scholarly journals Control of sensory ectopic spike initiation by descending modulatory projection neurons

2015 ◽  
Author(s):  
Carola Städele ◽  
Wolfgang Stein

Descending pathways are important modulators of motor networks and allow the dynamic adjustment of behaviors to changing internal and external conditions. Central pattern generating networks (CPG) have been particularly amenable to study the modulation of motor networks and demonstrated that virtually all levels of information processing are controlled by descending projections. CPGs receive sensory feedback and while it is known that sensory activity can be gated by central pathways, we here present for the first time that descending projection neurons modulate action potential initiation in sensory neurons. We used the fact that the anterior gastric receptor neuron (AGR), a single-cell bipolar muscle tendon organ in the crustacean stomatogastric nervous system, generates spontaneous ectopic action potentials in its axon. We found that axonal spike initiation is under direct neuromodulatory control by a pair of descending projection neurons. These IV (inferior ventricular) neurons descend from the brain and are known to control CPGs in the stomatogastric ganglion (STG). Activation of the IV neurons elicited a long-lasting decrease in AGR ectopic spike activity. This decrease was only observed when spikes were generated ectopically in the central portion of the axon, i.e. the modulation was specific to the site of spontaneous spike initiation. The decrease could be mimicked by focal application of the IV neuron co-transmitter histamine and IV neuron actions were diminished after blocking H2 receptors, indicating a direct descending modulation of the axonal spike initiation site. In contrast, the propagation dynamics of en-passant action potentials were not affected. Descending modulatory projection neurons therefore control axonal spike initiation in sensory neurons without affecting afferent spike propagation to increase the physiological activity repertoire of sensory pathways.

1978 ◽  
Vol 76 (1) ◽  
pp. 63-84 ◽  
Author(s):  
W. J. HEITLER ◽  
COREY S. GOODMAN

Recordings were made from the metathoracic dorsal unpaired median neurone to the extensor tibiae muscle (DUMETi) in the locust. This is a bifurcating neurone with axons exiting both sideS of the ganglion, whose soma can support a full action potential. Four different spike types were recorded in the soma, each of which we associate with a different region of the neurone. These were (1) a soma (S) spike of 70-90 mV, (2) a neurite (N) spike of 20-40 mV, occurring between the axon hillock and axon branch point, (3) and (4) axon (A) spikes of 8–15 mV, occurring distal to the branch point on the left and right axons. Each of these regions must therefore have its own spike initiation site. At spike frequencies greater than about 10 Hz at room temperature or 1-5 Hz at 32 °C (the preferred environmental temperature of the locust) the S-spike may fail, revealing A-spikes, or more rarely N-spikes. A-spikes usually consist of two more-or-less separate components, Al and Ar, which can be correlated with action potentials in the left and right axon branches by recording spikes extracellularly in the peripheral nerves on each side. Occasionally single component A-spikes occur when an action potential is initiated in only one axon, and fails to propagate across the branch point to the contralateral axon. Thus, action potentials may occur independently in the branches of this bifurcating neurone. After unilateral axotomy only S-spikes and N-spikes are recorded, indicating that action potentials no longer fail to propagate across the branch point. Anatomical asymmetries in the axon branches of DUMETi have been correlated with physiological asymmetries recorded in the soma of the same neurone.


Author(s):  
Eve Marder

The crustacean stomatogastric nervous system has become one of the premier preparations used for the study of the mechanisms underlying the generation of rhythmic motor patterns. The stomatogastric ganglion (STG) contains about 30 neurons, most of which are motor neurons that innervate more than 40 sets of striated muscles that move the animal’s stomach. Descending projection neurons from the two commissural ganglia (CoGs) and the single oesophageal ganglion (OG) are important for the generation of the motor patterns produced by the STG. Identified sensory neurons project either into the CoGs to activate descending modulatory neurons, or directly into the STG.


2000 ◽  
Vol 84 (5) ◽  
pp. 2204-2216 ◽  
Author(s):  
Marc L. Belleau ◽  
Richard A. Warren

We have studied the postnatal development of the physiological characteristics of nucleus accumbens (nAcb) neurons in slices from postnatal day 1 ( P1) to P49 rats using the whole cell patch-clamp technique. The majority of neurons (102/108) were physiologically identified as medium spiny (MS) projection neurons, and only these were subjected to detailed analysis. The remaining neurons displayed characteristics suggesting that they were not MS neurons. Around the time of birth and during the first postnatal weeks, the membrane and firing characteristics of MS neurons were quite different from those observed later. These characteristics changed rapidly during the first 3 postnatal weeks, at which point they began to resemble those found in adults. Both whole cell membrane resistance and membrane time constant decreased more than fourfold during the period studied. The resting membrane potential (RMP) also changed significantly from an average of −50 mV around birth to less than −80 mV by the end of the third postnatal week. During the first postnatal week, the current-voltage relationship of all encountered MS neurons was linear over a wide range of membrane potentials above and below RMP. Through the second postnatal week, the proportion of neurons displaying inward rectification in the hyperpolarized range increased steadily and after P15, all recorded MS neurons displayed significant inward rectification. At all ages, inward rectification was blocked by extracellular cesium and tetra-ethyl ammonium and was not changed by 4-aminopyridine; this shows that inward rectification was mediated by the same currents in young and mature MS neurons. MS neurons fired single and repetitive Na+/K+ action potentials as early as P1. Spike threshold and amplitude remained constant throughout development in contrast to spike duration, which decreased significantly over the same period. Depolarizing current pulses from rest showed that immature MS neurons fired action potentials more easily than their older counterparts. Taken together, the results from the present study suggest that young and adult nAcb MS neurons integrate excitatory synaptic inputs differently because of differences in their membrane and firing properties. These findings provide important insights into signal processing within nAcb during this critical period of development.


1995 ◽  
Vol 73 (5) ◽  
pp. 1793-1798 ◽  
Author(s):  
M. D. Womack ◽  
E. W. McCleskey

1. Using patch-clamp methods, we show that brief prepulses to very positive voltages increase (facilitate) the amplitude of current through Ca2+ channels during a subsequent test pulse in some, but not all, dorsal root ganglion (DRG) sensory neurons. The amplitude of this facilitated current generally increases when the Ca2+ channels are inhibited by activation of the mu-opioid receptor. 2. The facilitated current is blocked by omega-conotoxin GVIA, activates in the range of high-threshold Ca2+ channels, and inactivates at relatively negative holding voltages. Thus facilitated current passes through N-type Ca2+ channels, the same channels that are inhibited by opioids and control neurotransmitter release in sensory neurons. 3. Although maximal facilitation occurs only at unphysiologically high membrane potentials (above +100 mV), some facilitation is seen after prepulses to voltages reached during action potentials. After return to the holding potential, facilitation persists for hundreds of milliseconds, considerably longer than in other neurons. Brief trains of pulses designed to mimic action potentials caused small facilitation (19% of maximal) in a fraction (8 of 24) of opioid-inhibited neurons. 4. We conclude that 1) prepulses to extremely positive voltages can cause partial recovery of Ca2+ channels inhibited by opioids; and 2) small, but detectable, facilitation is also seen after physiological stimulation in some DRG neurons. Facilitation, largely considered a biophysical epiphenomenon because of the extreme voltages used to induce it, appears to be physiologically relevant during opioid inhibition of Ca2+ channels in DRG neurons.


2008 ◽  
Vol 294 (5) ◽  
pp. G1288-G1298 ◽  
Author(s):  
Walter E. B. Sipe ◽  
Stuart M. Brierley ◽  
Christopher M. Martin ◽  
Benjamin D. Phillis ◽  
Francisco Bautista Cruz ◽  
...  

Protease-activated receptor (PAR2) is expressed by nociceptive neurons and activated during inflammation by proteases from mast cells, the intestinal lumen, and the circulation. Agonists of PAR2 cause hyperexcitability of intestinal sensory neurons and hyperalgesia to distensive stimuli by unknown mechanisms. We evaluated the role of the transient receptor potential vanilloid 4 (TRPV4) in PAR2-induced mechanical hyperalgesia of the mouse colon. Colonic sensory neurons, identified by retrograde tracing, expressed immunoreactive TRPV4, PAR2, and calcitonin gene-related peptide and are thus implicated in nociception. To assess nociception, visceromotor responses (VMR) to colorectal distension (CRD) were measured by electromyography of abdominal muscles. In TRPV4+/+ mice, intraluminal PAR2 activating peptide (PAR2-AP) exacerbated VMR to graded CRD from 6–24 h, indicative of mechanical hyperalgesia. PAR2-induced hyperalgesia was not observed in TRPV4−/− mice. PAR2-AP evoked discharge of action potentials from colonic afferent neurons in TRPV4+/+ mice, but not from TRPV4−/− mice. The TRPV4 agonists 5′,6′-epoxyeicosatrienoic acid and 4α-phorbol 12,13-didecanoate stimulated discharge of action potentials in colonic afferent fibers and enhanced current responses recorded from retrogradely labeled colonic dorsal root ganglia neurons, confirming expression of functional TRPV4. PAR2-AP enhanced these responses, indicating sensitization of TRPV4. Thus TRPV4 is expressed by primary spinal afferent neurons innervating the colon. Activation of PAR2 increases currents in these neurons, evokes discharge of action potentials from colonic afferent fibers, and induces mechanical hyperalgesia. These responses require the presence of functional TRPV4. Therefore, TRPV4 is required for PAR2-induced mechanical hyperalgesia and excitation of colonic afferent neurons.


1994 ◽  
Vol 71 (4) ◽  
pp. 1422-1427 ◽  
Author(s):  
E. A. Seyfarth ◽  
A. S. French

1. We have developed an isolated mechanoreceptor-organ preparation in which the intact sensory structures are available for mechanical stimulation and electrical recording. The anterior lyriform slit sense organ on the patella of the spider, Cupiennius salei Keys., consists of seven or eight cuticular slits, each innervated by a pair of large bipolar sensory neurons. The neurons are fusiform, and the largest somata are < or = 120 microns long. The innervation of the organ was characterized by light microscopy of neurons backfilled with neuronal tracers. Intracellular recording was used to measure the passive and active electrical properties of the neurons, in several cases followed by identification with Lucifer yellow injection. Both neurons of each pair from one slit responded with action potentials to depolarization by a step current injection. Approximately half of the sensory neurons adapted very rapidly and generated only one or two action potentials in response to a sustained depolarizing step, while a second group produced a burst of action potentials that adapted to silence in approximately 1 s or less. Recordings from identified neuron pairs indicated that each pair consists of one rapidly adapting and one bursting neuron. Measurements of cell membrane impedances and time constants produced estimates of neuronal size that agreed with the morphological measurements. This new preparation offers the possibility of characterizing the mechanisms underlying transduction and adaptation in primary mechanosensory neurons.


1999 ◽  
Vol 81 (1) ◽  
pp. 334-344 ◽  
Author(s):  
Sergey Yagodin ◽  
Carlos Collin ◽  
Daniel L. Alkon ◽  
Norman F. Sheppard ◽  
David B. Sattelle

Yagodin, Sergey, Carlos Collin, Daniel L. Alkon, Norman F. Sheppard, Jr., and David B. Sattelle. Mapping membrane potential transients in crayfish ( Procambarus clarkii) optic lobe neuropils with voltage-sensitive dyes. J. Neurophysiol. 81: 334–344, 1999. Voltage-sensitive dyes NK 2761 and RH 155 were employed (in conjunction with a 12 × 12 photodiode array) to study membrane potential transients in optic lobe neuropils in the eye stalk of the crayfish Procambarus clarkii. By this means we investigated a pathway linking deutocerebral projection neurons, via hemiellipsoid body local interneurons, to an unidentified target (most likely neurons processing visual information) in the medulla terminalis. Rapid (10- to 20-ms duration), transient changes in absorption with the characteristics of action potentials were recorded from the optic nerve and the region occupied by deutocerebral projection neurons after stimulation of the olfactory globular tract in the optic nerve and were blocked by 1 μM tetrodotoxin. Action potentials appeared to propagate to the glomerular layer of the hemiellipsoid body where synaptic responses were recorded from a restricted region of the hemiellipsoid body occupied by dendrites of hemiellipsoid body neurons. Action potentials were also recorded from processes of hemiellipsoid body neurons located in the medulla terminalis. Synaptic responses in the hemiellipsoid body and medulla terminalis were eliminated by addition to the saline of 500 μM Cd2+ or 20 mM Co2+, whereas the action potential attributed to branches of deutocerebral projection neurons in the hemiellipsoid body remained unaffected. Action potentials of hemiellipsoid body neurons in the medulla terminalis evoked postsynaptic potentials (50- to 200-ms duration) with an unidentified target in the medulla terminalis. Transient absorption signals were not detected in either the internal or external medulla nor were they recorded from other parts of the optic lobes in response to electrical stimulation of axons of the deutocerebral projection neurons. Functional maps of optical activity, together with electrophysiological and pharmacological findings, suggest that γ-aminobutyric acid affects synaptic transmission in glomeruli of the hemiellipsoid body. Synapses of the olfactory pathway located in the medulla terminalis may act as a “filter,” modifying visual information processing during olfactory stimulation.


2019 ◽  
Vol 121 (3) ◽  
pp. 950-972 ◽  
Author(s):  
Dawn M. Blitz ◽  
Andrew E. Christie ◽  
Aaron P. Cook ◽  
Patsy S. Dickinson ◽  
Michael P. Nusbaum

Microcircuit modulation by peptides is well established, but the cellular/synaptic mechanisms whereby identified neurons with identified peptide transmitters modulate microcircuits remain unknown for most systems. Here, we describe the distribution of GYRKPPFNGSIFamide (Gly1-SIFamide) immunoreactivity (Gly1-SIFamide-IR) in the stomatogastric nervous system (STNS) of the crab Cancer borealis and the Gly1-SIFamide actions on the two feeding-related circuits in the stomatogastric ganglion (STG). Gly1-SIFamide-IR localized to somata in the paired commissural ganglia (CoGs), two axons in the nerves connecting each CoG with the STG, and the CoG and STG neuropil. We identified one Gly1-SIFamide-IR projection neuron innervating the STG as the previously identified modulatory commissural neuron 5 (MCN5). Brief (~10 s) MCN5 stimulation excites some pyloric circuit neurons. We now find that bath applying Gly1-SIFamide to the isolated STG also enhanced pyloric rhythm activity and activated an imperfectly coordinated gastric mill rhythm that included unusually prolonged bursts in two circuit neurons [inferior cardiac (IC), lateral posterior gastric (LPG)]. Furthermore, longer duration (>30 s) MCN5 stimulation activated a Gly1-SIFamide-like gastric mill rhythm, including prolonged IC and LPG bursting. The prolonged LPG bursting decreased the coincidence of its activity with neurons to which it is electrically coupled. We also identified local circuit feedback onto the MCN5 axon terminals, which may contribute to some distinctions between the responses to MCN5 stimulation and Gly1-SIFamide application. Thus, MCN5 adds to the few identified projection neurons that modulate a well-defined circuit at least partly via an identified neuropeptide transmitter and provides an opportunity to study peptide regulation of electrical coupled neurons in a functional context. NEW & NOTEWORTHY Limited insight exists regarding how identified peptidergic neurons modulate microcircuits. We show that the modulatory projection neuron modulatory commissural neuron 5 (MCN5) is peptidergic, containing Gly1-SIFamide. MCN5 and Gly1-SIFamide elicit similar output from two well-defined motor circuits. Their distinct actions may result partly from circuit feedback onto the MCN5 axon terminals. Their similar actions include eliciting divergent activity patterns in normally coactive, electrically coupled neurons, providing an opportunity to examine peptide modulation of electrically coupled neurons in a functional context.


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