Spatial Distribution of Suppressive Signals Outside the Classical Receptive Field in Lateral Geniculate Nucleus

2005 ◽  
Vol 94 (3) ◽  
pp. 1789-1797 ◽  
Author(s):  
Ben S. Webb ◽  
Christopher J. Tinsley ◽  
Christopher J. Vincent ◽  
Andrew M. Derrington

A suppressive surround modulates the responsiveness of cells in the lateral geniculate nucleus (LGN), but we know nothing of its spatial structure or the way in which it combines signals arising from different locations. It is generally assumed that suppressive signals are either uniformly distributed or balanced in opposing regions outside the receptive field. Here, we examine the spatial distribution and summation of suppressive signals outside the receptive field in extracellular recordings from 46 LGN cells in anesthetized marmosets. The receptive field of each cell was stimulated with a drifting sinusoidal grating of the preferred size and spatial and temporal frequency; we probed different positions in the suppressive surround with either a large half-annular grating or a small circular grating patch of the preferred spatial and temporal frequency. In many of the cells with a strong suppressive surround (29/46), the spatial distribution of suppression showed clear deviation from circular symmetry. In the majority of these of cells, suppressive signals were spatially asymmetrical or balanced in opposing areas outside the receptive field. A suppressive area was larger than the classical receptive field itself and spatial summation within and between these areas was nonlinear. There was no bias for suppression to arise from foveal or nasal retina where cone density is higher and no other sign of a systematic spatial organization to the suppressive surround. We conclude that nonclassical suppressive signals in LGN deviate from circular symmetry and are nonlinearly combined.

2002 ◽  
Vol 19 (5) ◽  
pp. 583-592 ◽  
Author(s):  
BEN S. WEBB ◽  
CHRIS J. TINSLEY ◽  
NICK E. BARRACLOUGH ◽  
ALEXANDER EASTON ◽  
AMANDA PARKER ◽  
...  

It is well established that the responses of neurons in the lateral geniculate nucleus (LGN) can be modulated by feedback from visual cortex, but it is still unclear how cortico-geniculate afferents regulate the flow of visual information to the cortex in the primate. Here we report the effects, on the gain of LGN neurons, of differentially stimulating the extraclassical receptive field, with feedback from the striate cortex intact or inactivated in the marmoset monkey, Callithrix jacchus. A horizontally oriented grating of optimal size, spatial frequency, and temporal frequency was presented to the classical receptive field. The grating varied in contrast (range: 0–1) from trial to trial, and was presented alone, or surrounded by a grating of the same or orthogonal orientation, contained within either a larger annular field, or flanks oriented either horizontally or vertically. V1 was ablated to inactivate cortico-geniculate feedback. The maximum firing rate of LGN neurons was greater with V1 intact, but was reduced by visually stimulating beyond the classical receptive field. Large horizontal or vertical annular gratings were most effective in reducing the maximum firing rate of LGN neurons. Magnocellular neurons were most susceptible to this inhibition from beyond the classical receptive field. Extraclassical inhibition was less effective with V1 ablated. We conclude that inhibition from beyond the classical receptive field reduces the excitatory influence of V1 in the LGN. The net balance between cortico-geniculate excitation and inhibition from beyond the classical receptive field is one mechanism by which signals relayed from the retina to V1 are controlled.


2003 ◽  
Vol 90 (5) ◽  
pp. 3398-3418 ◽  
Author(s):  
Stephen D. Van Hooser ◽  
J. Alexander F. Heimel ◽  
Sacha B. Nelson

Physiological studies of the lateral geniculate nucleus (LGN) have revealed three classes of relay neurons, called X, Y, and W cells in carnivores and parvocellular (P), magnocellular (M), and koniocellular (K) in primates. The homological relationships among these cell classes and how receptive field (RF) properties of these cells compare with LGN cells in other mammals are poorly understood. To address these questions, we have characterized RF properties and laminar organization in LGN of a highly visual diurnal rodent, the gray squirrel, under isoflurane anesthesia. We identified three classes of LGN cells. One class found in layers 1 and 2 showed sustained, reliable firing, center-surround organization, and was almost exclusively linear in spatial summation. Another class, found in layer 3, showed short response latencies, transient and reliable firing, center-surround organization, and could show either linear (76%) or nonlinear (24%) spatial summation. A third, heterogeneous class found throughout the LGN but primarily in layer 3 showed highly variable responses, a variety of response latencies and could show either center-surround or noncenter-surround receptive field organization and either linear (77%) or nonlinear (23%) spatial summation. RF sizes of all cell classes showed little dependency on eccentricity, and all of these classes showed low contrast gains. When compared with LGN cells in other mammals, our data are consistent with the idea that all mammals contain three basic classes of LGN neurons, one showing reliable, sustained responses, and center-surround organization (X or P); another showing transient but reliable responses, short latencies, and center-surround organization (Y or M); and a third, highly variable and heterogeneous class of cells (W or K). Other properties such as dependency of receptive field size on eccentricity, linearity of spatial summation, and contrast gain appear to vary from species to species.


2014 ◽  
Vol 112 (3) ◽  
pp. 603-619 ◽  
Author(s):  
Satoshi Shimegi ◽  
Ayako Ishikawa ◽  
Hiroyuki Kida ◽  
Hiroshi Sakamoto ◽  
Sin-ichiro Hara ◽  
...  

In the primary visual cortex (V1), a neuronal response to stimulation of the classical receptive field (CRF) is predominantly suppressed by a stimulus presented outside the CRF (extraclassical receptive field, ECRF), a phenomenon referred to as ECRF suppression. To elucidate the neuronal mechanisms and origin of ECRF suppression in V1 of anesthetized cats, we examined the temporal properties of the spatial extent and orientation specificity of ECRF suppression in V1 and the lateral geniculate nucleus (LGN), using stationary-flashed sinusoidal grating. In V1, we found three components of ECRF suppression: 1) local and fast, 2) global and fast, and 3) global and late. The local and fast component, which resulted from within 2° of the boundary of the CRF, started no more than 10 ms after the onset of the CRF response and exhibited low specificity for the orientation of the ECRF stimulus. These spatiotemporal properties corresponded to those of geniculate ECRF suppression, suggesting that the local and fast component of V1 is inherited from the LGN. In contrast, the two global components showed rather large spatial extents ∼5° from the CRF boundary and high specificity for orientation, suggesting that their possible origin is the cortex, not the LGN. Correspondingly, the local component was observed in all neurons of the thalamocortical recipient layer, while the global component was biased toward other layers. Therefore, we conclude that both subcortical and cortical mechanisms with different spatiotemporal properties are involved in ECRF suppression.


1990 ◽  
Vol 5 (6) ◽  
pp. 525-545 ◽  
Author(s):  
Earl L. Smith ◽  
Yuzo M. Chino ◽  
William H. Ridder ◽  
Kosuke Kitagawa ◽  
Andy Langston

AbstractThe purpose of this investigation was to analyze the influence of stimulus orientation on the responses of individual neurons in the monkey's lateral geniculate nucleus (LGN). Our specific goals were to assess the prevalence and the degree of orientation tuning in the monkey LGN and to determine if the preferred stimulus orientations of LGN neurons varied as a function of receptive-field position. The primary motivation for this research was to gain insight into the receptive-field configuration of LGN neurons and consequently into the neural mechanisms which determine the spatial organization of LGN receptive fields in primates.In both the parvocellular and magnocellular layers, the responses of the majority of individual neurons to sine-wave gratings varied as a function of stimulus orientation. The influence of stimulus orientation was, however, highly dependent on the spatial characteristics of the stimulus; the greatest degree of orientation bias was observed for spatial frequencies higher than the cell's optimal spatial frequency. On a population basis, the degree of orientation bias was similar for all major classes of LGN neurons (e.g. ON vs. OFF center; parvocellular vs. magnocellular) and did not vary systematically with receptive-field eccentricity. At a given receptive-field location, LGN neurons, particularly cells in the parvocellular laminae, tended to prefer either radially oriented stimuli or stimuli oriented more horizontally than their polar axis. Our analyses of the orientation-dependent changes in spatial-frequency response functions, which was based on the Soodak et al., (1987; Soodak, 1986) two-dimensional, difference-of-Gaussian receptive-field model, suggested that the orientation bias in LGN neurons was due to an elongation of the receptive-field center mechanism which in some cases appeared to consist of multiple subunits. Direct comparisons of the orientation-tuning characteristics of LGN cells and their retinal inputs (S potentials) indicated that the orientation bias in the monkey LGN reflects primarily the functional properties of individual retinal ganglion cells. We conclude that orientation sensitivity is a significant property of subcortical neurons in the primate's geniculo-cortical pathway.


1997 ◽  
Vol 78 (2) ◽  
pp. 1045-1061 ◽  
Author(s):  
Daqing Cai ◽  
Gregory C. Deangelis ◽  
Ralph D. Freeman

Cai, Daqing, Gregory C. DeAngelis, and Ralph D. Freeman. Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. J. Neurophysiol. 78: 1045–1061, 1997. We have studied the spatiotemporal receptive-field organization of 144 neurons recorded from the dorsal lateral geniculate nucleus (dLGN) of adult cats and kittens at 4 and 8 wk postnatal. Receptive-field profiles were obtained with the use of a reverse correlation technique, in which we compute the cross-correlation between the action potential train of a neuron and a randomized sequence of long bright and dark bar stimuli that are flashed throughout the receptive field. Spatiotemporal receptive-field profiles of LGN neurons generally exhibit a biphasic temporal response, as well as the classical center-surround spatial organization. For nonlagged cells, the first temporal phase of the response dominates, whereas for lagged neurons, the second temporal phase of the response is typically the largest. This temporal phase difference between lagged and nonlagged cells accounts for their divergent behavior in response to flashed stimuli. Most LGN cells exhibit some degree of space-time inseparability, which means that the receptive field cannot simply be viewed as the product of a spatial waveform and a temporal waveform. In these cases, the response of the surround is typically delayed relative to that of the center, and there is some blending of center and surround during the time course of the response. We demonstrate that a simple extension of the traditional difference-of-Gaussians (DOG) model, in which the surround response is delayed relative to that of the center, accounts nicely for these findings. With regard to development, our analysis shows that spatial and temporal aspects of receptive field structure mature with markedly different time courses. After 4 wk postnatal, there is little change in the spatial organization of LGN receptive fields, with the exception of a weak, but significant, trend for the surround to become smaller and stronger with age. In contrast, there are substantial changes in temporal receptive-field structure after 4 wk postnatal. From 4 to 8 wk postnatal, the shape of the temporal response profile changes, becoming more biphasic, but the latency and duration of the response remain unchanged. From 8 wk postnatal to adulthood, the shape of the temporal profile remains approximately constant, but there is a dramatic decline in both the latency and duration of the response. Comparison of our results with recent data from cortical (area 17) simple cells reveals that the temporal development of LGN cells accounts for a substantial portion of the temporal maturation of simple cells.


1995 ◽  
Vol 74 (3) ◽  
pp. 1222-1243 ◽  
Author(s):  
P. Mukherjee ◽  
E. Kaplan

1. We investigated the time domain transformation that thalamocortical relay cells of the cat lateral geniculate nucleus (LGN) perform on their retinal input, and used computational modeling to explore the biophysical properties that determine the dynamics of the LGN relay cells in vivo. 2. We recorded simultaneously the input (S potentials) and output (action potentials) of 50 cat LGN relay cells stimulated by drifting sinusoidal gratings of varying temporal frequency. The temporal modulation transfer functions (TMTFs) of the neurons were derived from these data. The burstiness of the LGN spike trains was also assessed using objective criteria. 3. We found that the form of the TMTF was quite variable among cells, ranging from low-pass to strongly band-pass. The optimal temporal frequency of band-pass neurons was between 2 and 8 Hz. In addition, the TMTF of some cells was nonstationary: their temporal tuning changed with time. 4. The temporal tuning of a cell was directly related to the degree of burstiness of its spike train. Tonically firing relay cells had low-pass TMTFs, whereas the most bursty neurons exhibited the most sharply band-pass transfer functions. This was also true for single cells that altered their temporal tuning: a shift to more band-pass tuning was associated with increased burstiness of the spike train, and vice versa. 5. We constructed a computer simulation of the LGN relay cell. The model was a simplified five-channel version of the thalamocortical neuron model of McCormick and Huguenard. It incorporated the quantitative kinetics of the Ca2+ T channel, as well as the Hodgkin-Huxley Na+ and K+ channels, as the only active membrane currents. To simulate the in vivo dynamics of the relay cell, the input to the model consisted of trains of synaptic potentials, recorded as S potentials in our physiological experiments. 6. When the resting membrane potential of the model neuron was relatively depolarized, the model's TMTF was low-pass, with no bursting evident in the simulated spike train. At hyperpolarized resting membrane potentials, however, the modeled TMTF was band-pass, with frequent burst discharges. Thus the biophysical model reproduced not only the range of dynamics seen in real LGN relay cells, but also the dependence of the overall dynamics on the burstiness of the spike train. However, neither of these phenomena could be simulated without the T channel. Thus the simulations demonstrated that the T-type Ca2+ channel was necessary and sufficient to explain the LGN dynamics observed in physiological experiments.(ABSTRACT TRUNCATED AT 400 WORDS)


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Bram-Ernst Verhoef ◽  
John HR Maunsell

Shifting attention among visual stimuli at different locations modulates neuronal responses in heterogeneous ways, depending on where those stimuli lie within the receptive fields of neurons. Yet how attention interacts with the receptive-field structure of cortical neurons remains unclear. We measured neuronal responses in area V4 while monkeys shifted their attention among stimuli placed in different locations within and around neuronal receptive fields. We found that attention interacts uniformly with the spatially-varying excitation and suppression associated with the receptive field. This interaction explained the large variability in attention modulation across neurons, and a non-additive relationship among stimulus selectivity, stimulus-induced suppression and attention modulation that has not been previously described. A spatially-tuned normalization model precisely accounted for all observed attention modulations and for the spatial summation properties of neurons. These results provide a unified account of spatial summation and attention-related modulation across both the classical receptive field and the surround.


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