Direction selectivity in a model of the starburst amacrine cell

被引:57
作者
Tukker, JJ
Taylor, WR
Smith, RG
机构
[1] Univ Penn, Dept Neurosci, Philadelphia, PA 19104 USA
[2] Oregon Hlth & Sci Univ, Inst Neurol Sci, Beaverton, OR USA
关键词
direction selectivity; Starburst amacrine; morphology; calcium channels; Modeling;
D O I
10.1017/S0952523804214109
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
The starburst amacrine cell (SBAC), found in all mammalian retinas, is thought to provide the directional inhibitory input recorded in On-Off direction-selective ganglion cells (DSGCs). While voltage recordings from the somas of SBACs have not shown robust direction selectivity (DS), the dendritic tips of these cells display direction-selective calcium signals, even when gamma-aminobutyric acid (GABA(a,c)) channels are blocked, implying that inhibition is not necessary to generate DS. This suggested that the distinctive morphology of the SBAC could generate a DS signal at the dendritic tips, where most of its synaptic output is located. To explore this possibility, we constructed a compartmental model incorporating realistic morphological structure, passive membrane properties, and excitatory inputs. We found robust DS at the dendritic tips but not at the soma. Two-spot apparent motion and annulus radial motion produced weak DS, but thin bars produced robust DS. For these stimuli, DS was caused by the interaction of a local synaptic input signal with a temporally delayed "global" signal, that is, an excitatory postsynaptic potential (EPSP) that spread from the activated inputs into the soma and throughout the dendritic tree. In the preferred direction the signals in the dendritic tips coincided, allowing summation, whereas in the null direction the local signal preceded the global signal, preventing summation. Sine-wave grating stimuli produced the greatest amount of DS, especially at high velocities and low spatial frequencies. The sine-wave DS responses could be accounted for by a simple mathematical model, which summed phase-shifted signals from soma and dendritic tip. By testing different artificial morphologies, we discovered DS was relatively independent of the morphological details, but depended on having a sufficient number of inputs at the distal tips and a limited electrotonic isolation. Adding voltage-gated calcium channels to the model showed that their threshold effect can amplify DS in the intracellular calcium signal.
引用
收藏
页码:611 / 625
页数:15
相关论文
共 55 条
[11]   Directionally selective calcium signals in dendrites of starburst amacrine cells [J].
Euler, T ;
Detwiler, PB ;
Denk, W .
NATURE, 2002, 418 (6900) :845-852
[12]   A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells [J].
Famiglietti, EV .
VISUAL NEUROSCIENCE, 2002, 19 (02) :145-162
[14]   SYNAPTIC ORGANIZATION OF STARBURST AMACRINE CELLS IN RABBIT RETINA - ANALYSIS OF SERIAL THIN-SECTIONS BY ELECTRON-MICROSCOPY AND GRAPHIC RECONSTRUCTION [J].
FAMIGLIETTI, EV .
JOURNAL OF COMPARATIVE NEUROLOGY, 1991, 309 (01) :40-70
[15]  
FREED MA, 1988, J NEUROSCI, V8, P2303
[16]   Mechanisms and circuitry underlying directional selectivity in the retina [J].
Fried, SI ;
Münch, TA ;
Werblin, FS .
NATURE, 2002, 420 (6914) :411-414
[17]   Cation-chloride cotransporters mediate neural computation in the retina [J].
Gavrikov, KE ;
Dmitriev, AV ;
Keyser, KT ;
Mangel, SC .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2003, 100 (26) :16047-16052
[18]  
Hassenstein B., 1956, Proc. 1st Int. Conf. Cybern, P797
[19]   Retinal direction selectivity after targeted laser ablation of starburst amacrine cells [J].
He, SG ;
Masland, RH .
NATURE, 1997, 389 (6649) :378-382
[20]   EFFECTS OF CA2+ CHANNEL BLOCKERS ON DIRECTIONAL SELECTIVITY OF RABBIT RETINAL GANGLION-CELLS [J].
JENSEN, RJ .
JOURNAL OF NEUROPHYSIOLOGY, 1995, 74 (01) :12-23