impact of presynaptic voltage transients on postsynaptic ...via.i-networx.de/docs/nwg_2009.pdf ·...

1
Literature 1) Haag and Borst (2004) Neuronal mechanism underlying complex receptive field properties of motion-selective interneurons. Nat Neurosci 7:628-635 2) Beckers et. al. (2007) Synapses in the fly motion vision pathway: evidence for a broad range of signal amplitudes and dynamics. J Neurophysiol 97:2032-2041 3) Haag and Borst (2008): Electrical coupling of lobula plate tangential cells to a heterolateral motion-sensitive neuron in the fly. J Neurosci 28(53):14435–14442 To assess how the occurrence and timing of V1 spikes is affected by VS spikes we monitored V1 spiking activity when single VS spikes were elicited by brief current injections (H). V1 spikes were tightly coupled to the injected current pulses in time (I). On occurence of a VS spike a V1 spike fol- lowed with much higher probability than when the current pulse remained subthreshold, i.e. when it failed to elicit a VS spike (J). The larger a VS spike is, the higher is the probability that a V1 spike is triggered (K). Voltage clamping of one VS cell during rest (i.e. in the ab- sence of visual motion) left the postsynaptic spike rate unaffected. However, the in- terspike interval distribution of V1 spikes was affected. While in the non-clamped situation (L) many doublet V1 spikes (marked by the X) occurred, the occurence of doublet V1 spikes was significantly reduced when one VS cell was voltage-clamped (M, N). When a presynaptic VS cell is voltage clamped V1 spikes are accompanied by a brief hyperpolari- zing current transients in the clamped VS cell (C). Some V1 spikes (3.1%) are not accompanied by a detectable current transient (D-E). The amplitu- des of these transients are not uniform (F). Some VS2/3 cells showed a clear bimodal distribution of current transient amplitudes (G). The occurence of ‘failures’ (V1 spikes not accompanied by a current transient in VS), the different amplitudes of the current transients, and in particular the bimo- dal distribution, speak against the assumption that the observed current transients result mainly from electri- cal coupling between VS and V1. We therefore propo- se that due to electrical coupling among the VS cells the current transients are caused by the occurrence of spikes in neighboring VS cells. We conclude the spike rate of the postsynaptic V1-neuron to be controlled by both, graded voltage modulations and spikes of the presynapic VS cells. Whereas the graded presynaptic component re- gulates the postsynaptic spike rate to a large extent, the presynaptic spikes predominantly control the actual timing of postsynaptic spikes. Presynaptic spikes play a role for ensemble synchroniza- tion, as is evident from the decrease in the rate of postsynaptic spike doublets when one VS cell is prevented from spiking. Signal transmission from VS to V1 is largely mediated by chemical synap- ses, but an additional contribution from electrical coupling cannot be excluded and an eleclectrical coupling between VS1 and V1 has recently been shown 3 . Introduction Results Results Conclusions Ulrich Beckers, Martin Egelhaaf and Rafael Kurtz Department of Neurobiology, Bielefeld University, 33501 Bielefeld, Germany [email protected] 20 ms 50 ms 1 nA 50 ms D E 1 nA 0 20 40 60 80 100 >120 0 10 20 30 40 50 60 70 80 90 100 110 0 0.05 0.1 0.15 0.2 0.25 0 20 40 60 80 100 >120 0 10 20 30 40 50 60 70 80 90 100 110 vc mode bridged number number V1 spike doublet probability interspike interval [ms] interspike interval [ms] mode 200 ms 10 mV 200 ms 10 mV M L N Information transfer between synaptically coupled neurons can be mediated by spikes, by graded signals, or by combi- nation of both types of signals. We simultaneously recorded from identified visual motion sensitive cell pairs of the fly (A). The presynaptic VS cells convey both graded and spike si- gnals (VS membrane potential: blue traces) to their common purely spiking postsynaptic target cell V1 (V1 spikes indicated as red dashes). The VS cells are electrically coupled among one another 1 . Synaptic transmission of graded signals from VS to V1 is linear over a broad signal range 2 . Postsynaptic spikes were elicited by voltage clamp (C) or injecting brief current pulses (H) into one VS cell. In this study we analyzed the time course of the holding current (C-G) to monitor the input received by the presynaptic cell and the correlation of V1 spike activity to single VS spikes (H-K). The role of fast signals for postsynaptic synchronization was studied by functionally removing one VS cell from the input ensemble (L-N). Contribution to the 8 th NWG Göttingen Meeting 2009 Impact of presynaptic voltage transients on postsynaptic spike timing at a graded synapse in the fly motion vision system intracellular recording electrode in VS axon extracellular recording electrode in V1's output region registered spikes VS-V1 synapse null direction preferred direction resting potential VS cell retinotopic input region V1 VS1 VS2 VS3 VS4 A B C 10 mV 50ms 10 mV 100 ms 100 ms 1 nA 20 mV 200 ms 1 nA 0 -2 -3 0 60 120 180 0 -1 -2 -3 0 40 80 120 0 -1 -2 -3 0 5 10 15 0 -1 -2 -3 0 10 20 30 0 -1 -2 -3 0 15 30 45 F G all 0 mV 10 mV 30 mV 50 mV -1 current [nA] number number current [nA] #1 #2 #3 #4 #5 #6 #7 #8 Sum 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1 I probability cell 2nA 50ms 10mV H 114 246 25 195 209 631 185 695 140 380 78 342 109 391 59 3141 919 261 0 10 30 20 0 1 2 3 40 50 time [ms] V1 spike rate [relative units] J K 0 0.5 1 1.5 2 2.5 3 3.5 4 x 0 10 20 30 40 50 60 70 80 90 100 VS-V1 spike coupling rate [%] relative threshold [mV] n=21 n=10 n=11 n=11 n=7 n=6 n=3 n=7 n=21 n=6

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Page 1: Impact of presynaptic voltage transients on postsynaptic ...via.i-networx.de/docs/nwg_2009.pdf · spikes were elicited by voltage clamp (C) or injecting brief current pulses (H) into

Literature1) Haag and Borst (2004) Neuronal mechanism underlying complex receptive field properties of motion-selective interneurons. Nat Neurosci 7:628-635

2) Beckers et. al. (2007) Synapses in the fly motion vision pathway: evidence for a broad range of signal amplitudes and dynamics. J Neurophysiol 97:2032-2041

3) Haag and Borst (2008): Electrical coupling of lobula plate tangential cells to a heterolateral motion-sensitive neuron in the fly. J Neurosci 28(53):14435–14442

To assess how the occurrence and timing of V1 spikes is affected by VS spikes we monitored V1

spiking activity when single VS spikes were elicited by brief current injections (H). V1 spikes were

tightly coupled to the injected current pulses in time (I). On occurence of a VS spike a V1 spike fol-

lowed with much higher probability than when the current pulse remained subthreshold, i.e. when it

failed to elicit a VS spike (J). The larger a VS spike is, the higher is the probability that a V1 spike is

triggered (K).

Voltage clamping of one VS

cell during rest (i.e. in the ab-

sence of visual motion) left

the postsynaptic spike rate

unaffected. However, the in-

terspike interval distribution of V1 spikes was affected. While in the non-clamped situation (L) many

doublet V1 spikes (marked by the X) occurred, the occurence of doublet V1 spikes was significantly

reduced when one VS cell was voltage-clamped (M, N).

When a presynaptic VS cell is voltage clamped V1 spikes are accompanied by a brief hyperpolari-

zing current transients in the clamped VS cell (C). Some V1 spikes (3.1%) are not accompanied by

a detectable current transient (D-E). The amplitu-

des of these transients are not uniform (F). Some

VS2/3 cells showed a clear bimodal distribution of

current transient amplitudes (G).

The occurence of ‘failures’ (V1 spikes not accompanied

by a current transient in VS), the different amplitudes

of the current transients, and in particular the bimo-

dal distribution, speak against the assumption that the

observed current transients result mainly from electri-

cal coupling between VS and V1. We therefore propo-

se that due to electrical coupling among the VS cells

the current transients are caused by the occurrence

of spikes in neighboring VS cells.

We conclude the spike rate of the postsynaptic V1-neuron to be controlled by both, graded voltage

modulations and spikes of the presynapic VS cells. Whereas the graded presynaptic component re-

gulates the postsynaptic spike rate to a large extent, the presynaptic spikes predominantly control

the actual timing of postsynaptic spikes. Presynaptic spikes play a role for ensemble synchroniza-

tion, as is evident from the decrease in the rate of postsynaptic spike doublets when one VS cell is

prevented from spiking. Signal transmission from VS to V1 is largely mediated by chemical synap-

ses, but an additional contribution from electrical coupling cannot be excluded and an eleclectrical

coupling between VS1 and V1 has recently been shown3.

Introduction Results

Results

Conclusions

Ulrich Beckers, Martin Egelhaaf and Rafael KurtzDepartment of Neurobiology, Bielefeld University, 33501 Bielefeld, [email protected]

20 ms50 ms

1 nA

50 ms

D

E

1 nA

0 20 40 60 80 100 >1200

10

20

30

40

50

60

70

80

90

100

110

0

0.05

0.1

0.15

0.2

0.25

0 20 40 60 80 100 >1200

10

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90

100

110

vcmode

bridged

num

ber

num

ber

V1 s

pike

dou

blet

pro

babi

lity

interspike interval [ms] interspike interval [ms] mode

200 ms

10 mV

200 ms

10 mV

ML N

Information transfer between synaptically coupled neurons

can be mediated by spikes, by graded signals, or by combi-

nation of both types of signals. We simultaneously recorded

from identified visual motion sensitive cell pairs of the fly (A).

The presynaptic VS cells convey both graded and spike si-

gnals (VS membrane potential: blue traces) to their common

purely spiking postsynaptic target cell V1 (V1 spikes indicated

as red dashes). The VS cells are electrically coupled among

one another1. Synaptic transmission of graded signals from

VS to V1 is linear over a broad signal range2. Postsynaptic

spikes were elicited by voltage clamp (C) or injecting brief

current pulses (H) into one VS cell. In this study we analyzed

the time course of the holding current (C-G) to monitor the input received by the presynaptic cell and

the correlation of V1 spike activity to single VS spikes (H-K). The role of fast signals for postsynaptic

synchronization was studied by functionally removing one VS cell from the input ensemble (L-N).

Contribution to the 8th NWG Göttingen Meeting 2009

Impact of presynaptic voltage transients on postsynaptic spike

timing at a graded synapse in the fly motion vision system

intracellular recording electrode in VS axon

extracellularrecording electrodein V1's output region

registeredspikes

VS-V1 synapse

null direction preferred direction

resting potential

VS cell retinotopic input region

V1

VS1VS2VS3VS4

A

B

C

10 mV

50ms

10 mV

100 ms

100 ms

1 nA

20 mV200 ms

1 nA

0 -2 -30

60

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180

0 -1 -2 -30

40

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120

0 -1 -2 -30

5

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0 -1 -2 -30

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45

F

Gall 0 mV 10 mV

30 mV 50 mV

-1current [nA]

num

ber

num

ber

current [nA]

#1 #2 #3 #4 #5 #6 #7 #8 Sum0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1I

prob

abili

ty

cell

2nA

50ms

10mV

H

114

246

25

195

209

631

185

695

140

380

78

342

109

391

59

3141

919

261

0 10 30200

1

2

3

40 50time [ms]

V1

spik

e ra

te [r

elat

ive

units

]

J K

0 0.5 1 1.5 2 2.5 3 3.5 4 x0102030405060708090

100

VS

-V1

spik

e co

uplin

g ra

te [%

]

relative threshold [mV]

n=21

n=10n=11

n=11

n=7

n=6

n=3

n=7

n=21

n=6