Odor-evoked responses in the olfactory center neurons in the terrestrial slug

The procerebrum (PC) of the terrestrial mollusk Limax is a highly developed second-order olfactory center consisting of two electrophysiologically distinct populations of neurons: nonbursting (NB) and bursting (B). NB neurons are by far the more numerous of the two cell types. They receive direct synaptic inputs from afferent fibers from the tentacle ganglion, the primary olfactory center, and also receive periodic inhibitory postsynaptic potentials (IPSPs) from B neurons. Odor-evoked activity in the NB neurons was examined using perforated patch recordings. Stimulation of the superior tentacle with odorants resulted in inhibitory responses in 45% of NB neurons, while 11% of NB neurons showed an excitatory response. The specific response was reproducible in each neuron to the same odorant, suggesting the possibility that activity of NB neurons may encode odor identity. Analysis of the cycle-averaged membrane potential of NB neurons revealed a correlation between the firing rate and the membrane potential at the plateau phase between IPSPs. Also, the firing rate of NB neurons was affected by the frequency of the IPSPs. These results indicate the existence of two distinct mechanisms for the regulation of NB neuron activity.     

Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta

Intracellular recordings were made from the major neurites of local interneurons in the moth antennal lobe. Antennal nerve stimulation evoked 3 patterns of postsynaptic activity: (i) a short-latency compound excitatory postsynaptic potential that, based on electrical stimulation of the antennal nerve and stimulation of the antenna with odors, represents a monosynaptic input from olfactory afferent axons (71 out of 86 neurons), (ii) a delayed activation of firing in response to both electrical- and odor-driven input (11 neurons), and (iii) a delayed membrane hyperpolarization in response to antennal nerve input (4 neurons).Simultaneous intracellular recordings from a local interneuron with short-latency responses and a projection (output) neuron revealed unidirectional synaptic interactions between these two cell types. In 20% of the 30 pairs studied, spontaneous and current-induced spiking activity in a local interneuron correlated with hyperpolarization and suppression of firing in a projection neuron. No evidence for recurrent or feedback inhibition of projection neurons was found. Furthermore, suppression of firing in an inhibitory local interneuron led to an increase in firing in the normally quiescent projection neuron, suggesting that a disinhibitory pathway may mediate excitation in projection neurons. This is the first direct evidence of an inhibitory role for local interneurons in olfactory information processing in insects. Through different types of multisynaptic interactions with projection neurons, local interneurons help to generate and shape the output from olfactory glomeruli in the antennal lobe.Abbreviations AL antennal lobe - EPSP excitatory postsynaptic potential - GABA -aminobutyric acid - IPSP inhibitory postsynaptic potential - LN local interneuron - MGC macroglomerular complex - OB olfactory bulb - PN projection neuron - TES N-tris[hydroxymethyl]methyl-2-aminoethane-sulfonic acid     

Novel peripheral motor neurons in the posterior tentacles of the snail responsible for local tentacle movements

Three flexor muscles of the posterior tentacles of the snail Helix pomatia have recently been described. Here, we identify their local motor neurons by following the retrograde transport of neurobiotin injected into these muscles. The mostly unipolar motor neurons (15–35 µm) are confined to the tentacle digits and send motor axons to the M2 and M3 muscles. Electron microscopy revealed small dark neurons (5–7 µm diameter) and light neurons with 12–18 (T1 type) and 18–30 µm diameters (T2 type) in the digits. The diameters of the neurobiotin-labeled neurons corresponded to the T1 type light neurons. The neuronal processes of T1 type motor neurons arborize extensively in the neuropil area of the digits and receive synaptic inputs from local neuronal elements involved in peripheral olfactory information processing. These findings support the existence of a peripheral stimulus–response pathway, consisting of olfactory stimulus—local motor neuron—motor response components, to generate local lateral movements of the tentacle tip (“quiver”). In addition, physiological results showed that each flexor muscle receives distinct central motor commands via different peritentacular nerves and common central motor commands via tentacle digits, respectively. The distal axonal segments of the common pathway can receive inputs from local interneurons in the digits modulating the motor axon activity peripherally without soma excitation. These elements constitute a local microcircuit consisting of olfactory stimulus—distal segments of central motor axons—motor response components, to induce patterned contraction movements of the tentacle. The two local microcircuits described above provide a comprehensive neuroanatomical basis of tentacle movements without the involvement of the CNS.     

Spike-timing precision and neuronal synchrony are enhanced by an interaction between synaptic inhibition and membrane oscillations in the amygdala

The basolateral complex of the amygdala (BLA) is a critical component of the neural circuit regulating fear learning. During fear learning and recall, the amygdala and other brain regions, including the hippocampus and prefrontal cortex, exhibit phase-locked oscillations in the high delta/low theta frequency band (～2-6 Hz) that have been shown to contribute to the learning process. Network oscillations are commonly generated by inhibitory synaptic input that coordinates action potentials in groups of neurons. In the rat BLA, principal neurons spontaneously receive synchronized, inhibitory input in the form of compound, rhythmic, inhibitory postsynaptic potentials (IPSPs), likely originating from burst-firing parvalbumin interneurons. Here we investigated the role of compound IPSPs in the rat and rhesus macaque BLA in regulating action potential synchrony and spike-timing precision. Furthermore, because principal neurons exhibit intrinsic oscillatory properties and resonance between 4 and 5 Hz, in the same frequency band observed during fear, we investigated whether compound IPSPs and intrinsic oscillations interact to promote rhythmic activity in the BLA at this frequency. Using whole-cell patch clamp in brain slices, we demonstrate that compound IPSPs, which occur spontaneously and are synchronized across principal neurons in both the rat and primate BLA, significantly improve spike-timing precision in BLA principal neurons for a window of ～300 ms following each IPSP. We also show that compound IPSPs coordinate the firing of pairs of BLA principal neurons, and significantly improve spike synchrony for a window of ～130 ms. Compound IPSPs enhance a 5 Hz calcium-dependent membrane potential oscillation (MPO) in these neurons, likely contributing to the improvement in spike-timing precision and synchronization of spiking. Activation of the cAMP-PKA signaling cascade enhanced the MPO, and inhibition of this cascade blocked the MPO. We discuss these results in the context of spike-timing dependent plasticity and modulation by neurotransmitters important for fear learning, such as dopamine.     

Synaptic mechanisms controlling receptor unit activity in the stretch receptor—Abdominal ganglionic chain system of the crayfish

Inhibitory control over activity of the receptor neuron was investigated in a preparation of the stretch receptor and abdominal ganglionic chain in crayfishes. Potentials were recorded intracellularly from receptor neurons and neurons of the abdominal ganglion, and extracellularly from the dorsal roots. IPSPs appeared in the receptor neuron in response to stimulation of that same neuron or of the abdominal ganglionic chain. The relationship between spikes at the input and output of the inhibitory neuron varied over a wide range depending on the functional state of the neuron. A linear relationship was established between the time before appearance of the IPSP and the duration of the interspike interval of the slowly adapting neuron (SAN) and also between the firing rate of this and the inhibitory neurons during recurrent inhibition. Factors influencing the length of the interspike interval of the SAN on the appearance of an IPSP in it were investigated. It is postulated that summation of potentials evoked by spikes of the SAN and also of potentials evoked by spikes of that neuron, together with local processes evidently of endogenous nature takes place in the inhibitory neuron. IPSPs were recorded from two neurons resistant to strychnine and blocked by picrotoxin on the receptor neuron. The structural and functional organization of the individual elements in the chain of recurrent inhibition and inhibition evoked by stimulation of the abdominal ganglionic chain is discussed.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 5, No. 3, pp. 323–332, May–June, 1973.     

Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception

Nitric oxide (NO) modulates the dynamics of central olfactory networks and has been implicated in olfactory processing including learning. Land mollusks have a specialized olfactory lobe in the brain called the procerebral (PC) lobe. The PC lobe produces ongoing local field potential (LFP) oscillation, which is modulated by olfactory stimulation. We hypothesized that NO should be released in the PC lobe in response to olfactory stimulation, and to prove this, we applied an NO electrode to the PC lobe of the land slug Limax in an isolated tentacle-brain preparation. Olfactory stimulation applied to the olfactory epithelium transiently increased the NO concentration in the PC lobe, and this was blocked by the NO synthase inhibitor L-NAME at 3.7 mM. L-NAME at this concentration did not block the ongoing LFP oscillation, but did block the frequency increase during olfactory stimulation. Olfactory stimulation also enhanced spatial synchronicity of activity, and this response was also blocked by L-NAME. Single electrical stimulation of the superior tentacle nerve (STN) mimicked the effects of olfactory stimulation on LFP frequency and synchronicity, and both of these effects were blocked by L-NAME. L-NAME did not block synaptic transmission from the STN to the nonbursting (NB)-type PC lobe neurons, which presumably produce NO in an activity-dependent manner. Previous behavioral experiments have revealed impairment of olfactory discrimination after L-NAME injection. The recording conditions in the present work likely reproduce the in vivo brain state in those behavioral experiments. We speculate that the dynamical effects of NO released during olfactory perception underlie precise odor representation and memory formation in the brain, presumably through regulation of NB neuron activity.     

Modulation of two oscillatory networks in the peripheral olfactory system by γ‐aminobutyric acid,glutamate, and acetylcholine in the terrestrial slug Limax marginatus

The digit‐like extensions (the digits) of the tentacular ganglion of the terrestrial slug Limax marginatus are the cell body rich region in the primary olfactory system, and they contain primary olfactory neurons and projection neurons that send their axons to the olfactory center via the tentacular nerves. Two cell clusters (the cell masses) at the bases of the digits form the other cell body rich regions. Although the spontaneous slow oscillations and odor responses in the tentacular nerve have been studied, the origin of the oscillatory activity is unknown. In the present study, we examined the contribution of the neurons in the digits and cell masses to generation of the tentacular nerve oscillations by surgical removal from the whole tentacle preparations. Both structures contributed to the tentacular oscillations, and surgical isolation of the digits from the whole tentacle preparations still showed spontaneous oscillations. To analyze the dynamics of odor‐processing circuits in the digits and tentacular ganglia, we studied the effects of γ‐aminobutyric acid, glutamate, and acetylcholine on the circuit dynamics of the oscillatory network(s) in the peripheral olfactory system. Bath or local puff application of γ‐aminobutyric acid to the cell masses decreased the tentacular nerve oscillations, whereas the bath or local puff application of glutamate and acetylcholine to the digits increased the digits' oscillations. Our results suggest the existence of two intrinsic oscillatory circuits that respond differentially to endogenous neurotransmitters in the primary olfactory system of slugs. © 2004 Wiley Periodicals, Inc. J Neurobiol 59: 304–318, 2004     

Firing pattern and synchronization property analysis in a network model of the olfactory bulb

In the olfactory system, both the temporal spike structure and spatial distribution of neuronal activity are important for processing odor information. In this paper, a biophysically-detailed, spiking neuronal model is used to simulate the activity of olfactory bulb. It is shown that by varying some key parameters such as maximal conductances of Ks and Nap the spike train of single neuron can exhibit various firing patterns. Synchronization in coupled neurons is also investigated as the coupling strength varying in the situation of two neurons and network. It is illustrated that the coupled neurons can exhibit different types of pattern when the coupling strength varies. These results may be instructive to understand information transmission in olfactory system.     

Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks

Temporal precision in spike timing is important in cortical function, interactions, and plasticity. We found that, during periods of recurrent network activity (UP states), cortical pyramidal cells in vivo and in vitro receive strong barrages of both excitatory and inhibitory postsynaptic potentials, with the inhibitory potentials showing much higher power at all frequencies above approximately 10 Hz and more synchrony between nearby neurons. Fast-spiking inhibitory interneurons discharged strongly in relation to higher-frequency oscillations in the field potential in vivo and possess membrane, synaptic, and action potential properties that are advantageous for transmission of higher-frequency activity. Intracellular injection of synaptic conductances having the characteristics of the recorded EPSPs and IPSPs reveal that IPSPs are important in controlling the timing and probability of action potential generation in pyramidal cells. Our results support the hypothesis that inhibitory networks are largely responsible for the dissemination of higher-frequency activity in cortex.     

Postinhibitory unit response of crustacean stretch receptors after direct and recurrent inhibition

The postinhibitory response of a slowly adapting neuron was investigated in experiments on an isolated preparation of crustacean stretch receptor and abdominal nerve chain. The structural features of this preparation are such that this response can be regarded as the response of the postsynaptic membrane to synaptic inhibition and not the action of synaptic excitation. IPSPs arise in the slowly adapting neuron in response to stimulation of the abdominal nerve chain (direct inhibition) or to excitation of the neuron itself (recurrent inhibition). The postinhibitory response consists of the development of action potentials or an increase in their amplitude and frequency. The magnitude of the response is determined by the duration of the inhibition and the state of the neuron membrane. The postinhibitory response was strongest when IPSPs were superposed on cathodal depression. IPSPs and an intracellular hyperpolarizing current evoke similar postinhibitory responses. Repetitive excitation of an inhibitory neuron may result in the appearance of a regular spike discharge from a previously inactive neuron through the mechanism of the postinhibitory response. Activation of a chain of recurrent inhibition increases the duration of the postinhibitory response evoked by direct inhibition or by a hyperpolarizing current. The existence of a chain of recurrent inhibition prevents the cessation of firing by a neuron during increasing cathodal depression. A mechanism of postinhibitory rebound lies at the basis of this phenomenon.     

Interplay of Intrinsic and Synaptic Conductances in the Generation of High-Frequency Oscillations in Interneuronal Networks with Irregular Spiking

High-frequency oscillations (above 30 Hz) have been observed in sensory and higher-order brain areas, and are believed to constitute a general hallmark of functional neuronal activation. Fast inhibition in interneuronal networks has been suggested as a general mechanism for the generation of high-frequency oscillations. Certain classes of interneurons exhibit subthreshold oscillations, but the effect of this intrinsic neuronal property on the population rhythm is not completely understood. We study the influence of intrinsic damped subthreshold oscillations in the emergence of collective high-frequency oscillations, and elucidate the dynamical mechanisms that underlie this phenomenon. We simulate neuronal networks composed of either Integrate-and-Fire (IF) or Generalized Integrate-and-Fire (GIF) neurons. The IF model displays purely passive subthreshold dynamics, while the GIF model exhibits subthreshold damped oscillations. Individual neurons receive inhibitory synaptic currents mediated by spiking activity in their neighbors as well as noisy synaptic bombardment, and fire irregularly at a lower rate than population frequency. We identify three factors that affect the influence of single-neuron properties on synchronization mediated by inhibition: i) the firing rate response to the noisy background input, ii) the membrane potential distribution, and iii) the shape of Inhibitory Post-Synaptic Potentials (IPSPs). For hyperpolarizing inhibition, the GIF IPSP profile (factor iii)) exhibits post-inhibitory rebound, which induces a coherent spike-mediated depolarization across cells that greatly facilitates synchronous oscillations. This effect dominates the network dynamics, hence GIF networks display stronger oscillations than IF networks. However, the restorative current in the GIF neuron lowers firing rates and narrows the membrane potential distribution (factors i) and ii), respectively), which tend to decrease synchrony. If inhibition is shunting instead of hyperpolarizing, post-inhibitory rebound is not elicited and factors i) and ii) dominate, yielding lower synchrony in GIF networks than in IF networks.     

Synaptic dendritic activity modulates the single synaptic event

Synaptic transmission is the key system for the information transfer and elaboration among neurons. Nevertheless, a synapse is not a standing alone structure but it is a part of a population of synapses inputting the information from several neurons on a specific area of the dendritic tree of a single neuron. This population consists of excitatory and inhibitory synapses the inputs of which drive the postsynaptic membrane potential in the depolarizing (excitatory synapses) or depolarizing (inhibitory synapses) direction modulating in such a way the postsynaptic membrane potential. The postsynaptic response of a single synapse depends on several biophysical factors the most important of which is the value of the membrane potential at which the response occurs. The concurrence in a specific time window of inputs by several synapses located in a specific area of the dendritic tree can, consequently, modulate the membrane potential such to severely influence the single postsynaptic response. The degree of modulation operated by the synaptic population depends on the number of synapses active, on the relative proportion between excitatory and inbibitory synapses belonging to the population and on their specific mean firing frequencies. In the present paper we show results obtained by the simulation of the activity of a single Glutamatergic excitatory synapse under the influence of two different populations composed of the same proportion of excitatory and inhibitory synapses but having two different sizes (total number of synapses). The most relevant conclusion of the present simulations is that the information transferred by the single synapse is not and independent simple transition between a pre- and a postsynaptic neuron but is the result of the cooperation of all the synapses which concurrently try to transfer the information to the postsynaptic neuron in a given time window. This cooperativeness is mainly operated by a simple mechanism of modulation of the postsynaptic membrane potential which influences the amplitude of the different components forming the postsynaptic excitatory response.     

Comparison of identified mitral and tufted cells in freely breathing rats: II. Odor-evoked responses

Mitral and tufted cells are the 2 types of output neurons of the main olfactory bulb. They are located in distinct layers, have distinct projection patterns of their dendrites and axons, and likely have distinct relationships with the intrabulbar inhibitory circuits. They could thus be functionally distinct and process different aspects of olfactory information. To examine this possibility, we compared the odor-evoked responses of identified single units recorded in the mitral cell layer (MCL units), in the core of the external plexiform layer (not at the glomerular border tufted cells), or at the glomerular border of this layer (GB tufted cells) of the entire olfactory bulb. Differences between mitral and tufted cells were observed only when subtle aspects of the responses were explored, such as the firing rate per respiratory cycle or the distribution of firing activity along the respiratory cycle. By contrast, more clear differences were found when the 2 subtypes of tufted cells were examined separately. GB units were significantly more responsive, had significantly higher firing activity, and showed greater activity at the transition between inspiration and expiration. The projection-type tufted cells situated closer to the entrance of the olfactory bulb may thus form a distinct physiological class of output neurons and differ from mitral cells and other tufted cells in the manner of processing olfactory information.     

Morphology and physiology of multiglomerular olfactory projection neurons in the spiny lobster

Whole-cell patch-clamp recording was used to characterize olfactory projection neurons in an isolated brain preparation of the spiny lobster, Panulirus argus. Responses to electrical stimulation of the olfactory afferents were recorded from projection neuron somata using biocytin-filled electrodes. All projection neurons were multiglomerular, innervating up to 80% of all olfactory lobe glomeruli, but the innervation was heterogeneous. Most neurons densely innervated only 3–4 glomeruli; the remaining glomeruli in their dendritic arbor were sparsely innervated, thereby creating two distinct patterns of intraglomerular branching. Projection neurons responded to orthodromic stimulation with an initial depolarization and spiking followed by a 1–3 s hyperpolarization. The inhibitory phase of the response was lower in threshold and longer in latency than the excitatory phase, a response pattern also reported in olfactory projection neurons of insects and vertebrates. The somata of the projection neurons supported voltage-activated currents and TTX-sensitive action potentials, suggesting that the soma, although spatially separated from the axon and dendrites, may play a significant functional role in these cells. Dye coupling between some projection neurons correlated with the presence of multiple amplitude action potentials, suggesting that at least some projection neurons may be coupled via gap junctions.     

Interaction of penicillin and pentobarbital with inhibitory synaptic mechanisms in neocortex

In this study we characterized the responses of neocortical neurons to iontophoretically applied gamma-aminobutyric acid (GABA) and examined how these GABA responses as well as the inhibitory postsynaptic potentials (IPSPs) were affected by the presence of penicillin or pentobarbital. Intracellular recordings were obtained from slices of rat neocortex maintained in vitro; injection of the dye Lucifer yellow indicated that recordings were primarily from pyramidal neurons. Orthodromically evoked responses were always depolarizing at the cell's resting membrane potential. Such depolarizing responses could easily be reversed in polarity by depolarizing the cell 10-15 mV, suggesting that the response consisted partly of an IPSP. In some cases, depolarization unmasked a small, short-latency excitatory postsynaptic potential (EPSP). Responses to iontophoretically applied GABA were also depolarizing at rest. Biphasic hyperpolarizing-depolarizing responses were occasionally observed upon depolarization of the neuron. Bath application of penicillin (1.7-3.4 mM) decreased the amplitude of the IPSPs and increased their time to peak, an effect associated with the development of epileptiform activity. Penicillin also reduced the maximum response to iontophoretically applied GABA without affecting the dose required to obtain a half-maximal response, suggesting a noncompetitive antagonism. Pentobarbital (100-200 microM) prolonged the time course and increased the amplitude of the IPSPs while producing a leftward shift in the GABA charge-response relation. These results suggest that the convulsant penicillin and the anticonvulsant pentobarbital have opposing actions on GABAergic inhibition in the neocortex.     

The sox gene Dichaete is expressed in local interneurons and functions in development of the Drosophila adult olfactory circuit

In insects, the primary sites of integration for olfactory sensory input are the glomeruli in the antennal lobes. Here, axons of olfactory receptor neurons synapse with dendrites of the projection neurons that relay olfactory input to higher brain centers, such as the mushroom bodies and lateral horn. Interactions between olfactory receptor neurons and projection neurons are modulated by excitatory and inhibitory input from a group of local interneurons. While significant insight has been gleaned into the differentiation of olfactory receptor and projection neurons, much less is known about the development and function of the local interneurons. We have found that Dichaete, a conserved Sox HMG box gene, is strongly expressed in a cluster of LAAL cells located adjacent to each antennal lobe in the adult brain. Within these clusters, Dichaete protein expression is detected in both cholinergic and GABAergic local interneurons. In contrast, Dichaete expression is not detected in mature or developing projection neurons, or developing olfactory receptor neurons. Analysis of novel viable Dichaete mutant alleles revealed misrouting of specific projection neuron dendrites and axons, and alterations in glomeruli organization. These results suggest noncell autonomous functions of Dichaete in projection neuron differentiation as well as a potential role for Dichaete‐expressing local interneurons in development of the adult olfactory circuitry. © 2012 Wiley Periodicals, Inc. Develop Neurobiol, 2013     

Postsynaptic inhibition in the primordial hippocampus of the frog

Postsynaptic responses of neurons of the primordial hippocampus to electrical stimulation of brain structures belonging to the visual and olfactory afferent systems were investigated in frogs (Rana temporaria) immobilized with diplacin. * Short-latency (early) and long-latency (late) IPSPs evoked by both olfactory and visual afferent inputs, most probably activated by different conducting systems, are described. Impulses of different modalities can induce both similar and different IPSPs in a neuron. The conducting systems may have a common interneuron for the visual input and specific interneurons for the olfactory input. IPSPs evoked by visual impulses were similar in location to the early IPSP of the olfactory afferent input. Convergence of the systems of early and late inhibition on one neuron was frequently observed for the olfactory afferent input.M. V. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 5, No. 6, pp. 583–592, November–December, 1973.     

Inhibitory synchrony as a mechanism for attentional gain modulation

Recordings from area V4 of monkeys have revealed that when the focus of attention is on a visual stimulus within the receptive field of a cortical neuron, two distinct changes can occur: The firing rate of the neuron can change and there can be an increase in the coherence between spikes and the local field potential (LFP) in the gamma-frequency range (30-50 Hz). The hypothesis explored here is that these observed effects of attention could be a consequence of changes in the synchrony of local interneuron networks. We performed computer simulations of a Hodgkin-Huxley type neuron driven by a constant depolarizing current, I, representing visual stimulation and a modulatory inhibitory input representing the effects of attention via local interneuron networks. We observed that the neuron's firing rate and the coherence of its output spike train with the synaptic inputs was modulated by the degree of synchrony of the inhibitory inputs. When inhibitory synchrony increased, the coherence of spiking model neurons with the synaptic input increased, but the firing rate either increased or remained the same. The mean number of synchronous inhibitory inputs was a key determinant of the shape of the firing rate versus current (f-I) curves. For a large number of inhibitory inputs (approximately 50), the f-I curve saturated for large I and an increase in input synchrony resulted in a shift of sensitivity-the model neuron responded to weaker inputs I. For a small number (approximately 10), the f-I curves were non-saturating and an increase in input synchrony led to an increase in the gain of the response-the firing rate in response to the same input was multiplied by an approximately constant factor. The firing rate modulation with inhibitory synchrony was highest when the input network oscillated in the gamma frequency range. Thus, the observed changes in firing rate and coherence of neurons in the visual cortex could be controlled by top-down inputs that regulated the coherence in the activity of a local inhibitory network discharging at gamma frequencies.     

Neural control of olfaction and tentacle movements by serotonin and dopamine in terrestrial snail

We investigated the role of serotonin (5HT) and dopamine (DA) in the regulation of olfactory system function and odor-evoked tentacle movements in the snail Helix. Preparations of the posterior tentacle (including sensory pad, tentacular ganglion and olfactory nerve) or central ganglia with attached posterior tentacles were exposed to cineole odorant and the evoked responses were affected by prior application of 5HT or DA or their precursors 5-hydroxytryptophan (5HTP) and l-DOPA, respectively. 5HT applications decreased cineole-evoked responses recorded in the olfactory nerve and hyperpolarized the identified tentacle retractor muscle motoneuron MtC3, while DA applications led to the opposite changes. 5HTP and l-DOPA modified MtC3 activity comparable to 5HT and DA action. DA was also found to decrease the amplitude of spontaneous local field potential oscillations in the procerebrum, a central olfactory structure. In vivo studies demonstrated that injection of 5HTP in freely moving snails reduced the tentacle withdrawal response to aversive ethyl acetate odorant, whereas the injection of l-DOPA increased responses to “neutral” cineole and aversive ethyl acetate odorants. Our data suggest that 5HT and DA affect the peripheral (sensory epithelium and tentacular ganglion), the central (procerebrum), and the single motor neuron (withdrawal motoneuron MtC3) level of the snail’s nervous system.     

Thermal sensitivity of voltage-gated Na(+) channels and A-type K(+) channels contributes to somatosensory neuron excitability at cooling temperatures

J. Neurochem. (2012) 122, 1145-1154. ABSTRACT: Cooling temperatures may modify action potential firing properties to alter sensory modalities. Herein, we investigated how cooling temperatures modify action potential firing properties in two groups of rat dorsal root ganglion (DRG) neurons, tetrodotoxin-sensitive (TTXs) Na(+) channel-expressing neurons and tetrodotoxin-resistant (TTXr) Na(+) channel-expressing neurons. We found that multiple action potential firing in response to membrane depolarization was suppressed in TTXs neurons but maintained or facilitated in TTXr neurons at cooling temperatures. We showed that cooling temperatures strongly inhibited A-type K(+) currents (IA) and TTXs Na(+) channels but had fewer inhibitory effects on TTXr Na(+) channels and non-inactivating K(+) currents (IK). We demonstrated that the sensitivity of A-type K(+) channels and voltage-gated Na(+) channels to cooling temperatures and their interplay determine somatosensory neuron excitability at cooling temperatures. Our results provide a putative mechanism by which cooling temperatures modify different sensory modalities including pain.