and do not affect the firing rate but they suppress the response to movement of a single object at distances of up to 15–30° away from the zone of habituation. The features of optic stimuli evoking maximal responses in high-frequency movement detector neurons correspond in many cases to the features of objects evoking fright and flight in the larvae.     

The effect of a vasopressin analog on the reaction of the command neurons in the defensive behavior of the edible snail during nerve stimulation

On the level of snail command neurones of the defensive behaviour an increase was revealed of the amplitude of summary EPSP recorded in command neurones in response to nerve stimulation, an increase of probability of appearance of action potential in the reaction and, under certain conditions, a significant decrease of habituation speed at rhythmic (0.1 Hz) nerve stimulation against the background of peptide. The latter effect was found during comparison of groups of neurones--control neurones and those to which the peptide was presented before the first series of stimulation in the test, i. e. without preliminary elaboration of habituation. The decrease of the speed of habituation concerned both the amplitude of summary EPSP and the probability of action potential appearance in the reaction. All these changes against the background of vasopressin analogue may be the basis of the increase of spike reactions of command neurones of the defensive behaviour and thus the basis of the initiation or the increase of behavioural defensive reactions. The obtained effects were not protracted and took place only in the presence of the peptide in the extracellular medium.     

The role of dopamine and serotonin in modulating the defensive behavior of the edible snail

Dopamine application in concentration of 10(-5)-10(-6) M into saline around the snail CNS leads to decrease of excitability of LPa7 neurone which is presynaptic in relation to defensive behaviour command neurones, and to decrease of amplitude of monosynaptic excitatory postsynaptic potential (EPSP) in the command neurones elicited by intracellular stimulation of LPa7 neurone. Besides, the dopamine causes a decrease of summated EPSP amplitude in the studied neurones in response to intestinal nerve stimulation (70% in average), a change of rest potential towards hyperpolarization for 6-8 mV, a reduction of the command neurones input resistance (20% in average). The described influences can lead to a general increase of the threshold of defensive system reaction to stimulation. Dopamine action on the defensive behaviour command neurones is significantly weakened in serotonine presence. Against the dopamine background, the efficiency of serotonine influence on the value of EPSP in command neurones in response to testing stimulus is reduced. According to the obtained data, a conclusion is made that interrelation of dopamine and serotonine concentrations can be a base for formation of behaviour choice in snail.     

The cardioregulatory system of crayfish: The role of circumoesophageal interneurones.

1. Interneurones located in the circumoesophageal commissures were found to control the activity of the cardioinhibitor and cardioaccelerator regularity neurones. 2. These interneurones (cardiac command fibres) fell into three classes: (1) strong inhibitors, which caused cardiac arrest, (2) weak inhibitors, which caused bradycardia, and (3) accelerators, which caused tachycardia. 3. When the positions of interneurones were plotted collectively, they formed distinct clusters, suggesting that each cluster was represented by one command unit in an individual preparation. Twenty strong inhibitor units and 16 accelerator units were found. Weak inhibitors did not form clusters. 4. Stimulus threshold characteristics were as low as 3.0 V and 3 Hz for the strong inhibitor units (mean range 4.7-7.1 V and 14-30 Hz). Higher values were found for weak inhibitors and accelerators. 5. The strong inhibitor command drives always showed a positive bias toward the contralateral cardioinhibitor neurone, relative to the ipsilateral cardioinhibitor. 6. Plots of command neurone stimulating frequency versus evoked cardio-inhibitor activity displayed steep positive slopes for strong inhibitor command units and shallow positive slopes for weak inhibitor units. 7. Reciprocity between the cardioinhibitor and cardioaccelerator neurones occurred during both inhibitory and acceleratory command drives. This is not likely to be a property inherent in the command units themselves because reciprocity was earlier observed during chemical and tactile reflex inhibition of the heart. (Field & Larimer, 1974a).     

The neurochemical basis of recurrent inhibition in the reflex arch of the defensive reaction]

Mechanisms of habituation in the network of identified neurones were investigated in isolated preparation of central nervous system in the snail Helix. It has been found that intracellularly induced spike discharge in premotor command neurones decreases synaptic responses to repeated nerve stimulation in all recorded command neurones. Application of the neuropeptide FMRFamide elicits similar changes in the network. Taking into account that the investigated command neurones contain FMRFamide, as was shown immunochemically, it is possible to assume the existence of recurrent inhibition in the network underlying avoidance reactions. This recurrent inhibition causes habituation of the network output in the cases when the repeated stimuli do not evoke sensitization via activation of serotonergic cells.     

Neuronal correlates of changes in the defensive behavior of Helix lucorum L. during ontogeny

In experiments on the isolated nervous system, responses of the same command neurones of avoidance behaviour to electrical stimulation of the intestinal nerve were compared in adult snails (Helix pomatia) and in snails 1-20 days old. Dynamics of spike reactions of the command neurones to rhythmic nerve stimulation differed in adult and newborn snails. In the neurones of young snails, no sensitization, common in the adult animals, was observed. Study of excitatory input in the command neurones during rhythmic nerve stimulation suggests independence of habituation of synaptic input amplitude and spike response sensitization, because dynamics of habituation coincided in the young and adult snails while spike response underwent sensitization only in adult animals.     

Responses of high-frequency movement detector neurons in dragonfly larvae to motion of single objects

Neurons of the class described respond by a discharge with a frequency of 150–250/sec to motion of single objects in a large receptive field. The response depends directly on the size of the object. The neurons are selectively sensitive to motion of dark objects. Widening a dark border (bringing a black disc closer) evokes a stronger response than narrowing a dark border (moving a white disc further away). The response to uniform movement consists of high-frequency volleys of discharges separated by pauses. Repeated movements along the same trajectory induce habituation; after cessation of the movements sensitivity is restored with a time constant of about 30 sec. The role of lateral inhibition and local habituation in the identification of the specific features of optical stimuli is discussed.     

Possible relation between learning and non-template RNA synthesis in neurons

A substrate of either matrix-(cytidinetriphosphate, CTPh) or non-matrix (cytidinediphosphate, CDPh, or uridinediphosphate, UDPh) RNA synthesis was injected into mollusc neurone by means of intracellular microionophoresis. Subsequently, habituation was elaborated, assuming that if this process depends on the RNA synthesis, then the formation of defective RNA molecules with an excessive content of cytidine or uridine will disturb the learning process. In control experiments, habituation was elaborated either without drugs administration or following an injection of cytidinemonophosphate non subject to polymerization, or of an equimolar mixture of four ribonucleotidediphosphates: CDPh+UDPh+ADPh++GDPh. In the latter case a minimal distortion of the ratio between the initial substrates of the non-matrix RNA synthesis was expected. Both in the control experiments and following CTPh administration, the habituation was attended with an increase of threshold and latencies of spikes evoked by repeated stimuli. Injection of CDPh or UDPh disturbed the dynamics of thresholds and latencies increase in the course of habituation. The data obtained suggest that the habituation process is connected with a non-matrix synthesis of RNA in the neurones.     

Principle of neuronal organization of defensive reflexes in mollusks

Spontaneous and evoked synaptic activity of command neurons for the defensive response of spiracle closing were studied by simultaneous intracellular recording of activity of several identified CNS neurons in snails. Comparison of monosynaptic EPSPs in command neurons evoked by discharges of presynaptic neurons with spontaneous synaptic potentials indicated that the central organization of the defensive reflex is in the form of a two-layered neuron net in which each neuron of the afferent layer possesses a local receptive field, but which overlaps with other afferent neurons. Each neuron of the afferent layer is connected with each neuron of the efferent layer by monosynaptic excitatory connections that differ in efficiency (maximal only with one neuron of the efferent layer). Both receptive fields of neurons of the afferent layer and "fields of efficiency of synaptic connections" are distributed according to the normal law. As a result of this organization the neuron net acquires a new quality: The action of different stimuli leads to the appearance of differently located "spatial excitation profiles" of efferent layer neurons even when this action of the stimulus occurs not at the center of the receptive field.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 1, pp. 26–34, January-February, 1984.     

Sensitization and habituation of command neurons during a defensive reflex in grape snails

All investigated neurones were classified into functional groups depending on their participation in unconditioned avoidance reflex of pneumostome closure. Habituation was produced by tactile stimuli applied with a frequency of 0.1 c/s. Spike responses of neurons participating in processing sensory information habituated gradually, while reactions of command neurones of avoidance behaviour became sensitized to the second or third stimulus of the series. Behavioral reaction was sensitized in parallel with command neurones in spite of habituation in other types of nerve cells. A conclusion is drawn that behavioral habituation is due to waning of responses in all the participating neurones, but the independnet process of sensitization is due to sensitization of command neurones. Probable mechanisms of neuronal sensitization are discussed.     

A model of the neural mechanisms responsible for pattern recognition and stimulus specific habituation in toads

A neural model of the mechanisms possibly responsible for stimulus-specific habituation in toads is proposed. The model follows the hypothesis that preypredator recognition is performed by command units as a result of retina-tectum-pretectum interaction. The model allow us to study the possible coding that the nervous system of toads uses for different prey stimuli, the neural mechanisms of habituation and dishabituation, and the dynamic changes that the command units may have during these processes. The model proposes specific hypothesis and experiments to clarify the nature of these processes and to test the validity of the command unit hypothesis.Research supported in part by CONACYT under grant PCCBBNA 021005Research supported in part by the NIH under grant NS 14971-05 from National Institute of Neurological and Communicative Disorders and Stroke     

Temperature dependent plasticity of habituation in the crayfish

To determine the effects of thermal preconditioning on a simple form of learning and memory, habituation, we preconditioned crayfish with extreme temperatures and subsequently analysed their effects on mechanosensory input that evokes a response in the lateral giant interneurons, within the normal temperature range of the animal. We found that repetitive stimulation with a 1 s interstimulus interval led to habituation of the response the lateral giant in control animals at 22°C. Neither heat nor cold preconditioning had any effect on the probability of evoking a response in the lateral giant nor on the rate at which habituation occurred. With a 1 min interstimulus interval, however, the rate of habituation of the lateral giant in the heat-preconditioned group was less than either the control or cold-preconditioned animals. The effect of heat or cold pre-exposure was specific to the input to the lateral giant at control temperatures. For example, at 22°C prior heat and cold preconditioning had no effect on spontaneous reductor motor neurone activity. They did, however, provide thermoprotection at extreme temperatures, with the probability of spontaneous activity higher in the cold-preconditioned group at low temperatures but higher in the heat-preconditioned group at higher temperatures.     

Specific Relationship between Excitatory Inputs and Climbing Fiber Receptive Fields in Deep Cerebellar Nuclear Neurons

Many mossy fiber pathways to the neurons of the deep cerebellar nucleus (DCN) originate from the spinal motor circuitry. For cutaneously activated spinal neurons, the receptive field is a tag indicating the specific motor function the spinal neuron has. Similarly, the climbing fiber receptive field of the DCN neuron reflects the specific motor output function of the DCN neuron. To explore the relationship between the motor information the DCN neuron receives and the output it issues, we made patch clamp recordings of DCN cell responses to tactile skin stimulation in the forelimb region of the anterior interposed nucleus in vivo. The excitatory responses were organized according to a general principle, in which the DCN cell responses became stronger the closer the skin site was located to its climbing fiber receptive field. The findings represent a novel functional principle of cerebellar connectivity, with crucial importance for our understanding of the function of the cerebellum in movement coordination.