Effects of stimulus spatial frequency, size, and luminance contrast on orientation tuning of neurons in the dorsal lateral geniculate nucleus of cat (original) (raw)
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Frontiers in Systems Neuroscience, 2011
Controversy remains about how orientation selectivity emerges in simple cells of the mammalian primary visual cortex. In this paper, we present a computational model of how the orientation-biased responses of cells in lateral geniculate nucleus (LGN) can contribute to the orientation selectivity in simple cells in cats. We propose that simple cells are excited by lateral geniculate fields with an orientation-bias and disynaptically inhibited by unoriented lateral geniculate fields (or biased fields pooled across orientations), both at approximately the same retinotopic co-ordinates.This interaction, combined with recurrent cortical excitation and inhibition, helps to create the sharp orientation tuning seen in simple cell responses. Along with describing orientation selectivity, the model also accounts for the spatial frequency and length-response functions in simple cells, in normal conditions as well as under the influence of the GABA A antagonist, bicuculline. In addition, the model captures the response properties of LGN and simple cells to simultaneous visual stimulation and electrical stimulation of the LGN. We show that the sharp selectivity for stimulus orientation seen in primary visual cortical cells can be achieved without the excitatory convergence of the LGN input cells with receptive fields along a line in visual space, which has been a core assumption in classical models of visual cortex. We have also simulated how the full range of orientations seen in the cortex can emerge from the activity among broadly tuned channels tuned to a limited number of optimum orientations, just as in the classical case of coding for color in trichromatic primates.
The Journal of Physiology, 2011
Non technical summary Neurones of the mammalian primary visual cortex have the remarkable property of being selective for the orientation of visual contours. It has been controversial whether this selectivity arises purely from mechanisms within the cortex itself, from the special way afferents from the thalamus project to the cortex or from the sharpening of a bias for orientation that already exists in the retina and the thalamus. Our experiments support the last of these three hypotheses. We used a special protocol to study both inhibitory and excitatory interactions within the cortex as well as in the thalamus and we find that the orientation selectivity may depend upon multiple mechanisms-including the thalamic biases for orientation and intracortical inhibition and excitation.
Journal of Neuroscience - J NEUROSCI, 2004
In the primary visual cortex (V1), the single-neuron response to a grating stimulus placed in the classical receptive field (CRF) is suppressed by a similar stimulus presented in the CRF surround. To assess the input mechanism underlying the surround suppression, we tested the effects of iontophoretically administered GABAA-receptor antagonist, bicuculline methiodide (BMI), for the 46 V1 neurons in anesthetized cats. First, the stimulus-size tuning curves were studied, with or without BMI administration, for each neuron by changing the size of the grating patch. During the BMI administration, the shape of the normalized size tuning curve did not change considerably. Second, the dependency of surround suppression on the orientation of the surround grating was examined. In the control, the surround suppression showed the clear orientation tuning that peaked at an orientation the same as the optimal orientation of the CRF response. The BMI administration did not change the orientation ...
Mechanisms of Direction Selectivity in Cat Primary Visual Cortex as Revealed by Visual Adaptation
Journal of Neurophysiology, 2010
In contrast to neurons of the lateral geniculate nucleus (LGN), neurons in the primary visual cortex (V1) are selective for the direction of visual motion. Cortical direction selectivity could emerge from the spatiotemporal configuration of inputs from thalamic cells, from intracortical inhibitory interactions, or from a combination of thalamic and intracortical interactions. To distinguish between these possibilities, we studied the effect of adaptation (prolonged visual stimulation) on the direction selectivity of intracellularly recorded cortical neurons. It is known that adaptation selectively reduces the responses of cortical neurons, while largely sparing the afferent LGN input. Adaptation can therefore be used as a tool to dissect the relative contribution of afferent and intracortical interactions to the generation of direction selectivity. In both simple and complex cells, adaptation caused a hyperpolarization of the resting membrane potential (−2.5 mV, simple cells, −0.95 ...
Journal of Neuroscience, 2009
The response of the classical receptive field of visual neurons can be suppressed by stimuli that, when presented alone, cause no change in the discharge rate. This suppression reveals the presence of an extraclassical receptive field (ECRF). In recordings from the lateral geniculate nucleus (LGN) of a New World primate, the marmoset, we characterize the mechanisms that contribute to the ECRF by measuring their spatiotemporal tuning during prolonged exposure to a high-contrast grating (contrast adaptation). The ECRF was strongest in magnocellular cells, where contrast adaptation reduced suppression from the ECRF: adaptation of the ECRF transferred across spatial frequency, temporal frequency, and orientation, but not across space. This implies that the ECRF of LGN cells comprises multiple adaptable mechanisms, each broadly tuned but spatially localized, and consistent with a retinal origin. Signals from the ECRF saturated at high contrasts, and so adaptation of one part of the ECRF brought into its operating range signals from other parts of the visual field. Although the ECRF is adaptable, its major impact during contrast adaptation to a spatially extended pattern was to reduce visual response and hence reduce a neuron's susceptibility to contrast adaptation; in normal viewing, a major role of the ECRF might be to protect visual sensitivity in scenes dominated by high contrast.
Subcortical orientation biases explain orientation selectivity of visual cortical cells
Physiological reports, 2015
The primary visual cortex of carnivores and primates shows an orderly progression of domains of neurons that are selective to a particular orientation of visual stimuli such as bars and gratings. We recorded from single-thalamic afferent fibers that terminate in these domains to address the issue whether the orientation sensitivity of these fibers could form the basis of the remarkable orientation selectivity exhibited by most cortical cells. We first performed optical imaging of intrinsic signals to obtain a map of orientation domains on the dorsal aspect of the anaesthetized cat's area 17. After confirming using electrophysiological recordings the orientation preferences of single neurons within one or two domains in each animal, we pharmacologically silenced the cortex to leave only the afferent terminals active. The inactivation of cortical neurons was achieved by the superfusion of either kainic acid or muscimol. Responses of single geniculate afferents were then recorded b...
Visual Neuroscience, 1995
There is controversy in the literature concerning whether or not neurons in the cat's posteromedial lateral suprasylvian (PMLS) visual cortex are orientation selective. Previous studies that have tested cells with simple bar stimuli have found that few, if any, PMLS cells are orientation selective. Conversely, studies that have used repetitive stimuli such as gratings have found that most or all PMLS cells are orientation selective. It is not known whether this difference in results is due to the stimuli used or the laboratories using them. The present experiments were designed to answer this question by testing individual PMLS neurons for orientation sensitivity with both bar and grating stimuli. Using quantitative response measures, we found that most PMLS neurons respond well enough to stationary flashed stimuli to use such stimuli to test for orientation sensitivity. On the basis of these tests, we found that about 85% of the cells with well-defined receptive fields are orie...
Contrast Sensitivity Is Enhanced by Expansive Nonlinear Processing in the Lateral Geniculate Nucleus
2008
The firing rates of neurons in the central visual pathway vary with stimulus strength, but not necessarily in a linear manner. In the contrast domain, the neural response function for cells in the primary visual cortex is characterized by expansive and compressive nonlinearities at low and high contrasts, respectively. A compressive nonlinearity at high contrast is also found for early visual pathway neurons in the LGN. This mechanism affects processing in the visual cortex. A fundamentally related issue is the possibility of an expansive nonlinearity at low contrast in LGN. To examine this possibility, we have obtained contrast-response data for a population of LGN neurons. We find for most cells that the best fit function requires an expansive component. Additionally, we have measured the responses of LGN neurons to m-sequence white noise and examine the static relationship between a linear prediction and actual spike rate. We find that this static relationship is well-fit by an expansive nonlinear power law with average exponent of 1.58. These results demonstrate that neurons in early visual pathways exhibit expansive nonlinear responses at low contrasts. While this thalamic expansive nonlinearity has been largely ignored in models of early visual processing, it may have important consequences because it potentially affects the interpretation of a variety of visual functions. intracellular study of the contrast-dependence of neuronal activity in cat visual cortex. Cereb Cortex 7: 559-570, 1997. Albrecht DG and Geisler WS. Motion selectivity and the contrast-response function of simple cells in the visual cortex. Vis Neurosci 7: 531-546, 1991. Albrecht DG and Hamilton DB. Striate cortex of monkey and cat: contrast response function. Anzai A, Ohzawa I, and Freeman RD. Neural mechanisms for processing binocular information I. Simple cells. J Neurophysiol 82: 891-908, 1999a. Anzai A, Ohzawa I, and Freeman RD. Neural mechanisms for processing binocular information II. Complex cells. J Neurophysiol 82: 909-924, 1999b. Bonin V, Mante V, and Carandini M. The statistical computation underlying contrast gain control. J Neurosci 26: 6346-6353, 2006. Bonin V, Mante V, and Carandini M. The suppressive field of neurons in lateral geniculate nucleus. J Neurosci 25: 10844-10856, 2005. Carandini M. Amplification of trial-to-trial response variability by neurons in visual cortex. PLoS Biol 2: E264, 2004. Carandini M and Heeger DJ. Summation and division by neurons in primate visual cortex. Science 264: 1333-1336, 1994. Carandini M, Heeger DJ, and Movshon JA. Linearity and normalization in simple cells of the macaque primary visual cortex. J Neurosci 17: 8621-8644, 1997. Chander D and Chichilnisky EJ. Adaptation to temporal contrast in primate and salamander retina. J Neurosci 21: 9904-9916, 2001. Chichilnisky EJ. A simple white noise analysis of neuronal light responses. Network 12: 199-213, 2001. Contreras D and Palmer L. Response to contrast of electrophysiologically defined cell classes in primary visual cortex. J Neurosci 23: 6936-6945, 2003. DeAngelis GC, Ohzawa I, and Freeman RD. Spatiotemporal organization of simplecell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. DeAngelis GC, Robson JG, Ohzawa I, and Freeman RD. Organization of suppression in receptive fields of neurons in cat visual cortex. J Neurophysiol 68: 144-163, 1992. Freeman TC, Durand S, Kiper DC, and Carandini M. Suppression without inhibition in visual cortex. Neuron 35: 759-771, 2002. Gardner JL, Anzai A, Ohzawa I, and Freeman RD. Linear and nonlinear contributions to orientation tuning of simple cells in the cat's striate cortex. Vis Neurosci 16: 1115-1121, 1999. Li B, Thompson JK, Duong T, Peterson MR, and Freeman RD. Origins of crossorientation suppression in the visual cortex. J Neurophysiol 96: 1755-1764, 2006. Mante V, Frazor RA, Bonin V, Geisler WS, and Carandini M. Independence of luminance and contrast in natural scenes and in the early visual system. Nat Neurosci 8: 1690-1697, 2005. Miller KD and Troyer TW. Neural noise can explain expansive, power-law nonlinearities in neural response functions. J Neurophysiol 87: 653-659, 2002. Naka KI and Rushton WA. S-potentials from luminosity units in the retina of fish (Cyprinidae). J Physiol 185: 587-599, 1966. Nykamp DQ and Ringach DL. Full identification of a linear-nonlinear system via crosscorrelation analysis. J Vis 2: 1-11, 2002. Priebe NJ and Ferster D. Mechanisms underlying cross-orientation suppression in cat visual cortex. Nat Neurosci 9: 552-561, 2006. Reid RC, Victor JD, and Shapley RM. The use of m-sequences in the analysis of visual neurons: linear receptive field properties.
Brain Research, 1983
Key words: X and Y cells --dorsolateral geniculate nucleus --centre surround antagonism --GABA --inhibitory processes Visually elicited inhibitory processes, underlying the receptive field structure of cells in layers A and A 1 of the cat dorsal lateral geniculate nucleus (dLGN), have been examined by a combination of visual neurophysiological and iontophoretic techniques. Discrete visual stimulation of both centre and surround mechanisms, produced a powerful suppression of the elevated background discharge levels induced by iontophoretic application of an excitatory amino acid. These observations are consistent with the activation of a postsynaptic inhibitory input, a view supported by the fact that the suppressive effects were blocked by iontophoretic application of bicuculline, an antagonist of GABA, a putative inhibitory transmitter in the dLGN. These inhibitory effects were always elicited by the opposite phase of a flashed stimulus to that eliciting responses associated with the receptive field region. That is 'on' inhibitory effects were elicited from 'off' excitatory regions and 'off' inhibitory effects from 'on' excitatory regions.