Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica

1982 ◽  
Vol 48 (2) ◽  
pp. 431-438 ◽  
Author(s):  
J. H. Byrne
Keyword(s):  
Sensory Neuron ◽  
Motor Neurons ◽  
Action Potentials ◽  
Time Course ◽  
Complex Function ◽  
Synaptic Depression ◽  
Short Term ◽  
Withdrawal Reflex ◽  
Single Complex ◽  
Gradual Decay

1. Repeated stimulation of the siphon skin results in short-term habituation of the reflex contractions of the gill (38). The habituation, in turn, is correlated with a depression of the excitatory postsynaptic potentials (EPSPs) in motor neurons from mechanoreceptor sensory neurons (SN) (7, 16). The present study was undertaken to examine the parametric features of the synaptic depression and gain insights into the mechanisms underlying the reduced transmitter release. 2. Single sensory neuron action potentials were repeatedly elicited with depolarizing current pulses while the amplitude of the resultant EPSPs in the motor neuron was monitored. Synaptic depression varies as a complex function of interstimulus interval (ISI). At an ISI of 1 s, depression is rapid and reaches a plateau at 36% of control. In contrast, the depression at an ISI of 100 s is less pronounced, showing a gradual decay to 65% of control with the 10th EPSP. Surprisingly, there are no significant differences in time course or magnitude of depression across a broad range of intermediate ISIs (3, 10, and 30 s), although depression at these ISIs is intermediate between the 1 and 100 s ISIs. 3. There is also a complex relationship between spike interval and the depression of the second of two EPSPs. Thus, depression of the second of two EPSPs or depression of a train of EPSPs is not a monotonic function of spike interval. Indeed, the data suggest that there may be a slight underlying facilitatory process with short spike intervals. 4. The results also indicate that the recovery of synaptic depression following a train of 10 stimuli is not constant. Shorter spike intervals produce more rapid recovery. 5. These data are inconsistent with a classical depletion model (33) for synaptic depression and indicate that either a single complex function of time and ISI or multiple functions underlie synaptic depression and its recovery at the sensory neuron synapse.

Sensitization of the gill and siphon withdrawal reflex of Aplysia: multiple sites of change in the neuronal network

1993 ◽  
Vol 70 (3) ◽  
pp. 1210-1220 ◽  
Author(s):  
L. E. Trudeau ◽  
V. F. Castellucci
Keyword(s):  
Sensory Neuron ◽  
Sensory Neurons ◽  
Motor Neurons ◽  
Neuronal Network ◽  
Feedback Inhibition ◽  
Excitatory Input ◽  
Major Mechanism ◽  
Withdrawal Reflex ◽  
The Difference ◽  
Central Synapses

1. Recent studies have emphasized the major contribution of interneuronal transmission to the mediation and learning-associated modulation of the gill and siphon withdrawal (GSW) reflex of Aplysia. We wish to provide more direct support for the hypothesis that inhibitory junctions are crucial sites of plasticity. 2. In parallel experiments we investigated modulation at five major sites of synaptic transmission in the GSW network: 1) from sensory neurons to motor neurons, 2) from sensory neurons to excitatory interneurons (INTs+) 3) from INTs+ to motor neurons (MNs), 4) from inhibitory interneurons (INTs-) to INTs+, and 5) from INTs+ to INTs-. 3. While recording simultaneously from a single sensory neuron of the LE cluster, an INT+, and a MN, we found that both LE-MN and LE-INTs+ synapses were facilitated by the activation of modulator neurons by stimulation of the left pleuroabdominal connective (185 and 93%, respectively) as well as by serotonin (5-HT) (191 and 84%). Junctions of the second type were therefore less facilitated. The difference in the magnitude of facilitation at these two sites is an indication of a branch-specific, differential efficacy in the modulation of different central synapses made by a single neuron. 4. Although INT(+)-MN junctions have the capacity to display marked posttetanic potentiation, they are not significantly potentiated after connective stimulation. Sensitization of the GSW reflex is therefore not necessarily accompanied by a modification of transmission at these synapses. 5. Inhibitory transmission to INTs+ is significantly reduced by connective stimulation (36%) and by 5-HT (71%). This supports the hypothesis that a reduction of feedback inhibition into INTs+ is a major mechanism of reflex sensitization and may account for the increased evoked firing of INTs+ that is observed after connective stimulation. 6. The excitatory input to INTs- is selectively decreased by 5-HT (50%) and by the molluscan neuropeptide small cardioactive peptide B (38%). This latter effect, which could produce disinhibition of INTs+, may explain the previous observation that this peptide is able to potentiate the evoked input to MNs of the reflex at a concentration (1 microM) that fails to modify monosynaptic sensory-motor transmission. 7. These results indicate that transmission through a small neuronal network that mediates a withdrawal reflex in Aplysia may be modulated at multiple sites and by different mechanisms. These mechanisms include: 1) branch-specific facilitation of sensory neuron outputs and 2) inhibition of INT(-)-INT+ inhibitory postsynaptic potentials by endogenous modulatory neurons and by 5-HT.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Factors Influencing Short-term Synaptic Plasticity in the Avian Cochlear Nucleus Magnocellularis

2015 ◽  
Vol 9s2 ◽  
pp. JEN.S25472 ◽  
Author(s):  
Jason Tait Sanchez Quinones ◽  
Quinones Karla ◽  
Otto-Meyer Sebastian
Keyword(s):  
Synaptic Plasticity ◽  
Cochlear Nucleus ◽  
Time Course ◽  
Synaptic Depression ◽  
Auditory Brainstem ◽  
Short Term ◽  
Nucleus Magnocellularis ◽  
Developmental Shift ◽  
Acid Type ◽  
Synaptic Dynamics

Defined as reduced neural responses during high rates of activity, synaptic depression is a form of short-term plasticity important for the temporal filtering of sound. In the avian cochlear nucleus magnocellularis (NM), an auditory brainstem structure, mechanisms regulating short-term synaptic depression include pre-, post-, and extrasynaptic factors. Using varied paired-pulse stimulus intervals, we found that the time course of synaptic depression lasts up to four seconds at late-developing NM synapses. Synaptic depression was largely reliant on exogenous Ca2+-dependent probability of presynaptic neurotransmitter release, and to a lesser extent, on the desensitization of postsynaptic α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-type glutamate receptor (AMPA-R). Interestingly, although extrasynaptic glutamate clearance did not play a significant role in regulating synaptic depression, blocking glutamate clearance at early-developing synapses altered synaptic dynamics, changing responses from depression to facilitation. These results suggest a developmental shift in the relative reliance on pre-, post-, and extrasynaptic factors in regulating short-term synaptic plasticity in NM.

Regulation of Synaptic Depression Rates in the Cricket Cercal Sensory System

1998 ◽  
Vol 79 (3) ◽  
pp. 1277-1285 ◽  
Author(s):  
Andrew A. V. Hill ◽  
Ping Jin
Keyword(s):  
Sensory Neuron ◽  
Sensory Neurons ◽  
High Frequency ◽  
Sensory System ◽  
Synaptic Depression ◽  
High Frequency Stimulation ◽  
Excitatory Postsynaptic Potential ◽  
Short Term ◽  
Frequency Stimulation ◽  
Postsynaptic Target

Hill, Andrew A. V. and Ping Jin. Regulation of synaptic depression rates in the cricket cercal sensory system. J. Neurophysiol. 79: 1277–1285, 1998. To assess the roles of pre- and postsynaptic mechanisms in the regulation of depression, short-term synaptic depression was characterized at the synapses between sensory neurons and two interneurons in the cricket cercal sensory system. Changes in excitatory postsynaptic potential (EPSP) amplitude with repetitive stimulation at 5 and 20 Hz were quantified and fitted to the depletion model of transmitter release. The depression rates of different sensory neuron synapses on a single interneuron varied with the age of the sensory neurons such that old sensory neuron synapses depressed faster than young synapses. Although all synapses showed depression, short-term facilitation was selectively expressed only at sensory neuron synapses on one interneuron, the medial giant interneuron (MGI). These synapses showed concurrent facilitation and depression with high-frequency stimulation (100 Hz), whereas the synapses on another interneuron, 10-3, showed only depression at all stimulus frequencies. A previous study showed that the ability of a synapse to facilitate is correlated with the identity of the postsynaptic neuron. The present results indicate that depression and facilitation are regulated independently. Depression is regulated presynaptically in a manner related to sensory neuron age; whereas, facilitation is regulated by the postsynaptic target.

Mechanoafferent neurons innervating tail of Aplysia. II. Modulation by sensitizing stimulation

1983 ◽  
Vol 50 (6) ◽  
pp. 1543-1559 ◽  
Author(s):  
E. T. Walters ◽  
J. H. Byrne ◽  
T. J. Carew ◽  
E. R. Kandel
Keyword(s):  
Sensory Neuron ◽  
Sensory Neurons ◽  
Motor Neurons ◽  
Action Potentials ◽  
Input Resistance ◽  
Test Site ◽  
Response Characteristics ◽  
Multiple Trials ◽  
A Site ◽  
Aversive Classical Conditioning

The tail-withdrawal reflex of Aplysia can be sensitized by weak stimulation of a site outside the site used to test the reflex or by repeatedly stimulating the test site itself. The sensitization of tail-withdrawal responses is associated with enhanced activation of the tail motor neurons and heterosynaptic facilitation of the monosynaptic connections between the tail sensory neurons and tail motor neurons. This synaptic facilitation can occur under conditions in which neither posttetanic potentiation nor generalized changes in postsynaptic input resistance contribute to the facilitation. In addition to producing monosynaptic excitatory postsynaptic potentials (EPSPs), action potentials in tail sensory neurons often recruit longer latency polysynaptic input to the tail motor neurons during sensitization. Strong, noxious tail shock similar in intensity to that used previously for sensitization and aversive classical conditioning of other responses in Aplysia produces more heterosynaptic facilitation than does weak sensitizing stimulation. Heterosynaptic facilitation builds up progressively with multiple trials and lasts for hours. Very strong shocks to the tail can change the response characteristics of tail sensory neurons so that a prolonged, regenerative burst of spikes is elicited by a brief intracellular depolarizing pulse. This bursting response produced by sensitizing stimulation has not been described previously in Aplysia sensory neurons and can greatly amplify the synaptic input to tail motor neurons from the sensory neurons. In addition, strong shocks to the tail increase the duration and magnitude of individual sensory neuron action potentials. Sensitizing tail stimulation usually produces long-lasting depolarization of the tail motor neurons and often long-lasting hyperpolarization of the tail sensory neurons. The tail motor and sensory neurons show both increases and decreases of input resistance following sensitizing stimulation. However, the small, occasional increases in input resistance of the motor neuron are insufficient to explain the heterosynaptic facilitation produced by sensitizing stimulation. Serotonin (5-HT) application can mimic many of the effects of sensitizing tail shock, including facilitation of both tail withdrawal and the monosynaptic connections between tail sensory and motor neurons, hyperpolarizing and depolarizing responses in the tail sensory neurons, and an increase in the duration and magnitude of the sensory neuron action potential. In the nearly isolated sensory neuron soma, 5-HT usually produces a slow, decreased conductance depolarizing response, suggesting that the 5-HT-induced hyperpolarizing response see

Contribution of individual mechanoreceptor sensory neurons to defensive gill-withdrawal reflex in Aplysia

1978 ◽  
Vol 41 (2) ◽  
pp. 418-431 ◽  
Author(s):  
J. H. Byrne ◽  
V. F. Castellucci ◽  
E. R. Kandel
Keyword(s):  
Motor Neuron ◽  
Sensory Neuron ◽  
Sensory Neurons ◽  
Motor Neurons ◽  
Tactile Stimulation ◽  
Sensory Cell ◽  
Divalent Cations ◽  
Plastic Properties ◽  
Withdrawal Reflex ◽  
Stimulation Of

1. To evaluate the contribution which mechanoreceptor sensory neurons make to the defensive gill-withdrawal reflex we developed an isolated reflex preparation. We then reduced this isolated reflex to a microcircuit (consisting of a single sensory cell and single motor cell) so as to causally relate the contribution of individual cells to the expression and plastic properties of the behavior. 2. Mechanoreceptor neurons make significant contributions to the amplitude and duration of the complex PSP in the motor neurons. A single spike in a sensory neuron produces an EPSP in the motor neuron which accounts for 7-36% of the complex EPSP produced by weak tactile stimulation of the skin. 3. More than 50% of the synaptic input to the gill motor neurons appears to be monosynaptic. Perfusing the ganglion with solutions of high divalent cations reduced the motor neurons' complex PSP by only 40%. 4. The population response of the mechanoreceptors to a point stimulus can be simulated by repetitively firing a single sensory neuron. Firing a single sensory cell discharges the motor neuron and produces a gill contraction similar to that produced by a natural stimulus. 5. Mechanoreceptors make monosynaptic connections onto gill motor neurons which decrement with repeated stimulation paralleling the decrement of the complex PSP to punctate tactile stimulation of the skin. 6. The results indicate that the known neural elements may quantitatively account for most of the expression of the behavior and its short-term habituation.

Role of Calcium-Calmodulin–Dependent Protein Kinase II in Modulation of Sensorimotor Synapses in Aplysia

1997 ◽  
Vol 78 (1) ◽  
pp. 409-416 ◽  
Author(s):  
Keiko Nakanishi ◽  
Fan Zhang ◽  
Douglas A. Baxter ◽  
Arnold Eskin ◽  
John H. Byrne
Keyword(s):  
Protein Kinase ◽  
Sensory Neuron ◽  
Action Potentials ◽  
Short Term ◽  
Dependent Protein Kinase ◽  
Duration Of Action ◽  
Calcium Calmodulin Dependent ◽  
Protein Kinase Ii ◽  
Dependent Protein

Nakanishi, Keiko, Fan Zhang, Douglas A. Baxter, Arnold Eskin, and John H. Byrne. Role of calcium-calmodulin–dependent protein kinase II in modulation of sensorimotor synapses in Aplysia. J. Neurophysiol. 78: 409–416, 1997. The Ca2+-calmodulin–dependent protein kinase II (CaMKII) inhibitor, {1-[N,O - bis(5 - isoquinolinesulfonyl) - N - methyl - L - tyrosyl] - 4 - phenylpiper azine} (KN-62), was used to investigate the role of CaMKII in synaptic transmission and serotonin (5-HT)-induced facilitation in Aplysia. Application of KN-62 (10 μM) by itself increased the amplitude of excitatory postsynaptic potentials (EPSPs) at sensorimotor synapses in pleural-pedal ganglia. Moreover, in the presence of KN-62, 5-HT–induced short-term facilitation was attenuated. Application of KN-62 by itself slightly increased the duration of action potentials in isolated sensory neuron somata but did not block spike broadening produced by 5-HT. KN-62 had no effect on excitability of isolated sensory neuron somata nor did it block 5-HT–induced enhancement of excitability. These results indicate that the attenuation of short-term facilitation by KN- 62 is not due to modulation of the membrane currents contributing to 5-HT–induced spike broadening or enhancement of excitability. Rather, these data are consistent with the hypothesis that CaMKII contributes to the regulation of sensorimotor connections and that it has a role in spike-duration–independent processes contributing to short-term facilitation.

Receptive fields and properties of a new cluster of mechanoreceptor neurons innervating the mantle region and the branchial cavity of the marine mollusk Aplysia californica

1991 ◽  
Vol 156 (1) ◽  
pp. 315-334
Author(s):  
B. Dubuc ◽  
V. F. Castellucci
Keyword(s):  
Motor Neurons ◽  
Action Potentials ◽  
Aplysia Californica ◽  
Receptive Fields ◽  
Abdominal Ganglion ◽  
Sensory Cells ◽  
Sensory Threshold ◽  
Marine Mollusk ◽  
Withdrawal Reflex ◽  
Branchial Cavity

The rostral LE cluster (rLE) is a new set of mechanoreceptor neurons of the abdominal ganglion innervating the mantle area, the branchial cavity, the gill and the siphon of the marine mollusk Aplysia californica Cooper. We have compared the organization of rLE cell receptive fields with that of three other clusters of sensory neurons in the abdominal ganglion (LE, RE and RF) that we have reanalysed. There is extensive overlap of receptive fields from the four populations of sensory cells, and the most exposed areas of the mantle are the most densely innervated. The sensory threshold is similar for all groups. The action potentials of the LE, rLE and RE neurons are broadened by serotonin and the peptide SCPB and narrowed by dopamine and FMRFamide. The RF group does not show the same kind of sensitivity to these neuromodulators. The synaptic outputs of the LE and rLE neurons undergo similar synaptic depression and homosynaptic and heterosynaptic facilitation. We estimate that 100 mechanoreceptor neurons innervate the entire mantle and siphon skin, gill and branchial cavity of Aplysia. The degree of their convergence onto various interneurons and motor neurons mediating the gill- and siphon-withdrawal reflex and other reflexes is under investigation.

Short-Term Dynamics of Synaptic Transmission Within the Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex

2002 ◽  
Vol 87 (6) ◽  
pp. 2904-2914 ◽  
Author(s):  
Carl C. H. Petersen
Keyword(s):  
Synaptic Transmission ◽  
Dynamic Behavior ◽  
Neuronal Network ◽  
Action Potentials ◽  
Time Course ◽  
Barrel Cortex ◽  
Short Term ◽  
Short Term Plasticity ◽  
Layer 4 ◽  
Detection Of Objects

The short-term plasticity of synaptic transmission between excitatory neurons within a barrel of layer 4 rat somatosensory neocortex was investigated. Action potentials in presynaptic neurons at frequencies ranging from 1 to 100 Hz evoked depressing postsynaptic excitatory postsynaptic potentials (EPSPs). Recovery from synaptic depression followed an exponential time course with best-fit parameters that differed greatly between individual synaptic connections. The average maximal short-term depression was close to 0.5 with a recovery time constant of around 500 ms. Analysis of each individual sweep showed that there was a correlation between the amplitude of the response to the first and second action potentials such that large first EPSPs were followed by smaller than average second EPSPs and vice versa. Short-term depression between excitatory layer 4 neurons can thus be termed use dependent. A simple model describing use-dependent short-term plasticity was able to closely simulate the experimentally observed dynamic behavior of these synapses for regular spike trains. More complex irregular trains of 10 action potentials occurring within 500 ms were initially well described, but during the train errors increased. Thus for short periods of time the dynamic behavior of these synapses can be predicted accurately. In conjunction with data describing the connectivity, this forms a first step toward computational modeling of the excitatory neuronal network of layer 4 barrel cortex. Simulation of whisking-evoked activity suggests that short-term depression may provide a mechanism for enhancing the detection of objects within the whisker space.

Simulation of synaptic depression, posttetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia

1985 ◽  
Vol 53 (3) ◽  
pp. 652-669 ◽  
Author(s):  
K. J. Gingrich ◽  
J. H. Byrne
Keyword(s):  
Action Potential ◽  
Sensory Neuron ◽  
Sensory Neurons ◽  
Transmitter Release ◽  
Neurotransmitter Release ◽  
Synaptic Depression ◽  
Posttetanic Potentiation ◽  
Withdrawal Reflex ◽  
Classic Conditioning ◽  
Presynaptic Facilitation

The defensive gill-withdrawal reflex in Aplysia has proven to be an attractive system for analyzing the neural mechanisms underlying simple forms of learning such as habituation, sensitization, and classic conditioning. Previous studies have shown that habituation is associated with synaptic depression and sensitization with presynaptic facilitation of transmitter release from sensory neurons mediating the reflex. The synaptic depression, in turn, is associated with a decrease in Ca2+ currents in the sensory neurons, whereas presynaptic facilitation with increased Ca2+ currents produced indirectly by a decrease in a novel serotonergic sensitive K+ current. The present work represents an initial quantitative examination of the extent to which these mechanisms account for each of these types of synaptic plasticity. To address these issues a lumped parameter mathematical model of the sensory neuron release process was constructed. Major components of this model include Ca2+-channel inactivation, Ca2+-mediated neurotransmitter release and mobilization, and readily releasable and upstream feeding pools of neurotransmitter. In the model, release of neurotransmitter has a linear function of Ca2+ concentration and is not affected directly by residual Ca2+. The model not only simulates the data of synaptic depression and recovery from depression, but also qualitatively predicts other features of neurotransmitter release that it was not designed to fit. These include features of synaptic depression with high and low levels of transmitter release, posttetanic potentiation, a steep relationship between action potential duration and transmitter release, enhanced release produced by broadening the sensory neuron action potential (presynaptic facilitation), and dramatic synaptic depression with two closely spaced tetraethylammonium (TEA) spikes. The model cannot account fully for synaptic depression with empirically observed somatic Ca2+-current kinetics. Rather a large component of synaptic depression is due to reduction to the pools of releasable neurotransmitter (depletion). In the model when spike durations are greater than 15-20 ms, spike broadening produces little facilitation. However, when spike durations are more physiological, spike broadening leads to enhanced transmitter release.

Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections

1983 ◽  
Vol 50 (6) ◽  
pp. 1522-1542 ◽  
Author(s):  
E. T. Walters ◽  
J. H. Byrne ◽  
T. J. Carew ◽  
E. R. Kandel
Keyword(s):  
Electrical Stimulation ◽  
Receptive Field ◽  
Motor Neurons ◽  
Action Potentials ◽  
Receptive Fields ◽  
The Body ◽  
Tail Region ◽  
Withdrawal Reflex ◽  
Somatotopic Organization ◽  
Stimulation Of

Mechanical, chemical, or electrical stimulation of the tail elicits a short-latency (less than 1 s) tail-withdrawal reflex that is graded with the intensity of the stimulus. The tail-withdrawal reflex is not elicited by stimulation of parts of the body outside of the tail region. Mechanoafferent neurons innervating the tail are located in a small subcluster within a large, homogeneous group of medium-size (40-80 micron) cells on the ventrocaudal (VC) surface of each pleural ganglion. The tail sensory neurons within this large VC cluster are activated by tactile pressure or by electrical stimulation of discrete regions of the tail. They adapt slowly to maintained stimulation and sometimes respond to stimulus offset as well. Both mechanical and electrical stimuli produce responses that are graded with the intensity of the stimulus. Cells in the VC cluster appear to be primary mechanoreceptors because they have axons in peripheral nerves (including nerves innervating the tail), they exhibit action potentials lacking prepotentials in response to tactile stimulation, and these action potentials are still produced by cutaneous stimulation when peripheral and central chemical synaptic transmission is blocked. Stimulation of fields all over the body surface evokes synaptically mediated hyperpolarizing responses in individual mechanoafferent neurons that may represent afferent inhibition. Hyperpolarizing responses lasting many seconds can be produced by brief cutaneous stimuli. The mechanoafferent neurons innervating the tail region make strong monosynaptic connections to tail motor neurons in the ipsilateral pedal ganglion, and through these connections this subpopulation of the VC neurons appears to make a substantial contribution to the short-latency tail-withdrawal reflex. In addition, the combined excitatory receptive fields of these mechanoafferents match the excitatory receptive field of the tail-withdrawal reflex. Mechanoafferent neurons in the VC cluster that have receptive fields on other parts of the body (outside the excitatory receptive field of the tail-withdrawal reflex) have not been observed to make monosynaptic connections to the tail motor neurons. The neurons innervating the tail are reliably found in a discrete region within the larger VC cluster. In addition to this gross somatotopic organization, there is evidence of a finer level of somatotopic organization between the position of the excitatory receptive field on the tail and the position of the cell soma in the tail subcluster.(ABSTRACT TRUNCATED AT 400 WORDS)

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