Direction selectivity in a model of the starburst amacrine cell

2004 ◽  
Vol 21 (4) ◽  
pp. 611-625 ◽  
Author(s):  
JOHN J. TUKKER ◽  
W. ROWLAND TAYLOR ◽  
ROBERT G. SMITH
Keyword(s):  
Amacrine Cell ◽  
Dendritic Tree ◽  
Sine Wave ◽  
Direction Selectivity ◽  
Membrane Properties ◽  
Calcium Signal ◽  
Inhibitory Input ◽  
Excitatory Postsynaptic Potential ◽  
Global Signal ◽  
Starburst Amacrine Cell

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 γ-aminobutyric acid (GABAa,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.

scholarly journals Origins of direction selectivity in the primate retina

2021 ◽  
Author(s):  
Yeon Jin Kim ◽  
Beth Peterson ◽  
Joanna Crook ◽  
Hannah Joo ◽  
Jiajia Wu ◽  
...  
Keyword(s):  
Neural Coding ◽  
Amacrine Cell ◽  
Cell Types ◽  
Macaque Monkey ◽  
Direction Selectivity ◽  
Bipolar Cells ◽  
Motion Processing ◽  
Motion Direction ◽  
Motion Sensitivity ◽  
Starburst Amacrine Cell

Abstract From mouse to primate, there is a striking discontinuity in our current understanding of the neural coding of motion direction. In non-primate mammals, directionally selective cell types and circuits are a signature feature of the retina, situated at the earliest stage of the visual process1,2. In primates, by contrast, direction selectivity is a hallmark of motion processing areas in visual cortex3,4, but has not been found in the retina, despite significant effort5,6. Here we combined functional recordings of light-evoked responses and connectomic reconstruction to identify diverse direction-selective cell types in the macaque monkey retina with distinctive physiological properties and synaptic motifs. This circuitry includes an ON-OFF ganglion cell type, a spiking, ON-OFF poly-axonal amacrine cell and the starburst amacrine cell, all of which show direction selectivity. Moreover, we found unexpectedly that macaque starburst cells possess a strong, non-GABAergic, antagonistic surround mediated by input from excitatory bipolar cells that is critical for the generation of radial motion sensitivity in these cells. Our findings open a new door to investigation of a novel circuitry that computes motion direction in the primate visual system.

Receptive-field properties of displaced starburst amacrine cells change following axotomy-induced degeneration of ganglion cells

1995 ◽  
Vol 12 (1) ◽  
pp. 177-184 ◽  
Author(s):  
Ralph J. Jensen
Keyword(s):  
Receptive Field ◽  
Amacrine Cell ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Membrane Properties ◽  
Optic Disk ◽  
Receptive Field Properties ◽  
Tungsten Microelectrode ◽  
Starburst Amacrine Cells ◽  
Starburst Amacrine Cell

AbstractStarburst amacrine cells in the rabbit retina were labeled following an intraocular injection of the fluorescent dye, 4, 6, diamidino-2-phenylindole (DAPI). From each eye a strip of retina was removed, mounted on a platform beneath an epifluorescence microscope, and superfused with a physiological solution. The tip of a tungsten microelectrode (for extracellular recording) was visually positioned near the cell body of a DAPI-labeled starburst amacrine cell that was located in the ganglion cell layer. Light-evoked responses from the displaced starburst amacrine cells were studied in normal retinas and in retinas that had received a small electrolytic lesion near the optic disk 5–9 months beforehand. In normal retinas, a small spot of light centered over the receptive field of a displaced starburst amacrine cell in nearly all cases evoked a brief burst of spikes only at light onset. When stimulated with a large spot or an annulus of light, many cells gave a small burst of spikes at light offset. In lesioned retinas, the light responses of displaced starburst amacrine cells were recorded in areas of the retina where ganglion cells had degenerated. All cells responded with a large burst of spikes at the onset and offset of a small, centered spot of light. Large spots and annuli of light also evoked robust ON/OFF responses from these cells. The results from this study show that the receptive-field properties of displaced starburst amacrine cells change following axotomy-induced degeneration of ganglion cells. This finding indicates that changes in either synaptic transmission or the membrane properties of neurons occur in the retina following degeneration of ganglion cells.

scholarly journals Functional and structural features of L2/3 pyramidal cells continuously covary with pial depth in mouse visual cortex

2021 ◽  
Author(s):  
Simon Weiler ◽  
Drago Guggiana Nilo ◽  
Tobias Bonhoeffer ◽  
Mark H&uumlbener ◽  
Tobias Rose ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Dendritic Tree ◽  
Pyramidal Cells ◽  
Structural Features ◽  
Direction Selectivity ◽  
Dendritic Morphology ◽  
Systematic Change ◽  
Inhibitory Input ◽  
Electrophysiological Properties

Pyramidal cells of neocortical layer 2/3 (L2/3 PyrCs) integrate signals from numerous brain areas and project throughout the neocortex. Within L2/3, PyrCs show functional and structural specializations depending on their pial depth, indicating participation in different functional microcircuits. However, it is unknown whether these depth-dependent differences result from separable L2/3 PyrC subtypes or whether functional and structural features represent a continuum while correlating with pial depth. Here, we assessed the stimulus selectivity, electrophysiological properties, dendritic morphology, and excitatory and inhibitory synaptic connectivity across the depth of L2/3 in the binocular visual cortex (bV1) of female mice. We find that the structure of the apical but not the basal dendritic tree varies with pial depth, which is accompanied by differences in passive but not active electrophysiological properties. PyrCs in lower L2/3 receive increased excitatory and inhibitory input from L4, while upper L2/3 PyrCs receive a larger proportion of intralaminar input. Complementary in vivo calcium imaging revealed a systematic change in visual responsiveness, with deeper L2/3 PyrCs showing more robust responses than superficial PyrCs. Furthermore, deeper L2/3 PyrCs are more strongly driven by contralateral than ipsilateral eye stimulation. In contrast, orientation- and direction-selectivity of L2/3 PyrCs are not dependent on pial depth. Importantly, the transitions of the various properties are gradual, and cluster analysis does not support the classification of L2/3 PyrCs into discrete subtypes. These results show that L2/3 PyrCs' multiple functional and structural properties systematically correlate with their depth within L2/3, forming a continuum rather than representing discrete subtypes.

scholarly journals Author response: Retinal direction selectivity in the absence of asymmetric starburst amacrine cell responses

2019 ◽  
Author(s):  
Laura Hanson ◽  
Santhosh Sethuramanujam ◽  
Geoff deRosenroll ◽  
Varsha Jain ◽  
Gautam B Awatramani
Keyword(s):  
Amacrine Cell ◽  
Direction Selectivity ◽  
Author Response ◽  
Cell Responses ◽  
Starburst Amacrine Cell

scholarly journals The functional organization of excitation and inhibition in the dendritic arbors of retinal direction-selective ganglion cells

2019 ◽  
Author(s):  
Varsha Jain ◽  
Benjamin L. Murphy-Baum ◽  
Geoff deRosenroll ◽  
Santhosh Sethuramanujam ◽  
Mike Delsey ◽  
...  
Keyword(s):  
Functional Organization ◽  
Ganglion Cells ◽  
Dendritic Tree ◽  
Amacrine Cells ◽  
Direction Selectivity ◽  
Inhibitory Input ◽  
Processing Scheme ◽  
Fine Grained ◽  
Cell Ablation ◽  
Starburst Amacrine Cells

SUMMARYRecent studies indicate that the precise timing and location of excitation and inhibition (E/I) within active dendritic trees can significantly impact neuronal function. How excitatory and inhibitory inputs are functionally organized at the subcellular level in intact circuits remains unclear. To address this issue, we took advantage of the retinal direction-selective ganglion cell circuit, in which directionally tuned inhibitory GABAergic input arising from starburst amacrine cells shape direction-selective dendritic responses. We combined two-photon Ca2+ imaging with genetic, pharmacological, and single-cell ablation methods to examine local E/I. We demonstrate that when active dendritic conductances are blocked, direction selectivity emerges semi-independently within unusually small dendritic segments (<10 µm). Impressively, the direction encoded by each segment is relatively homogenous throughout the ganglion cell’s dendritic tree. Together the results demonstrate a precise subcellular functional organization of excitatory and inhibitory input, which suggests that the parallel processing scheme proposed for direction encoding could be more fine-grained than previously envisioned.

scholarly journals A model of direction selectivity in the starburst amacrine cell network

2010 ◽  
Vol 28 (3) ◽  
pp. 567-578 ◽  
Author(s):  
Germán A. Enciso ◽  
Michael Rempe ◽  
Andrey V. Dmitriev ◽  
Konstantin E. Gavrikov ◽  
David Terman ◽  
...  
Keyword(s):  
Amacrine Cell ◽  
Direction Selectivity ◽  
Cell Network ◽  
Starburst Amacrine Cell

Nonequivalent cylinder models of neurons: interpretation of voltage transients generated by somatic current injection

1988 ◽  
Vol 60 (1) ◽  
pp. 125-148 ◽  
Author(s):  
P. K. Rose ◽  
A. Dagum
Keyword(s):  
Regional Differences ◽  
Dendritic Tree ◽  
Membrane Properties ◽  
Reliable Estimate ◽  
Voltage Response ◽  
Spinal Motoneurons ◽  
Membrane Resistivity ◽  
Voltage Dependent ◽  
Voltage Transients ◽  
Specific Membrane

1. Numerical methods were used to simulate the voltage responses to an intrasomatic current step of neuronal models that incorporated tapering dendrites, dendrites of unequal electrotonic length, nonlinear membrane properties, and regional differences in specific membrane resistivity (Rm). A "peeling" technique was used to estimate the time constants (tau 0 and tau 1) and coefficients (a0 and a1) of the first two exponential terms of the series of exponential terms whose sum represented the slope of the voltage response. 2. The electrotonic structure of models with a uniform Rm was calculated using equations derived by Rall or Johnston or Brown et al. The adequacy of these methods were tested using a wide variety of models that conformed to the equivalent cylinder approximation of Rall. Johnston's method provided the most reliable estimate of electrotonic length (L) and the ratio of the dendritic conductance to the somatic conductance (rho). However, if L exceeded 2 and rho was eight or larger, the equations derived by Johnston could frequently not be solved due to small errors in the peeled values of tau 0, tau 1, a0, and a1. Although the method suggested by Brown et al. could be applied to all models, this method invariably underestimated L and rho. These errors were particularly large for model neurons with L values of 1.5 or larger and rho values of four or larger. Estimates of L using Rall's method were only reliable if rho was large and L was two or less. 3. Changing the geometry of the dendritic tree (dendritic tapering or dendrites of unequal L) or the addition of a time- and voltage-dependent conductance designed to mimic a sag process commonly seen in spinal motoneurons caused systematic changes in tau 0, tau 1, a0, and a1. The sag process always led to an underestimate of tau 0 even after applying a correction procedure. On the other hand, the ratio, tau 0/tau 1, was not affected by the sag process or dendritic tapering.(ABSTRACT TRUNCATED AT 400 WORDS)

Capacitance Measurements in the Mouse Rod Bipolar Cell Identify a Pool of Releasable Synaptic Vesicles

2006 ◽  
Vol 96 (5) ◽  
pp. 2539-2548 ◽  
Author(s):  
Zhen-Yu Zhou ◽  
Qun-Fang Wan ◽  
Pratima Thakur ◽  
Ruth Heidelberger
Keyword(s):  
Bipolar Cell ◽  
Synaptic Vesicles ◽  
Sine Wave ◽  
Membrane Capacitance ◽  
Membrane Properties ◽  
Intact Mouse ◽  
Time Resolved ◽  
Capacitance Measurements ◽  
Treatment Conditions ◽  
Capacitance Response

The mouse is an important model system for understanding the molecular basis of neuronal signaling and diseases of synaptic communication. However, the best-characterized retinal ribbon-style synapses are those of nonmammalian vertebrates. To remedy this situation, we asked whether it would be feasible to track synaptic vesicle dynamics in the isolated mouse rod bipolar cell using time-resolved capacitance measurements. The results demonstrate that membrane depolarization triggered an increase in membrane capacitance that was Ca2+ dependent and restricted to the synaptic compartment, consistent with exocytosis. The amplitude of the capacitance response recorded from the easily accessible soma of an intact mouse rod bipolar cell was identical to that recorded directly from the small synaptic terminal, suggesting that in the carefully selected cohort of cells presented here, axonal resistance was not a significant barrier to current flow. This supposition was supported by the analysis of passive membrane properties and a comparison of membrane capacitance measurements in cells with and without synaptic terminals and reinforced by the lack of an effect of sine-wave frequency (200–1,600 Hz) on the measured capacitance increase. The magnitude of the capacitance response increased with Ca2+ entry until a plateau was reached at a spatially averaged intraterminal calcium of about 600 nM. We interpret this plateau, nominally 30 fF, as corresponding to a releasable pool of synaptic vesicles. The robustness of this measure suggests that capacitance measurements may be used in the mouse rod bipolar cell to compare pool size across treatment conditions.

Sign in / Sign up

Export Citation Format

Share Document