Evidence for an additive inhibitory component of contrast adaptation

The latency of visual responses generally decreases as contrast increases. Recording in the lateral geniculate nucleus (LGN), we find that response latency increases with increasing contrast in ON cells for some visual stimuli. We propose that this surprising latency trend can be explained if ON cells rest further from threshold at higher contrasts. Indeed, while contrast changes caused a combination of multiplicative gain change and additive shift in LGN cells, the additive shift predominated in ON cells. Modeling results supported this theory: the ON cell latency trend was found when the distance-to-threshold shifted with contrast, but not when distance-to-threshold was fixed across contrasts. In the model, latency also increases as surround-to-center ratios increase, which has been shown to occur at higher contrasts. We propose that higher-contrast full-field stimuli can evoke more surround inhibition, shifting the potential further from spiking threshold and thereby increasing response latency

Brain Differently Changes Its Algorithms in Parallel Processing of Visual Information

Feedback from the visual cortex (Vl) to the Lateral Geniculate Nucleus (LGN) in macaque monkey increase contrast gain of LGN neurons for black and white (B&W) and for color (C) stimuli. LGN parvocellular cells responses to B&W gratings are enhanced by feedback multiplicatively and in contrast independent manner. However, in magnocellular neurons corticofugal pathways enhance cells responses in a contrast~dependent non-linear manner. For C stimuli cortical feedback enhances parvocellular neurons responses in a very strong contrast-dependent manner. Based on these results [13] we propose a model which includes excitatory and inhibitory effects on cells activity (shunting equations) in retina and LGN while taking into account the anatomy of cortical feedback connections. The main mechanisms related to different algorithms of the data processing in the visual brain are differences in feedback properties from Vl to parvocellular (PC) and to magnocellular (MC) neurons. Descending pathways from Vl change differently receptive field (RF) structure of PC and MC cells. For B&W stimuli, in PC cells feedback changes gain similarly in the RF center and in the RF surround, leaving PC RF structure invariant. However, feedback influence MC cells in two ways: directly and through LGN interneurons, which together changes gain and sizes of their RF center differently than gain and size of the RF surround. For C stimuli PC cells operate like MC cells for B&W. The first mechanism extracts from the stimulus an important features in a independent way from other stimulus parameters, whereas the second channel changes its tuning properties as a function of other stimulus attributes like contrast and/or spatial extension. The model suggests novel idea about the possible functional role of PC and MC pathways

A Nonlinear Model of Spatiotemporal Retinal Processing: Simulations of X and Y Retinal Ganglion Cell Behavior

This article describes a nonlinear model of neural processing in the vertebrate retina, comprising model photoreceptors, model push-pull bipolar cells, and model ganglion cells. Previous analyses and simulations have shown that with a choice of parameters that mimics beta cells, the model exhibits X-like linear spatial summation (null response to contrast-reversed gratings) in spite of photoreceptor nonlinearities; on the other hand, a choice of parameters that mimics alpha cells leads to Y-like frequency doubling. This article extends the previous work by showing that the model can replicate qualitatively many of the original findings on X and Y cells with a fixed choice of parameters. The results generally support the hypothesis that X and Y cells can be seen as functional variants of a single neural circuit. The model also suggests that both depolarizing and hyperpolarizing bipolar cells converge onto both ON and OFF ganglion cell types. The push-pull connectivity enables ganglion cells to remain sensitive to deviations about the mean output level of nonlinear photoreceptors. These and other properties of the push-pull model are discussed in the general context of retinal processing of spatiotemporal luminance patterns.Alfred P. Sloan Research Fellowship (BR-3122); Air Force Office of Scientific Research (F49620-92-J-0499

Thalamic contributions to mechanisms underlying genesis of sensitivity to contour length in the visual system

Sensitivity to visual stimulus length was first described by Hubei and Wiesel for cells at the end of the proposed hierarchical sequence in the visual cortex, the so called "hypercomplex cells". However, it has subsequently become clear that length sensitivity is seen in a significant proportion of cells at the first level of processing in the visual cortex, and in lateral geniculate cells relaying retinal input to the visual cortex. This project is concerned with synaptic processes generating length preference at the level of the geniculate, and their significance for the cortical representation of stimulus length. Utilising single unit recording techniques, length response curves were obtained from cells recorded in the dorsal lateral geniculate nucleus (dLGN) and the perigeniculate nucleus (PGN). The majority of dLGN cells exhibited a degree of length tuning equivalent to that seen in tightly tuned cortical hypercomplex cells. Additionally, an apparently distinct sub-population of poorly tuned Y cells was identified. Most PGN cells also exhibited poorly tuned fields. These results are discussed in terms of possible synaptic circuitry generating length sensitivity at sub- cortical and cortical levels. It is suggested that the results have bearing on the modelling of synaptic processes contributing to cortical cell length tuning profiles. The corticofugal system provides the largest single input to the dLGN and has previously been shown to contribute to the generation of length tuning in the dLGN. Knowledge of the mode of synaptic action of the corticofugal system is therefore critical to an understanding of mechanisms generating length tuning. Koch suggested that corticofugal fibres mediate their effects by modulating NMDA receptor responses. While some studies suggest that the retinal neurotransmitter acts on NMDA and non- NMDA receptors, others suggest that it acts only on non-NMDA receptors. In the mammalian dLGN there is no clear evidence as to the identity of the optic nerve transmitter. As a preliminary attempt to address this issue, an iontophoretic technique was utilised to examine the effects and pharmacology of two putative optic nerve transmitters thought to act on NMDA receptors. The effects of selective NMDA and non-NMDA receptor antagonists were examined on the responses to these and to visual stimuli

The Role of Non-Linearities in Visual Perception studied with a Computational Model of the Vertebrate Retina

Processing of visual stimuli in the vertebrate retina is complex and diverse. The retinal output to the higher centres of the nervous system, mediated by ganglion cells, consists of several different channels. Neurons in these channels can have very distinct response properties, which originate in different retinal pathways. In this work, the retinal origins and possible functional implications of the segregation of visual pathways will be investigated with a detailed, biologically realistic computational model of the retina. This investigation will focus on the two main retino-cortical pathways in the mammalian retina, the parvocellular and magnocellular systems, which are crucial for conscious visual perception. These pathways differ in two important aspects. The parvocellular system has a high spatial, but low temporal resolution. Conversely, the magnocellular system has a high temporal fidelity, spatial sampling however is less dense than for parvocellular cells. Additionally, the responses of magnocellular ganglion cells can show pronounced nonlinearities, while the parvocellular system is essentially linear. The origin of magnocellular nonlinearities is unknown and will be investigated in the first part of this work. As their main source, the results suggest specific properties of the photoreceptor response and a specialised amacrine cell circuit in the inner retina. The results further show that their effect combines in a multiplicative way. The model is then used to examine the influence of nonlinearities on the responses of ganglion cells in the presence of involuntary fixational eye movements. Two different stimulus conditions will be considered: visual hyperacuity and motion induced illusions. In both cases, it is possible to directly compare properties of the ganglion cell population response with psychophysical data, which allows for an analysis of the influence of different components of the retinal circuitry. The simulation results suggest an important role for nonlinearities in the magnocellular stream for visual perception in both cases. First, it will be shown how nonlinearities, triggered by fixational eye movements, can strongly enhance the spatial precision of magnocellular ganglion cells. As a result, their performance in a hyperacuity task can be equal to or even surpass that of the parvocellular system. Second, the simulations imply that the origin of some of the illusory percepts elicited by fixational eye movements could be traced back to the nonlinear properties of magnocellular ganglion cells. As these activity patterns strongly differ from those in the parvocellular system, it appears that the magnocellular system can strongly dominate visual perception in certain conditions. Taken together, the results of this theoretical study suggest that retinal nonlinearities may be important for and strongly influence visual perception. The model makes several experimentally verifiable predictions to further test and quantify these findings. Furthermore, models investigating higher visual processing stages may benefit from this work, which could provide the basis to produce realistic afferent input

Spatiotemporal receptive field properties of epiretinally recorded spikes and local electroretinograms in cats

BACKGROUND: Receptive fields of retinal neural signals of different origin can be determined from extracellular microelectrode recordings at the inner retinal surface. However, locations and types of neural processes generating the different signal components are difficult to separate and identify. We here report epiretinal receptive fields (RFs) from simultaneously recorded spikes and local electroretinograms (LERGs) using a semi-chronic multi-electrode in vivo recording technique in cats. Broadband recordings were filtered to yield LERG and multi unit as well as single unit spike signals. RFs were calculated from responses to multifocal pseudo-random spatiotemporal visual stimuli registered at the retinal surface by a 7-electrode array. RESULTS: LERGs exhibit spatially unimodal RFs always centered at the location of the electrode tip. Spike-RFs are either congruent with LERG-RFs (N = 26/61) or shifted distally (N = 35/61) but never proximally with respect to the optic disk. LERG-RFs appear at shorter latencies (11.9 ms ± 0.5 ms, N = 18) than those of spikes (18.6 ms ± 0.4 ms, N = 53). Furthermore, OFF-center spike-RFs precede and have shorter response rise times than ON-center spike-RFs. Our results indicate that displaced spike-RFs result from action potentials of ganglion cell axons passing the recording electrode en route to the optic disk while LERG-RFs are related to superimposed postsynaptic potentials of cells near the electrode tip. CONCLUSION: Besides contributing to the understanding of retinal function we demonstrate the caveats that come with recordings from the retinal surface, i.e., the likelihood of recordings from mixed sets of retinal neurons. Implications for the design of an epiretinal visual implant are discussed

Retinal ganglion cells and the magnocellular, parvocellular, and koniocellular subcortical visual pathways from the eye to the brain

In primates including humans, most retinal ganglion cells send signals to the lateral geniculate nucleus (LGN) of the thalamus. The anatomical and functional properties of the two major pathways through the LGN, the parvocellular (P) and magnocellular (M) pathways, are now well understood. Neurones in these pathways appear to convey a filtered version of the retinal image to primary visual cortex for further analysis. The properties of the P-pathway suggest it is important for high spatial acuity and red-green color vision, while those of the M-pathway suggest it is important for achromatic visual sensitivity and motion vision. Recent work has sharpened our understanding of how these properties are built in the retina, and described subtle but important nonlinearities that shape the signals that cortex receives. In addition to the P- and M-pathways, other retinal ganglion cells also project to the LGN. These ganglion cells are larger than those in the P- and M-pathways, have different retinal connectivity, and project to distinct regions of the LGN, together forming heterogenous koniocellular (K) pathways. Recent work has started to reveal the properties of these K-pathways, in the retina and in the LGN. The functional properties of K-pathways are more complex than those in the P- and M-pathways, and the K-pathways are likely to have a distinct contribution to vision. They provide a complementary pathway to the primary visual cortex, but can also send signals directly to extrastriate visual cortex. At the level of the LGN, many neurones in the K-pathways seem to integrate retinal with non-retinal inputs, and some may provide an early site of binocular convergence

Interhemispheric transfer and the processing of foveally presented stimuli

A review of the literature shows that the LVF and the RVF do not overlap. This means that foveal representations of words are effectively split and that interhemispheric communication is needed to recognise centrally presented words