Presynaptic effects of biogenic amines modulating synaptic transmission between identified sensory neurons and giant interneurons in the first instar cockroach

2001 ◽  
Vol 187 (8) ◽  
pp. 633-645 ◽  
Author(s):  
Evan Hill ◽  
Jonathan Blagburn
1996 ◽  
Vol 76 (6) ◽  
pp. 4031-4039 ◽  
Author(s):  
D. Parker ◽  
S. Grillner

1. Tachykinin-like immunoreactivity is found in the dorsal roots, dorsal horn, and dorsal column of the lamprey. The effect of tachykinins on sensory processing was examined by recording intracellularly from primary sensory dorsal cells and second-order spinobulbar giant interneurons. Modulation of synaptic transmission was examined by making paired recordings from dorsal cells and giant interneurons, or by eliciting compound depolarizations in the giant interneurons by stimulating the dorsal root or dorsal column. 2. Bath application of tachykinins depolarized the dorsal cells. This effect was mimicked by stimulation of the dorsal root, suggesting that dorsal root afferents may be a source of endogenous tachykinin input to the spinal cord. The depolarization was reduced by removal of sodium or calcium from the Ringer, or when potassium conductances were blocked, and was not associated with a measurable change in input resistance. Dorsal root stimulation also caused a depolarization in the dorsal cells, and this effect and that of bath-applied substance P, was blocked by the tachykinin antagonist spantide. 3. The tachykinin substance P could reduce inward and outward rectification in the dorsal cells, the effect on outward rectification only being seen when potassium conductances were blocked by tetraethylammonium (TEA). 4. Substance P increased the excitability of the dorsal cells and giant interneurons, shown by the increased spiking in response to depolarizing current pulses. The increased excitability was blocked by the tachykinin antagonist spantide. 5. Substance P modulated the dorsal cell action potential, by increasing the spike duration and reducing the amplitude of the afterhyperpolarization. The spike amplitude was not consistently affected. 6. Stimulation of the dorsal column resulted in either depolarizing or hyperpolarizing potentials in the giant interneurons. The amplitude of the depolarization was increased by substance P, whereas the amplitude of the hyperpolarization was reduced. These effects occurred independently of a measurable change in postsynaptic input resistance, suggesting that the modulation occurred presynaptically. Paired recordings from dorsal cells and giant interneurons failed to reveal an effect of substance P on dorsal cell-evoked excitatory postsynaptic potentials (EPSPs), suggesting that the potentiation of the dorsal column-evoked depolarization was due to an effect on other axons in the dorsal column. Dorsal root-evoked potentials could also be increased in the presence of substance P, although this effect was less consistent than the effect on dorsal column stimulation. 7. These results suggest that tachykinins modulate sensory input to the lamprey spinal cord by increasing the excitability of primary afferents and second-order giant interneurons, and also by modulating synaptic transmission. Tachykinins may result in potentiation of local spinal reflexes and also modulation of descending reticulospinal inputs to the spinal locomotor network as a result of potentiation of spinobulbar inputs.


1996 ◽  
Vol 75 (2) ◽  
pp. 855-866 ◽  
Author(s):  
L. L. Stark ◽  
A. R. Mercer ◽  
N. J. Emptage ◽  
T. J. Carew

1. Modulation of mechanoafferent sensory neurons (SNs) by the neutrotransmitter serotonin (5HT) plays a significant role in behavioral sensitization of several withdrawal reflexes in Aplysia. The modulatory effects of 5HT on these SNs include increased excitability, increased input resistance, action potential broadening, and increased synaptic transmission. Based on a previously described dissociation of some of these modulatory effects, revealed with the 5HT-receptor antagonist, cyproheptadine, we investigated whether a similar dissociation could be found by systematically varying the concentration of the endogenous agonist, 5HT. 2. We first applied a range of 5HT concentrations to isolated pleural/pedal ganglia (containing tail SNs and tail motor neurons, respectively), and measured the magnitude of 5HT-induced modulation of spike broadening and increased excitability. The resulting dose-response curve showed that both forms of modulation increase monotonically as a function of 5HT concentration, but that excitability has a lower threshold for modulation by 5HT than does spike duration. 3. We further characterized the modulatory effects of 5HT on Aplysia SNs by comparing the time course of onset of modulation by 5HT and the time course of recovery after washout. Independent of 5HT concentration, modulation of excitability increases rapidly in the presence of 5HT and recovers rapidly (< 3 min) after washout. Similarly, input resistance increases and recovers rapidly, mirroring the profile of increased excitability. However, modulation of spike duration exhibits two profiles, dependent on 5HT concentration. Low concentrations of 5HT (0.5 and 1 microM) induce a rapid-onset and transient-recovery form of spike broadening, which resembles the kinetics of increased excitability and increased input resistance. Higher concentrations of 5HT (2.5 and 5 microM) induce a more slowly developing and prolonged-recovery form of spike broadening (> 9 min). At these higher concentrations, the recovery profile for prolonged spike broadening is significantly different from those observed for both increased excitability and increased input resistance. 4. We next compared the relationship between spike broadening and short-term synaptic facilitation. We found that significant facilitation of synaptic transmission requires a high 5HT concentration, which is comparable with that required to induce prolonged spike broadening. Similarly, the recovery profiles for spike broadening and synaptic facilitation are strikingly similar, recovering in parallel. 5. Our experiments show that the modulatory effects of 5HT in the tail SNs can be dissociated both by their sensitivity to different concentrations of 5HT and by their kinetics of serotonergic modulation. Based on these results, together with extensive evidence from other laboratories, we propose that the short-term modulatory effects of 5HT fall into two distinct functional classes. The first class, which includes excitability, input resistance, and transient spike broadening, has a low threshold for 5HT modulation and recovers rapidly. The second class, which includes prolonged spike broadening and short-term synaptic facilitation, has a higher threshold for modulation and recovers more slowly. It now will be of interest to determine the functional contribution of each of these classes to different aspects of sensitization.


1997 ◽  
Vol 17 (5) ◽  
pp. 1786-1794 ◽  
Author(s):  
Abdeljabbar El Manira ◽  
Weiqi Zhang ◽  
Erik Svensson ◽  
Nathalie Bussières

2007 ◽  
Vol 25 (1) ◽  
pp. 159-167 ◽  
Author(s):  
Rossana Scuri ◽  
Paola Lombardo ◽  
Enrico Cataldo ◽  
Chiara Ristori ◽  
Marcello Brunelli

1997 ◽  
Vol 33 (4) ◽  
pp. 439-458 ◽  
Author(s):  
Michael Stern ◽  
Vernita L. Ediger ◽  
Charles R. Gibbon ◽  
Jonathan M. Blagburn ◽  
Jonathan P. Bacon

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