Distance-dependent Scaling of Calcium Transients Evoked by Backpropagating Spikes and Synaptic Activity in Dendrites of Hippocampal Interneurons

Overview

Journal J Neurosci

Specialty Neurology

Date 2004 Jan 23

PMID 14736852

Citations 36

Authors

Balazs Rozsa

Tibor Zelles

E Sylvester Vizi

Balazs Lendvai

Affiliations

Soon will be listed here.

Abstract

Although interactions between backpropagating action potentials and synaptic stimulations have been extensively studied in pyramidal neurons, dendritic propagation and the summation of these signals in interneurons are not nearly as well known. In this study, two-photon imaging was used to explore the basic properties of dendritic calcium signaling in CA1 stratum radiatum interneurons. In contrast to hippocampal pyramidal neurons, the backpropagating action potential-evoked calcium transients in dendrites of interneurons underwent a distance-dependent increment. Although, in proximal dendrites, an increment could be attributed to a smaller dendrite diameter, distal dendrites did not show such dependence. Calcium responses in interneurons had a smaller amplitude, slower rise time, and decay than in pyramidal neurons. To explore the factors underlying the difference, we compared the calcium-binding capacity in interneurons and in pyramidal neurons. Our finding that endogenous calcium buffers had a higher level in interneurons may primarily explain the different kinetics and amplitudes of calcium transients. Synaptic stimulation-evoked calcium transients were also larger at distant dendritic locations. The spread of these signals was restricted to 12-13 microm long dendritic compartments. Supporting the reported lack of long-term potentiation in these interneurons, we found only sublinear or linear summations of calcium responses to coincident synaptic inputs and backpropagating spikes.

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References

Schiller J, Schiller Y, Clapham D . NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat Neurosci. 1999; 1(2):114-8. DOI: 10.1038/363. View

Svoboda K, Helmchen F, Denk W, Tank D . Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nat Neurosci. 1999; 2(1):65-73. DOI: 10.1038/4569. View

Linden D . The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron. 1999; 22(4):661-6. DOI: 10.1016/s0896-6273(00)80726-6. View

McBain C, Freund T, Mody I . Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity. Trends Neurosci. 1999; 22(5):228-35. DOI: 10.1016/s0166-2236(98)01347-2. View

Helmchen F, Svoboda K, Denk W, Tank D . In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat Neurosci. 1999; 2(11):989-96. DOI: 10.1038/14788. View

Gulyas A, Megias M, Emri Z, Freund T . Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J Neurosci. 1999; 19(22):10082-97. PMC: 6782984. View

Martina M, Vida I, Jonas P . Distal initiation and active propagation of action potentials in interneuron dendrites. Science. 2000; 287(5451):295-300. DOI: 10.1126/science.287.5451.295. View

Maravall M, Mainen Z, Sabatini B, Svoboda K . Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys J. 2000; 78(5):2655-67. PMC: 1300854. DOI: 10.1016/S0006-3495(00)76809-3. View

Pettit D, Augustine G . Distribution of functional glutamate and GABA receptors on hippocampal pyramidal cells and interneurons. J Neurophysiol. 2000; 84(1):28-38. DOI: 10.1152/jn.2000.84.1.28. View

10.

Magee J, Cook E . Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci. 2000; 3(9):895-903. DOI: 10.1038/78800. View

11.

Hausser M, Spruston N, Stuart G . Diversity and dynamics of dendritic signaling. Science. 2000; 290(5492):739-44. DOI: 10.1126/science.290.5492.739. View

12.

Stuart G, Hausser M . Dendritic coincidence detection of EPSPs and action potentials. Nat Neurosci. 2001; 4(1):63-71. DOI: 10.1038/82910. View

13.

Nimchinsky E, Oberlander A, Svoboda K . Abnormal development of dendritic spines in FMR1 knock-out mice. J Neurosci. 2001; 21(14):5139-46. PMC: 6762842. View

14.

Kaiser K, Zilberter Y, Sakmann B . Back-propagating action potentials mediate calcium signalling in dendrites of bitufted interneurons in layer 2/3 of rat somatosensory cortex. J Physiol. 2001; 535(Pt 1):17-31. PMC: 2278771. DOI: 10.1111/j.1469-7793.2001.t01-1-00017.x. View

15.

Zelles T, Franklin L, Koncz I, Lendvai B, Zsilla G . The nootropic drug vinpocetine inhibits veratridine-induced [Ca2+]i increase in rat hippocampal CA1 pyramidal cells. Neurochem Res. 2001; 26(8-9):1095-100. DOI: 10.1023/a:1012365408215. View

16.

Isomura Y, Fujiwara-Tsukamoto Y, Imanishi M, Nambu A, Takada M . Distance-dependent Ni(2+)-sensitivity of synaptic plasticity in apical dendrites of hippocampal CA1 pyramidal cells. J Neurophysiol. 2002; 87(2):1169-74. DOI: 10.1152/jn.00536.2001. View

17.

Holthoff K, Tsay D, Yuste R . Calcium dynamics of spines depend on their dendritic location. Neuron. 2002; 33(3):425-37. DOI: 10.1016/s0896-6273(02)00576-7. View

18.

Sabatini B, Oertner T, Svoboda K . The life cycle of Ca(2+) ions in dendritic spines. Neuron. 2002; 33(3):439-52. DOI: 10.1016/s0896-6273(02)00573-1. View

19.

Williams S, Stuart G . Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science. 2002; 295(5561):1907-10. DOI: 10.1126/science.1067903. View

20.

Xiong W, Chen W . Dynamic gating of spike propagation in the mitral cell lateral dendrites. Neuron. 2002; 34(1):115-26. DOI: 10.1016/s0896-6273(02)00628-1. View