Spike timing and visual processing in the retinogeniculocortical pathway

Although the visual response properties of neurons along the retinogeniculocortical pathway have been studied for decades, relatively few studies have examined how individual neurons along the pathway communicate with each other. Recent studies in the cat (Felis domestica) now show that the strength of these connections is very dynamic and spike timing plays an important part in determining whether action potentials will be transferred from pre- to postsynaptic cells. This review explores recent progress in our understanding of what role spike timing has in establishing different patterns of geniculate activity and how these patterns ultimately drive the cortex.     

The human visual system is optimised for processing the spatial information in natural visual images

A fundamental tenet of visual science is that the detailed properties of visual systems are not capricious accidents, but are closely matched by evolution and neonatal experience to the environments and lifestyles in which those visual systems must work. This has been shown most convincingly for fish and insects. For mammalian vision, however, this tenet is based more upon theoretical arguments than upon direct observations. Here, we describe experiments that require human observers to discriminate between pictures of slightly different faces or objects. These are produced by a morphing technique that allows small, quantifiable changes to be made in the stimulus images. The independent variable is designed to give increasing deviation from natural visual scenes, and is a measure of the Fourier composition of the image (its second-order statistics). Performance in these tests was best when the pictures had natural second-order spatial statistics, and degraded when the images were made less natural. Furthermore, performance can be explained with a simple model of contrast coding, based upon the properties of simple cells in the mammalian visual cortex. The findings thus provide direct empirical support for the notion that human spatial vision is optimised to the second-order statistics of the optical environment.     

Retinotopic mapping of categorical and coordinate spatial relation processing in early visual cortex

Spatial relations are commonly divided in two global classes. Categorical relations concern abstract relations which define areas of spatial equivalence, whereas coordinate relations are metric and concern exact distances. Categorical and coordinate relation processing are thought to rely on at least partially separate neurocognitive mechanisms, as reflected by differential lateralization patterns, in particular in the parietal cortex. In this study we address this textbook principle from a new angle. We studied retinotopic activation in early visual cortex, as a reflection of attentional distribution, in a spatial working memory task with either a categorical or a coordinate instruction. Participants were asked to memorize a dot position, with regard to a central cross, and to indicate whether a subsequent dot position matched the first dot position, either categorically (opposite quadrant of the cross) or coordinately (same distance to the centre of the cross). BOLD responses across the retinotopic maps of V1, V2, and V3 indicate that the spatial distribution of cortical activity was different for categorical and coordinate instructions throughout the retention interval; a more local focus was found during categorical processing, whereas focus was more global for coordinate processing. This effect was strongest for V3, approached significance in V2 and was absent in V1. Furthermore, during stimulus presentation the two instructions led to different levels of activation in V3 during stimulus encoding; a stronger increase in activity was found for categorical processing. Together this is the first demonstration that instructions for specific types of spatial relations may yield distinct attentional patterns which are already reflected in activity early in the visual cortex.     

Simultaneous processing of spatial and chromatic components of patterned stimuli by the human visual system

We report measurements on discrimination of orientation and magnification made for elements differentiated in colour and/or luminance from their background. By performing measurements at a series of background luminances and for fixed luminance of the elements, we show that with colour contrast, discrimination for both spatial parameters is unimpaired when the background is at isoluminance with the elements. Under simple luminance contrast, however, these discriminations become poorer when the background luminance is within some +/- 5% of that of the elements, and are completely absent when the two values are the same. A deuteranomalous subject is unable to make the spatial discrimination around the isoluminance point for colour contrasts which are too small for him to distinguish, but for which subjects with normal colour vision maintain spatial discriminations at isoluminance. This observation establishes that the physiological mechanisms of normal colour vision, rather than stimulus artefacts, mediate the observed spatial discriminations. We conclude that the visual processing of colour and spatial parameters such as orientation and magnification are intrinsically related to each other.     

Laminar processing in the visual cortical column

Sensory regions of neocortex are organized as arrays of vertical columns composed of cells that share similar response properties, with the orientation columns of the cat's visual cortex being the best known example. Interest in how sensitivity to different stimulus features first emerges in the columns and how this selectivity is refined by subsequent processing has fueled decades of research. A natural starting point in approaching these issues is anatomy. Each column traverses the six cortical layers and each layer has a unique pattern of inputs, intrinsic connections and outputs. Thus, it makes sense to explore the possibility of corresponding laminar differences in sensory function, that is, to examine relationships between morphology and physiology. In addition, to help identify general patterns of cortical organization, it is useful to compare results obtained from different sensory systems and diverse species. The picture that emerges from such comparisons is that each cortical layer serves a distinct role in sensory function. Furthermore, different cortices appear to share some common strategies for processing information but also have specialized mechanisms adapted for the demands of specific sensory tasks.     

Plant N-glycan processing enzymes employ different targeting mechanisms for their spatial arrangement along the secretory pathway

The processing of N-linked oligosaccharides in the secretory pathway requires the sequential action of a number of glycosidases and glycosyltransferases. We studied the spatial distribution of several type II membrane-bound enzymes from Glycine max, Arabidopsis thaliana, and Nicotiana tabacum. Glucosidase I (GCSI) localized to the endoplasmic reticulum (ER), alpha-1,2 mannosidase I (ManI) and N-acetylglucosaminyltransferase I (GNTI) both targeted to the ER and Golgi, and beta-1,2 xylosyltransferase localized exclusively to Golgi stacks, corresponding to the order of expected function. ManI deletion constructs revealed that the ManI transmembrane domain (TMD) contains all necessary targeting information. Likewise, GNTI truncations showed that this could apply to other type II enzymes. A green fluorescent protein chimera with ManI TMD, lengthened by duplicating its last seven amino acids, localized exclusively to the Golgi and colocalized with a trans-Golgi marker (ST52-mRFP), suggesting roles for protein-lipid interactions in ManI targeting. However, the TMD lengths of other plant glycosylation enzymes indicate that this mechanism cannot apply to all enzymes in the pathway. In fact, removal of the first 11 amino acids of the GCSI cytoplasmic tail resulted in relocalization from the ER to the Golgi, suggesting a targeting mechanism relying on protein-protein interactions. We conclude that the localization of N-glycan processing enzymes corresponds to an assembly line in the early secretory pathway and depends on both TMD length and signals in the cytoplasmic tail.     

Binocular visual processing in the owl's telencephalon.

Single neurons recorded from the owl's visual Wulst are surprisingly similar to those found in mammalian striate cortex. The receptive fields of Wulst neurons are elaborated, in an apparently hierarchical fashion, from those of their monocular, concentrically organized inputs to produce binocular interneurons with increasingly sophisticated requirements for stimulus orientation, movement and binocular disparity. Output neurons located in the superficial laminae of the Wulst are the most sophisticated of all, with absolute requirements for a combination of stimuli, which include binocular presentation at a particular horizontal binocular disparity, and with no response unless all of the stimulus conditions are satisfied simultaneously. Such neurons have the properties required for 'global stereopsis', including a receptive field size many times larger than their optimal stimulus, which is more closely matched to the receptive fields of the simpler, disparity-selective interneurons. These marked similarities in functional organization between the avian and mammalian systems exist in spite of a number of structural differences which reflect their separate evoluntionary origins. Discussion therefore includes the possibility that there may exist for nervous systems only a very small number of possible solutions, perhaps a unique one, to the problem of stereopsis.     

Flexibility of spatial averaging in visual perception

The classical receptive field (RF) concept-the idea that a visual neuron responds to fixed parts and properties of a stimulus-has been challenged by a series of recent physiological results. Here, we extend these findings to human vision, demonstrating that the extent of spatial averaging in contrast perception is also flexible, depending strongly on stimulus contrast and uniformity. At low contrast, spatial averaging is greatest (about 11 min of arc) within uniform regions such as edges, as expected if the relevant neurons have orientation-selective RFs. At high contrast, spatial averaging is minimal. These results can be understood if the visual system is balancing a trade-off between noise reduction, which favours large areas of averaging, and detail preservation, which favours minimal averaging. Two distinct populations of neurons with hard-wired RFs could account for our results, as could the more intriguing possibility of dynamic, contrast-dependent RFs.     

Profound contrast adaptation early in the visual pathway

Prior exposure to a moving grating of high contrast led to a substantial and persistent reduction in the contrast sensitivity of neurons in the lateral geniculate nucleus (LGN) of macaque. This slow contrast adaptation was potent in all magnocellular (M) cells but essentially absent in parvocellular (P) cells and neurons that received input from S cones. Simultaneous recordings of M cells and the potentials of ganglion cells driving them showed that adaptation originated in ganglion cells. As expected from the spatiotemporal tuning of M cells, adaptation was broadly tuned for spatial frequency and lacked orientation selectivity. Adaptation could be induced by high temporal frequencies to which cortical neurons do not respond, but not by low temporal frequencies that can strongly adapt cortical neurons. Our observations confirm that contrast adaptation occurs at multiple levels in the visual system, and they provide a new way to reveal the function and perceptual significance of the M pathway.     

Melanopsin regulates visual processing in the mouse retina

The discovery of melanopsin-dependent inner retinal photoreceptors in mammals has precipitated a fundamental reassessment of such non-image forming (NIF) light responses as circadian photoentrainment and the pupil light reflex. By contrast, it remains unclear whether these new photoreceptors also play a role in classical image-forming vision. The retinal ganglion cells that subserve inner retinal photoreception (ipRGCs) project overwhelmingly to brain areas involved in NIF responses, indicating that, in terms of central signaling, their predominant function is non-image forming. However, ipRGCs also exhibit intraretinal communication via gap junction coupling, which could allow them to modulate classical visual pathways within this tissue. Here, we explore this second possibility by using melanopsin knockout (Opn4-/-) mice to examine the role of inner retinal photoreceptors in diurnal regulation of retinal function. By using electroretinography in wild-type mice, we describe diurnal rhythms in both the amplitude and speed of the retinal cone pathway that are a function of both prior light exposure and circadian phase. Unexpectedly, loss of the melanopsin gene abolishes circadian control of these parameters, causing significant attenuation of the diurnal variation in cone vision. Our results demonstrate for the first time a melanopsin-dependent regulation of visual processing within the retina, revealing an important function for inner retinal photoreceptors in optimizing classical visual pathways according to time of day.     

Molecular guidance cues in the development of visual pathway

70%–80% of our sensory input comes from vision. Light hit the retina at the back of our eyes and the visual information is relayed into the dorsal lateral geniculate nuclei (dLGN) and primary visual cortex (V1) thereafter, constituting the image-forming visual circuit. Molecular cues are one of the key factors to guide the wiring and refinement of the image-forming visual circuit during pre- and post-embryonic stages. Distinct molecular cues are involved in different developmental stages and nucleus, suggesting diverse guidance mechanisms. In this review, we summarize molecular guidance cues throughout the image-forming visual circuit, including chiasm determination, eye-specific segregation and refinement in the dLGN, and at last the reciprocal connections between the dLGN and V1.     

Spatiotemporal inseparability in early visual processing

We examine the implications of significant inseparable behaviour in centre-surround retinal cell types. From the form of a spatiotemporal centre-surround (CS) model which agrees qualitatively with physiological observations, we find that the sustained/transient dichotomy is a poor distinction for X-type/Y-type retinal ganglion cells since both exhibit inseparability. Static centre-surround models and spatiotemporal separable models are not valid for time-varying stimuli. Our results contradict the models for X- and Y-type ganglion cells proposed by Marr and Hildreth (1980) and Marr and Ullman (1981), and raise doubts about the physiological validity of Marr's zerocrossing theory. The CS filter is an attractive precursor to the extraction of 2-d motion information.     

The role of attention in visual processing

Attention to a visual stimulus typically increases the responses of cortical neurons to that stimulus. Because many studies have shown a close relationship between the performance of individual neurons and behavioural performance of animal subjects, it is important to consider how attention affects this relationship. Measurements of behavioural and neuronal performance taken from rhesus monkeys while they performed a motion detection task with two attentional states show that attention alters the relationship between behaviour and neuronal response. Notably, attention affects the relationship differently in different cortical visual areas. This indicates that a close relationship between neuronal and behavioural performance on a given task persists over changes in attentional state only within limited regions of visual cortex.