scholarly journals Nonlinear spatial integration underlies the diversity of retinal ganglion cell responses to natural stimuli

2020 ◽  
Author(s):  
Dimokratis Karamanlis ◽  
Tim Gollisch

AbstractHow neurons encode natural stimuli is a fundamental question for sensory neuroscience. In the early visual system, standard encoding models assume that neurons linearly filter incoming stimuli through their receptive fields, but artificial stimuli, such as reversing gratings, often reveal nonlinear spatial processing. We investigated whether such nonlinear processing is relevant for the encoding of natural images in ganglion cells of the mouse retina. We found that standard linear receptive field models fail to capture the spiking activity for a large proportion of cells. These cells displayed pronounced sensitivity to fine spatial contrast, and local signal rectification was identified as the dominant nonlinearity. In addition, we also observed a class of nonlinear ganglion cells with opposite tuning for spatial contrast and a particular sensitivity for spatially homogeneous stimuli. Our work highlights receptive field nonlinearities as a crucial component for understanding early sensory encoding in the context of natural stimuli.

Perception ◽  
1994 ◽  
Vol 23 (6) ◽  
pp. 691-708 ◽  
Author(s):  
Lothar Spillmann

Psychophysical research on the Hermann grid illusion is reviewed and possible neurophysiological mechanisms are discussed. The illusion is most plausibly explained by lateral inhibition within the concentric receptive fields of retinal and/or geniculate ganglion cells, with contributions by the binocular orientation-specific cortical cells. Results may be summarized as follows: (a) For a strong Hermann grid illusion to be seen bar width must be matched to the mean size of receptive-field centers at any given retinal eccentricity. (b) With the use of this rationale, the diameter of foveal perceptive-field centers (the psychophysical correlate of receptive-field centers) has been found to be in the order of 4–5 min arc and that of total fields (centers plus surrounds) 18 min arc. These small diameters explain why the illusion tends to be absent in foveal vision. (c) With increasing distance from the fovea, perceptive-field centers increase to 1.7 deg at 15 deg eccentricity and then to 3.4 deg at 60 deg eccentricity. This doubling in diameter agrees with the change in size of retinal receptive-field centers in the monkey. (d) The Hermann grid illusion is diminished with dark adaptation. This finding is consistent with the reduction of the center—surround antagonism in retinal receptive fields. (e) The illusion is also weakened when the grid is presented diagonally, which suggests a contribution by the orientation-sensitive cells in the lateral geniculate nucleus and visual cortex. (f) Strong induction effects, similar to the bright and dark spots in the Hermann grid illusion, may be elicited by grids made of various shades of grey; and by grids varying only in chroma or hue. Not accounted for are: the illusory spots occurring in an outline grid ie with hollow squares, and the absence of an illusion when extra bars are added to the grid. Alternative explanations are discussed for the spurious lines connecting the illusory spots along the diagonals and the fuzzy dark bands traversing the rhombi in modified Hermann grids.


2000 ◽  
Vol 17 (2) ◽  
pp. 263-271 ◽  
Author(s):  
HIROYUKI UCHIYAMA ◽  
TAKAHIDE KANAYA ◽  
SHOICHI SONOHATA

One type of retinal ganglion cells prefers object motion in a particular direction. Neuronal mechanisms for the computation of motion direction are still unknown. We quantitatively mapped excitatory and inhibitory regions of receptive fields for directionally selective retinal ganglion cells in the Japanese quail, and found that the inhibitory regions are displaced about 1–3 deg toward the side where the null sweep starts, relative to the excitatory regions. Directional selectivity thus results from delayed transient suppression exerted by the nonconcentrically arranged inhibitory regions, and not by local directional inhibition as hypothesized by Barlow and Levick (1965).


1998 ◽  
Vol 15 (6) ◽  
pp. 1145-1155 ◽  
Author(s):  
D.-J. OH ◽  
D.P.M. NORTHMORE

After being severed, optic axons in goldfish regenerate and eventually restore the retinotectal map; refinement of the map depends upon impulse activity generated by the ganglion cells. Because little is known about the changes in activity and receptive-field properties of ganglion cells during regeneration, we made extracellular recordings from them in the intact eye up to 95 days after sectioning their axons in the optic tract. Their receptive fields were classified as OFF-, ON–OFF-, or ON-centers, and their axonal conduction velocities measured by antidromic activation. The rate of encountering single units dropped drastically at 4–8 days postsection when only a few OFF-center units could be recorded, recovering to normal between 42 and 63 days. Receptive-field centers were normal in size, except for the few OFF-centers at 4–8 days which were abnormally large. Maintained discharge rates of all types were depressed up to 42 days, but ON–OFF-center units were more spontaneously active than normal around 42 days. Light-evoked responses in OFF-center units were subnormal at 4–8 days, becoming supernormal at 16 days and normal thereafter. ON–OFF- and ON-center units started to regain responsiveness at 16 days, and became supernormal at 42 days, before returning to normal. Conduction velocities of all fiber groups dropped to a minimum at 8 days, the fastest being affected most. There was a gradual recovery to normal conduction velocity by 63 days. The conduction latencies of OFF- and ON–OFF-center units recovered to normal by 42 days, and ON-center units by 63 days. Recovery of ganglion cell responsiveness correlates with functional recovery in the retinotectal system: OFF-center units recover light-evoked responses at about the time OFF activity first reappears in the tectum. ON- and ON–OFF-center units recover later, exhibiting supernormal spiking activity around the time that ON responses reappear in the tectum.


1997 ◽  
Vol 14 (6) ◽  
pp. 1153-1165 ◽  
Author(s):  
Stewart A. Bloomfield ◽  
Daiyan Xin

AbstractRecent studies have shown that amacrine and ganglion cells in the mammalian retina are extensively coupled as revealed by the intercellular movement of the biotinylated tracers biocytin and Neurobiotin. These demonstrations of tracer coupling suggest that electrical networks formed by proximal neurons (i.e. amacrine and ganglion cells) may underlie the lateral propagation of signals across the inner retina. We studied this question by comparing the receptive-field size, dendritic-field size, and extent of tracer coupling of amacrine and ganglion cells in the dark-adapted, supervised, isolated retina eyecup of the rabbit. Our results indicate that while the center-receptive fields of proximal neurons are approximately 15% larger than their corresponding dendritic diameters, this slight difference can be explained by factors other than electrical coupling such as tissue shrinkage associated with histological processing. However, the extent of tracer coupling of amacrine and ganglion cells was, on average, about twice the size of the corresponding receptive fields. Thus, the receptive field of an individual proximal neuron matched far more closely to its dendritic diameter than to the size of the tracer-coupled network of cells to which it belonged. The exception to this rule was the AII amacrine cells for which center-receptive fields were 2–3 times the size of their dendritic diameters but matched closely to the size of the tracer-coupled arrays. Thus, with the exception of AII cells, our data indicate that tracer coupling between proximal neurons is not associated with an enlargement of their receptive fields. Our results, then, provide no evidence for electrical coupling or, at least, indicate that extensive lateral spread of visual signals does not occur in the proximal mammalian retina.


2021 ◽  
Author(s):  
Miloslav Sedlacek ◽  
William Grimes ◽  
Morgan Musgrove ◽  
Amurta Nath ◽  
Hua Tian ◽  
...  

In retinal neurons, morphology strongly influences visual response features. Ganglion cell (GC) dendrites ramify in distinct strata of the inner plexiform layer (IPL) so that GCs responding to light increments (ON) or decrements (OFF) receive appropriate excitatory inputs. This vertical stratification prescribes response polarity and ensures consistent connectivity between cell types, whereas the lateral extent of GC dendritic arbors typically dictates receptive field (RF) size. Here, we identify circuitry in mouse retina that contradicts these conventions. A2 amacrine cells are interneurons understood to mediate 'cross-over' inhibition by relaying excitatory input from the ON layer to inhibitory outputs in the OFF layer. Ultrastructural and physiological analyses show, however, that some A2s deliver powerful inhibition to OFF GC somas and proximal dendrites in the ON layer, rendering their inhibitory RFs smaller than their dendritic arbors. This OFF pathway, avoiding entirely the OFF region of the IPL, challenges several tenets of retinal circuitry.


2021 ◽  
Author(s):  
Sarah Strauss ◽  
Maria M Korympidou ◽  
Yanli Ran ◽  
Katrin Franke ◽  
Timm Schubert ◽  
...  

Motion is a critical aspect of vision. We studied the representation of motion in mouse retinal bipolar cells and found, surprisingly, that some bipolar cells possess motion-sensing capabilities that rely on their center-surround receptive fields. Using a glutamate sensor, we directly observed motion-sensitive bipolar cell synaptic output, which was strongest for local motion and dependent on the motion's origin. We characterized bipolar cell receptive fields and found that there are motion and non-motion sensitive bipolar cell types, the majority being motion sensitive. Next, we used these bipolar cell receptive fields along with connectomics to design biophysical models of downstream cells. The models and experiments demonstrated that bipolar cells pass motion-sensitive excitation to starburst amacrine cells through direction-specific signals mediated by bipolar cells' center-surround receptive field structure. As bipolar cells provide excitation to most amacrine and ganglion cells, their motion sensitivity may contribute to motion processing throughout the visual system.


1988 ◽  
Vol 1 (4) ◽  
pp. 377-385 ◽  
Author(s):  
Michael W. Levine ◽  
Roger P. Zimmerman

AbstractA new form of receptive field map, the response-component map, was developed to identify points within a receptive field that produce similar response patterns. The fields were probed with discretely flashed small spots of light. The magnitudes of the responses to stimulus onset and to stimulus offset elicited at each point were represented on the map by a vector radiating from the position representing the location of that point. Thus, response-component maps preserve the spatial distributions of responsivity and temporal nonlinearities. Points with similar response patterns were identified from a scatterplot in which the response at each spatial position was located in a plane representing the angles of the response-component vectors. Points with similar response characteristics that were also spatially contiguous were considered as a distinct response subregion within the receptive field.Barely 10% of the receptive fields of goldfish ganglion cells mapped with this technique proved as simple as the traditional concentric field described for retinal cells. In at least 17% of the cases, the field showed three concentric rings, with a very small “inner center” within the center of the field. In at least 50% of the cases, response subregions of different type lay side by side, rather than in a concentric configuration. Some subregions could be differentiated by the relative strengths of the responses to onset and offset of the stimulus spot, supporting the hypothesis that a push-pull system generates ganglion cell responses. Subregions were evident in successive mappings of the same cell, demonstrating they are not due to the vagaries of individual responses. They probably represent the spatial domains (or their intersections) of individual interneurons distal to the retinal ganglion cells. It is possible that position within the receptive field may be coded by the temporal pattern of the responses.


1993 ◽  
Vol 10 (1) ◽  
pp. 31-39 ◽  
Author(s):  
Charlene Stone ◽  
Lawrence H. Pinto

AbstractWe have studied the organization of receptive fields of ganglion cells in the isolated mouse retina and have shown that the organization is similar to that of the cat. Based upon responses to circular and annular stimuli, most ganglion cells (90%; N = 83) had receptive fields with concentric center-surround organization, either ON or OFF center. The plot of response amplitude vs. stimulus area for these cells increased to a maximum (corresponding to a diameter of 10.0 ± 2.8 deg S.E.M.; N = 13) and then decreased for larger stimuli, demonstrating the presence of an antagonistic surround. The dark-adapted sensitivity (205 ± 43.8 impulses quantum−1 rod−1; mean ± S.E.M.) did not differ from that measured for the intact preparation. We found a subset of OFF-center cells for which the dark discharge was very regular (mean coefficient of variation = 0.30). Using sinusoidal grating stimuli, we classified ganglion cells as X-like (87%) and Y-like (13%) based on spatial summation properties and the presence of subunit activity in the receptive-field center. We found no difference in the spatial-frequency preference between X-like and Y-like cells in the central retina (high cutoff frequency, 0.20 ± 0.014 cycle/deg, mean ± S.E.M.), in contrast to the marked difference between X cells and Y cells in the cat. Thus, ganglion cell receptive fields in the mouse retina resemble those of the cat, although the spatial characteristics of the receptive fields in the central retina are more homogeneous. This homogeneity would simplify the comparison of retinas from normal and mutant strains of the mouse.


2014 ◽  
Vol 112 (8) ◽  
pp. 1950-1962 ◽  
Author(s):  
Minggang Chen ◽  
Seunghoon Lee ◽  
Silvia J. H. Park ◽  
Loren L. Looger ◽  
Z. Jimmy Zhou

Retinal bipolar cells (BCs) transmit visual signals in parallel channels from the outer to the inner retina, where they provide glutamatergic inputs to specific networks of amacrine and ganglion cells. Intricate network computation at BC axon terminals has been proposed as a mechanism for complex network computation, such as direction selectivity, but direct knowledge of the receptive field property and the synaptic connectivity of the axon terminals of various BC types is required in order to understand the role of axonal computation by BCs. The present study tested the essential assumptions of the presynaptic model of direction selectivity at axon terminals of three functionally distinct BC types that ramify in the direction-selective strata of the mouse retina. Results from two-photon Ca2+ imaging, optogenetic stimulation, and dual patch-clamp recording demonstrated that 1) CB5 cells do not receive fast GABAergic synaptic feedback from starburst amacrine cells (SACs); 2) light-evoked and spontaneous Ca2+ responses are well coordinated among various local regions of CB5 axon terminals; 3) CB5 axon terminals are not directionally selective; 4) CB5 cells consist of two novel functional subtypes with distinct receptive field structures; 5) CB7 cells provide direct excitatory synaptic inputs to, but receive no direct GABAergic synaptic feedback from, SACs; and 6) CB7 axon terminals are not directionally selective, either. These findings help to simplify models of direction selectivity by ruling out complex computation at BC terminals. They also show that CB5 comprises two functional subclasses of BCs.


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