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Suppression outside the classical cortical receptive field.

The important visual stimulus parameters for a given cell are defined by the classical receptive field (CRF). However, cells are also influenced by visual stimuli presented in areas surrounding the CRF. The experiments described here were conducted to determine the incidence and nature of CRF surround influences in the primary visual cortex. From extracellular recordings in the cat's striate cortex, we find that for over half of the cells investigated (56%, 153/271), the effect of stimulation in the surround of the CRF is to suppress the neuron's activity by at least 10% compared to the response to a grating presented within the CRF alone. For the remainder of the cells, the interactions were minimal and a few were of a facilitatory nature. In this paper, we focus on the suppressive interactions. Simple and complex cell types exhibit equal incidences of surround suppression. Suppression is observed for cells in all layers, and its degree is strongly correlated between the two eyes for binocular neurons. These results show that surround suppression is a prevalent form of inhibition and may play an important role in visual processing.

Animals↗

Transneuronal retrograde transport of attenuated pseudorabies viruses within central visual pathways.

Pseudorabies virus (PRV) has been shown to be an effective transneuronal tracer within both the peripheral and the central nervous system. The only investigations of this virus in the visual system have examined anterograde transport of PRV from injection sites in the retina. In the present study, we injected attenuated forms of PRV into the primary visual cortex of both rats and cats to determine whether transneuronal retrograde infection would occur back to the retina. In rats, we made small injections into visual cortex of a strain of PRV (Bartha Blu) that contained a beta-galactosidase promoter insert. In cats, we injected PRV-M201 into area V1 of visual cortex. After a 2- to 4-day incubation period, we examined tissue from these animals for the presence of the beta-galactosidase marker (rats) or the virus itself (cats). Cortical PRV injections resulted in transneuronal retrograde infection of the lateral geniculate nucleus (LGN), thalamic reticular nucleus (TRN), and retina. PRV was retinotopically distributed in the pathway. In addition, double-labeling experiments in cats using an antibody against gamma-aminobutyric acid (GABA) were conducted to reveal PRV-labeled interneurons within the LGN and TRN. All TRN neurons were GABA+, as was a subset of LGN neurons. Only the subset of TRN neurons adjacent to the PRV-labeled sector of LGN was labeled with PRV. In addition, a subset of GABA+ interneurons in LGN was also labeled with PRV. We processed some tissue for electron microscopy to examine the morphology of the virus at various replication stages. No mature virions were detected in terminals from efferent pathways, although forms consistent with retrograde infection were encountered. We conclude that the PRV strains we have used produce a local infection that progresses primarily in the retrograde direction in the central visual pathways. The infection is transneuronal and viral replication maintains the intensity of the label throughout the chain of connected neurons, providing a means of examining detailed circuitry within the visual pathway.

Animals↗

Effects of surround motion on receptive-field gain and structure in area 17 of the cat.

Modulation of responses elicited by moving bars within the classical receptive fields (CRF) of cat area 17 neurons were studied as a function of the direction and velocity of drifting gratings in the surrounds. Several different types of modulation were observed; collectively, the responses of most cells, both simple and complex, were strongly modulated by surround motion. None of these cells appear to signal relative velocity between the CRF and its surround. The gain and spatiotemporal structure of the CRF mechanism were estimated using contrast-response functions and reverse correlation with spatiotemporal ternary white noise, respectively. These measurements were made in the presence of surround gratings shown to significantly modify responses elicited from the CRF. In all cases, the gain of the CRF mechanism was driven up or down relative to controls but the receptive-field structure did not change in any way. We conclude that neurons in cat area 17 act like scalable filters, meaning that their gains can be adjusted by stimuli in the surrounds without altering the properties of the CRF. This was verified by showing that velocity tuning curves were also unmodified by stimuli in the surround that did change the gain. Based in part on these data, we discuss the notion that primary visual cortex makes use of a double-opponent mechanism for the representation of local discontinuities in motion and orientation.

Animals↗

A simple model accounts for the response of disparity-tuned V1 neurons to anticorrelated images.

Disparity-tuned cells in primary visual cortex (VI) are thought to play a significant role in the processing of stereoscopic depth. The disparity-specific responses of these neurons have been previously described by an energy model based on local, feedforward interactions. This model fails to predict the response to binocularly anticorrelated stimuli, in which images presented to left and right eyes have opposite contrasts. The original energy model predicts that anticorrelation should invert the disparity tuning curve (phase difference pi), with no change in the amplitude of the response. Experimentally, the amplitude tends to be reduced with anticorrelated stimuli and a spread of phase differences is observed, although phase differences near pi are the most common. These experimental observations could potentially reflect a modulation of the V1 signals by feedback from higher visual areas (because anticorrelated stimuli create a weaker or nonexistent stereoscopic depth sensation). This hypothesis could explain the effects on amplitude, but the spread of phase differences is harder to understand. Here, we demonstrate that changes in both amplitude and phase can be explained by a straightforward modification of the energy model that involves only local processing. Input from each eye is passed through a monocular simple cell, incorporating a threshold, before being combined at a binocular simple cell that feeds into the energy computation. Since this local feedforward model can explain the responses of complex cells to both correlated and anticorrelated stimuli, there is no need to invoke any influence of global stereoscopic matching.

Animals↗

Artificial scotoma-induced perceptual distortions are orientation dependent and short lived.

Conditioning human observers with an "artificial scotoma"-a small retinal area deprived of patterned stimulation within a larger area of dynamically textured noise-results in contractions and expansions of perceived space that are thought to reflect receptive-field changes among cells in the primary visual cortex (Kapadia et al., 1994). Here we show that one-dimensional counter-phase flickering grating patterns are also potent stimuli for producing artificial scotomata capable of altering three-element bisection ability analogous to those results reported earlier. Moreover, we found that the magnitude of the induced spatial distortions depends critically on the relative orientations of peri-scotomatous and test-stimulus spatial contrast. In addition, the perceptual distortions are found to be relatively short lived, decaying within 660 ms. The results support the hypothesis that artificial scotoma-induced perceptual distortions are generated by dynamic alteration of connection efficacy within a network linking cortical areas of similar orientation specificity, consistent with established anatomical and physiological results.

Humans↗

Decorrelation of neural activity during fixational instability: possible implications for the refinement of V1 receptive fields.

Early in life, visual experience appears to influence the refinement and maintenance of the orientation-selective responses of neurons in the primary visual cortex. After eye opening, the statistical structure of visually driven neural responses depends not only on the stimulus, but also on how the stimulus is scanned during behavior. Modulations of neural activity due to behavior may thus play a role in the experience-dependent refinement of cell response characteristics. To investigate the possible influences of eye movements on the maturation of thalamocortical connectivity, we have simulated the responses of neuronal populations in the lateral geniculate nucleus (LGN) and V1 of the cat while images of natural scenes were scanned in a way that replicated the cat's oculomotor activity. In the model, fixational eye movements were essential to attenuate neural sensitivity to the broad correlational structure of natural visual input, decorrelate neural responses, and establish a regime of neural activity that was compatible with a Hebbian segregation of geniculate afferents to the cortex. We show that this result is highly robust and does not depend on the precise characteristics of the model.

Animals↗

Telencephalic projections to the nucleus of the basal optic root and pretectal nucleus lentiformis mesencephali in pigeons.

In birds, the nucleus of the basal optic root (nBOR) of the accessory optic system (AOS) and the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow and the generation of the optokinetic response. In several species, it has been shown that the AOS and pretectum receive input from visual areas of the telencephalon. Previous studies in pigeons using anterograde tracers have shown that both nBOR and LM receive input from the visual Wulst, the putative homolog of mammalian primary visual cortex. In the present study, we used retrograde and anterograde tracing techniques to further characterize these projections in pigeons. After injections of the retrograde tracer cholera toxin subunit B (CTB) into either LM or nBOR, retrograde labeling in the telencephalon was restricted to the hyperpallium apicale (HA) of the Wulst. From the LM injections, retrograde labeling appeared as a discrete band of cells restricted to the lateral edge of HA. From the nBOR injections, the retrograde labeling was more distributed in HA, generally dorsal and dorso-medial to the LM-projecting neurons. In the anterograde experiments, biotinylated dextran amine (BDA) was injected into HA and individual axons were reconstructed to terminal fields in the LM and nBOR. Those fibers projecting to the nBOR also innervated the adjacent ventral tegmental area. However, tracing of BDA-labeled axons revealed no evidence that individual neurons project to both LM and nBOR. In summary, our results suggest that the nBOR and LM receive input from different areas of the Wulst. We discuss how these projections may transmit visual and/or somatosensory information to the nBOR and LM.

Animals↗

Spatial coding and response redundancy in parallel visual pathways of the marmoset Callithrix jacchus.

Many neurons in the primary visual cortex (area V1) show pronounced selectivity for the orientation and spatial frequency of visual stimuli, whereas most neurons in subcortical afferent streams show little selectivity for these stimulus attributes. It has been suggested that this transformation is a functional sign of increased coding efficiency, whereby the redundancy (or overlap in response properties) is reduced at consecutive levels of visual processing. Here we compared experimentally the response redundancy in area V1 with that in the three main dorsal thalamic afferent streams, the parvocellular (PC), koniocellular (KC), and magnocellular (MC) divisions of the dorsal lateral geniculate nucleus (LGN) in marmosets. The spatial frequency and orientation tuning of single cells in the LGN and area V1 were measured, using luminance contrast sine-wave gratings. A joint spatial frequency-orientation response selectivity profile was calculated for each cell. Response redundancy for each population was estimated by cross-multiplication of the joint selectivity profiles for pairs of cells. We show that when estimated in this way, redundancy in LGN neurons is approximately double that of neurons in cortical area V1. However, there are differences between LGN subdivisions, such that the KC pathway has a spatial representation that lies between the redundant code of the PC and MC pathways and the more efficient sparse spatial code of area V1.

Action Potentials↗

The squirrel as a rodent model of the human visual system.

Over the last 50 years, studies of receptive fields in the early mammalian visual system have identified many classes of response properties in brain areas such as retina, lateral geniculate nucleus (LGN), and primary visual cortex (V1). Recently, there has been significant interest in understanding the cellular and network mechanisms that underlie these visual responses and their functional architecture. Small mammals like rodents offer many advantages for such studies, because they are appropriate for a wide variety of experimental techniques. However, the traditional rodent models, mice and rats, do not rely heavily on vision and have small visual brain areas. Squirrels are highly visual rodents that may be excellent model preparations for understanding mechanisms of function and disease in the human visual system. They use vision for navigating in their environment, predator avoidance, and foraging for food. Visual brain areas such as LGN, V1, superior colliculus, and pulvinar are particularly large and well elaborated in the squirrel, and the squirrel has several extrastriate cortical areas lateral to V1. Unlike many mammals, most squirrel species are diurnal with cone-dominated retinas, similar to the primate fovea, and have excellent dichromatic color vision that is mediated by green and blue cones. Owing to their larger size, squirrels are physiologically more robust than mice and rats under anesthesia, and some hibernating species are particularly tolerant of hypoxia that occurs during procedures such as brain slicing. Finally, many basic anatomical and physiological properties in the early visual system of squirrel have now been described, permitting investigations of cellular mechanisms. In this article, we review four decades of anatomical, behavioral, and physiological studies in squirrel and make comparisons with other species.

Animals↗

Vision in mice with neuronal redundancy due to inhibition of developmental cell death.

Transgenic mice overexpressing bcl-2, due to inhibition of naturally occurring cell death, have much larger brains and optic nerves as compared to wild-type mice. Since developmental cell death is believed to exert a crucial role in establishing the mature neural circuitry and function, we asked the question of whether basic aspects of vision were altered in bcl-2 mice. Local visually evoked potentials (VEPs) in response to patterned stimuli were recorded from the primary visual cortex. The representation of the vertical meridian was displaced by about 15% in the bcl-2 mouse, accounting for brain expansion. However, visual acuity, contrast threshold, and response latency were normal, indicating that compensatory mechanisms can ensure normal basic properties of vision in spite of marked neuronal redundancy.

Animals↗

Mechanism of binocular interaction in refraction errors: study using pattern-reversal visual evoked potentials.

In this study we sought to determine whether a natural condition involving fine discrimination, for example moderately severe myopia, might yield interesting information regarding the binocular interaction expressed by visual evoked potentials (VEPs). We studied ten normal subjects with a mild refraction deficits. Transient VEPs were elicited by monocular and binocular stimulation under conditions of natural and lens-corrected vision. The visual stimulus was a pattern-reversal checkerboard consisting of 15' and 40' checks. VEPs in response to binocular stimulation were compared with monocular VEPs. We plotted the monocular 'better-VEP' and 'worse-VEP' response, since significant differences between individual eye stimulations were present. We found no significant difference between the mean N75 and P100 latencies of the binocular VEP and the better monocular VEP, regardless of the check size used and of natural or corrected vision. Under all stimulus conditions, the mean amplitude of the N75-P100 of the binocular VEPs was also larger than the better monocular VEP response. The difference proved more significant when we stimulated our subjects with smaller squares and left vision uncorrected. The mean P100-N145 amplitude obtained with binocular stimulation was larger than the better monocular VEP response only when using small checks (15') and uncorrected vision. Overlapping latencies are consistent with an earlier hypothesis that monocular and binocular VEPs originate postsynaptically from the binocular neurons in the primary visual cortex. The gain in amplitude achieved by binocular stimulation may depend upon the removal of 'tonic interocular inhibition' and/or on a cortical modulatory mechanism.

Adult↗

Traveling waves and the processing of weakly tuned inputs in a cortical network module.

Recent studies have shown that local cortical feedback can have an important effect on the response of neurons in primary visual cortex to the orientation of visual stimuli. In this work, we study the role of the cortical feedback in shaping the spatiotemporal patterns of activity in cortex. Two questions are addressed: one, what are the limitations on the ability of cortical neurons to lock their activity to rotating oriented stimuli within a single receptive field? Two, can the local architecture of visual cortex lead to the generation of spontaneous traveling pulses of activity? We study these issues analytically by a population-dynamic model of a hypercolumn in visual cortex. The order parameter that describes the macroscopic behavior of the network is the time-dependent population vector of the network. We first study the network dynamics under the influence of a weakly tuned input that slowly rotates within the receptive field. We show that if the cortical interactions have strong spatial modulation, the network generates a sharply tuned activity profile that propagates across the hypercolumn in a path that is completely locked to the stimulus rotation. The resultant rotating population vector maintains a constant angular lag relative to the stimulus, the magnitude of which grows with the stimulus rotation frequency. Beyond a critical frequency the population vector does not lock to the stimulus but executes a queasi-periodic motion with an average frequency that is smaller than that of the stimulus. In the second part we consider the stable intrinsic state of the cortex under the influence of isotropic stimulation. We show that if the local inhibitory feedback is sufficiently strong, the network does not settle into a stationary state but develops spontaneous traveling pulses of activity. Unlike recent models of wave propagation in cortical networks, the connectivity pattern in our model is spatially symmetric, hence the direction of propagation of these waves is arbitrary. The interaction of these waves with an external-oriented stimulus is studied. It is shown that the system can lock to a weakly tuned rotating stimulus if the stimulus frequency is close to the frequency of the intrinsic wave.

Animals↗

Electrophysiology of the postreceptoral visual pathway in mice.

Pattern VEPs have been recorded locally from the binocular portion of the primary visual cortex of wild type- and different transgenic mice by means of microelectrodes. Local pattern VEPs have been used on the one hand to obtain information on basic cortical layout (topography, laminar analysis) and ocularity (relative contribution of the contralateral and ipsilateral eye), and on the other hand to evaluate several aspects of visual physiology that have a counterpart in visual behavior (visual acuity, contrast sensitivity, motion sensitivity, response latency). As compared to visual behavior, pattern VEPs offer the advantage that several aspects of vision can be evaluated in the same animals, including those with poor behavior due to motor- or cognitive deficits, even during the postnatal development. Pattern VEPs provide a means for characterizing the visual phenotype of mutant mice and for the evaluation of the effects induced by experimental manipulation.

Animals↗

A model-based approach for the analysis of neuronal information transmission in multi-input and -output systems.

We present a new method to characterize multi-input and output neuronal systems using information theory. To obtain a lower bound of transinformation we take three steps: (1) Estimation of the deterministic response to isolate components carrying stimulus information. The deviation of the original response from the deterministic estimate is defined as noise. (2) Coordinate transformation using PCA yields an uncorrelated representation. (3) Partial transinformation values are calculated independently either by Shannon's formula assuming normality or based on density estimation for arbitrary distributions. We investigate the performance of the algorithms using simulated data and discuss suitable parameter settings. The approach allows to evaluate the degree to which stimulus features are encoded. Its potential is illustrated by analyses of neuronal activity in cat primary visual cortex evoked by electrical retina stimulation.

Action Potentials↗

Spike-based synaptic plasticity and the emergence of direction selective simple cells: simulation results.

Direction selectivity (DS) of simple cells in the primary visual cortex was recently suggested to arise from short-term synaptic depression in thalamocortical afferents (Chance F, Nelson S, Abbott L (1998), J. Neuroscience 18(12): 4785-4799). In the model, two groups of afferents with spatially displaced receptive fields project through either depressing and non-depressing synapses onto the V1 cell. The degree of synaptic depression determines the temporal phase advance of the response to drifting gratings. We show that the spatial displacement and the appropriate degree of synaptic depression required for DS can develop within an unbiased input scenario by means of temporally asymmetric spike-timing dependent plasticity (STDP) which modifies both the synaptic strength and the degree of synaptic depression. Moving stimuli of random velocities and directions break any initial receptive field symmetry and produce DS. Frequency tuning curves and subthreshold membrane potentials akin to those measured for non-directional simple cells are thereby changed into those measured for directional cells. If STDP is such that down-regulation dominates up-regulation the overall synaptic strength adapts in a self-organizing way such that eventually the postsynaptic response for the non-preferred direction becomes subthreshold. To prevent unlearning of the acquired DS by randomly changing stimulus directions an additional learning threshold is necessary. To further protect the development of the simple cell properties against noise in the stimulus, asynchronous and irregular synaptic inputs are required.

Afferent Pathways↗

One axon-multiple functions: specificity of lateral inhibitory connections by large basket cells.

The functional specificity of the projections of single large basket cells of the cat primary visual cortex was studied using novel analytical approaches. The distribution of the labelled axons and that of the target cells were three-dimensionally reconstructed and compared quantitatively to orientation, direction and ocular dominance maps obtained with the intrinsic signal optical imaging technique. Quantitative analysis was carried out (i) for the entire basket cell, (ii) separately, for local and distal projections of the axon and (iii) by dissecting the same axon into two projection fields at the first bifurcation. It was found that although the functional distributions (orientation, direction and ocular dominance) for the entire cell were multi-modal and broadly tuned, individual main branches of the same cell displayed highly specific topography. In the further analysis, 2-dimensional probability density estimates of the target cell distributions revealed clear clustering which may be important for local subfield antagonism. These findings provide support to the idea that the same basket cell mediates several specific receptive field operations depending on the location of the target somata in the functional maps.

Animals↗

Resolving ability and image discretization in the visual system.

Psychophysiological studies were performed to measure the spatial threshold for resolution of two "points" and the thresholds for discriminating their orientations depending on the distance between the two points. Data were compared with the scattering of the "point" by the eye's optics, the packing density of cones in the fovea, and the characteristics of the receptive fields of ganglion cells in the foveal area of the retina and neurons in the corresponding projection zones of the primary visual cortex. The effective zone was shown to have to contain a scattering function for several receptors, as this allowed preliminary blurring of the image by the eye's optics to decrease the subsequent (at the level of receptors) discretization noise created by a matrix of receptors. The concordance of these parameters supports the optical operation of the spatial elements of the neural network determining the resolving ability of the visual system at different levels of visual information processing. It is suggested that the special geometry of the receptive fields of neurons in the striate cortex, which are concordant with the statistics of natural scenes, results in a further increase in the signal:noise ratio.

Adult↗

Decision processes in visual discrimination of line orientation.

The contribution of decision factors to the meridional variations in line orientation discrimination was determined for two-alternative forced-choice experimental designs. Using Johnson's (1980) formalization of decision processes in discrimination tasks, we identified three decision factors: the decision rule, memory variance, and criterial noise. In a first experiment, we showed the effect of experimental design on orientation discrimination to be similar at horizontal and oblique standard orientations, indicating that the meridional variations in orientation discrimination were not due to a decision rule anisotropy. In a second experiment, the effect of the interstimulus interval was also found to be similar at both standard orientations, suggesting that the memory variance is isotropic in the orientation domain. The results of two other experiments supported the hypothesis that the meridional variations in orientation discrimination are not due to a criterial noise anisotropy. These different results strongly suggested that the oblique effect in line orientation discrimination is due to sensorial factors rather than to decision factors. Therefore, they further support the hypothesis linking the anisotropy of the preferred orientation distribution of Area 17-S cells (a single physiologically defined class of cells in the primary visual cortex) and the meridional variations in line orientation discrimination.

Adult↗

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