A retinal source of spatial contrast gain control

Sensory cortex is able to encode a broad range of stimulus features despite a great variation in signal strength. In cat primary visual cortex (V1), for example, neurons are able to extract stimulus features like orientation or spatial configuration over a wide range of stimulus contrasts. The contrast-invariant spatial tuning found in V1 neuron responses has been modeled as a gain control mechanism, but at which stage of the visual pathway it emerges has remained unclear. Here we describe our findings that contrast-invariant spatial tuning occurs not only in the responses of lateral geniculate nucleus (LGN) relay cells but also in their afferent retinal input. Our evidence suggests that a similar contrast-invariant mechanism is found throughout the stages of the early visual pathway, and that the contrast-invariant spatial selectivity is evident in both retinal ganglion cell and LGN cell responses.     

Contrast gain control and retinogeniculate communication

Visual information processed in the retina is transmitted to primary visual cortex via relay cells in the lateral geniculate nucleus (LGN) of the dorsal thalamus. Although retinal ganglion cells are the primary source of driving input to LGN neurons, not all retinal spikes are transmitted to the cortex. Here, we investigate the relationship between stimulus contrast and retinogeniculate communication and test the hypothesis that both the time course and strength of retinogeniculate interactions are dynamic and dependent on stimulus contrast. By simultaneously recording the spiking activity of synaptically connected retinal ganglion cells and LGN neurons in the cat, we show that the temporal window for retinogeniculate integration and the effectiveness of individual retinal spikes are inversely proportional to stimulus contrast. This finding provides a mechanistic understanding for the phenomenon of augmented contrast gain control in the LGN—a nonlinear receptive field property of LGN neurons whereby response gain during low‐contrast stimulation is enhanced relative to response gain during high‐contrast stimulation. In addition, these results support the view that network interactions beyond the retina play an essential role in transforming visual signals en route from retina to cortex.     

Binocular response modulation in the lateral geniculate nucleus

The dorsal lateral geniculate nucleus of the thalamus (LGN) receives the main outputs of both eyes and relays those signals to the visual cortex. Each retina projects to separate layers of the LGN so that each LGN neuron is innervated by a single eye. In line with this anatomical separation, visual responses of almost all of LGN neurons are driven by one eye only. Nonetheless, many LGN neurons are sensitive to what is shown to the other eye as their visual responses differ when both eyes are stimulated compared to when the driving eye is stimulated in isolation. This, predominantly suppressive, binocular modulation of LGN responses might suggest that the LGN is the first location in the primary visual pathway where the outputs from the two eyes interact. Indeed, the LGN features several anatomical structures that would allow for LGN neurons responding to one eye to modulate neurons that respond to the other eye. However, it is also possible that binocular response modulation in the LGN arises indirectly as the LGN also receives input from binocular visual structures. Here we review the extant literature on the effects of binocular stimulation on LGN spiking responses, highlighting findings from cats and primates, and evaluate the neural circuits that might mediate binocular response modulation in the LGN.     

Relation of koniocellular layers of dorsal lateral geniculate to inferior pulvinar nuclei in common marmosets

Traditionally, the dorsal lateral geniculate nucleus (LGN) and the inferior pulvinar (IPul) nucleus are considered as anatomically and functionally distinct thalamic nuclei. However, in several primate species it has also been established that the koniocellular (K) layers of LGN and parts of the IPul have a shared pattern of immunoreactivity for the calcium‐binding protein calbindin. These calbindin‐rich cells constitute a thalamic matrix system which is implicated in thalamocortical synchronisation. Further, the K layers and IPul are both involved in visual processing and have similar connections with retina and superior colliculus. Here, we confirmed the continuity between calbindin‐rich cells in LGN K layers and the central lateral division of IPul (IPulCL) in marmoset monkeys. By employing a high‐throughput neuronal tracing method, we found that both the K layers and IPulCL form comparable patterns of connections with striate and extrastriate cortices; these connections are largely different to those of the parvocellular and magnocellular laminae of LGN. Retrograde tracer‐labelled cells and anterograde tracer‐labelled axon terminals merged seamlessly from IPulCL into LGN K layers. These results support continuity between LGN K layers and IPulCL, providing an anatomical basis for functional congruity of this region of the dorsal thalamic matrix and calling into question the traditional segregation between LGN and the inferior pulvinar nucleus.     

Bio-inspired model of visual information encoding for localization: from the retina to the lateral geniculate nucleus

In this study, a bio-inspired approach for extracting efficient features prior to the recognition of scenes is proposed. It is highly inspired from the model of the mammals visual system. The retina contains many levels of neurons (bipolar, amacrine, horizontal and ganglion cells) accurately organized from cones and rods to the optic nerve up till the lateral geniculate nucleus (LGN) which is the main thalamic relay for inputs to the visual cortex. This structure probably eases other brain areas tasks in preprocessing the visual information. This paper is focusing on the study of these specific structures, relying on a bottom up approach to propose a comprehensive mathematical model of the low level image processing performed within the eye. The presented system takes into account the foveolar structure of the retina to produce a low-resolution representation of observed images by decomposing them into a local summation of elementary gaussian color histograms. This representation corresponds to the LGN biological organization. It has been thought that due to short timings, some very quick localization tasks involving particularly fast information processing pathways cannot be provided by the classical ones passing through higher level cortical areas. This work proposes a model of retinal coding and LGN-visual representation that we show provides reliable and sufficient early features for scenes recognition and localization. Experiments on real scenes using the developed model are presented showing the efficiency of the approach on localization.     

Color responses of the human lateral geniculate nucleus: [corrected] selective amplification of S-cone signals between the lateral geniculate nucleno and primary visual cortex measured with high-field fMRI

The lateral geniculate nucleus (LGN) is the primary thalamic nucleus that relays visual information from the retina to the primary visual cortex (V1) and has been extensively studied in non-human primates. A key feature of the LGN is the segregation of retinal inputs into different cellular layers characterized by their differential responses to red-green (RG) color (L/M opponent), blue-yellow (BY) color (S-cone opponent) and achromatic (Ach) contrast. In this study we use high-field functional magnetic resonance imaging (4 tesla, 3.6 x 3.6 x 3 mm(3)) to record simultaneously the responses of the human LGN and V1 to chromatic and Ach contrast to investigate the LGN responses to color, and how these are modified as information transfers between LGN and cortex. We find that the LGN has a robust response to RG color contrast, equal to or greater than the Ach response, but a significantly poorer sensitivity to BY contrast. In V1 at low temporal rates (2 Hz), however, the sensitivity of the BY color pathway is selectively enhanced, rising in relation to the RG and Ach responses. We find that this effect generalizes across different stimulus contrasts and spatial stimuli (1-d and 2-d patterns), but is selective for temporal frequency, as it is not found for stimuli at 8 Hz. While the mechanism of this cortical enhancement of BY color vision and its dynamic component is unknown, its role may be to compensate for a weak BY signal originating from the sparse distribution of neurons in the retina and LGN.     

Analysis of the lateral geniculate nucleus in dichromatic and trichromatic marmosets

Marmosets are diurnal New World monkeys that show sex‐linked cone photopigment polymorphism, whereby all males and some females are dichromats ("red‐green colorblind"), but most females show trichromatic color vision. Here we asked whether trichromats express chromatic‐specific circuitry in the lateral geniculate nucleus (LGN). The volume of parvocellular (P), magnocellular (M), and koniocellular (K) layers was calculated in Nissl‐stained sections from the LGN of adult marmosets (Callithrix jacchus; 10 trichromatic females; 2 dichromatic females; and 13 dichromatic males). Retinal ganglion cell axon terminals within the P and K layers were reconstructed and measured following anterograde tracer (dextran) injections. We show that there is little difference in LGN layer volume with respect to age, weight, or sex of the animals, or between dichromatic and trichromatic phenotypes. The morphology of retinal ganglion cell terminals was largely indistinguishable on comparing dichromats and trichromats, and likewise on comparing terminals representing peripheral or foveal retina. We conclude that the LGN circuits we studied are largely independent of red‐green color vision phenotype and visual field location. J. Comp. Neurol. 523:1948–1966, 2015 © 2015 Wiley Periodicals, Inc.     

N-acetylaspartylglutamate immunoreactivity in neurons of the cat's visual system

The acidic dipeptide, N-acetylaspartyglutamate (NAAG) was identified immunohistochemically within neurons of the cat's visual system. In the retina, NAAG-like immunoreactivity was observed in some horizontal and amacrine cells at the inner and outer margins of the bipolar cell layer. NAAG-like immunoreactivity was also observed in many retinal ganglion cell bodies, their neurites and the neuropil of their target areas, the lateral geniculate nucleus (LGN) and the superior colliculus. Additionally, peptide immunoreactivity was also seen in the projection neurons of the LGN, in cells of the pulvinar nucleus, and in the pyramidal cells of layers III and V in areas 17, 18 and 19 of the cerebral cortex. These data suggest that NAAG or a structurally related molecule may have a prominent role in the communication of visual signals at retinal, thalamic and cortical levels.     

The Amygdala Responds Rapidly to Flashes Linked to Direct Retinal Innervation: A Flash-evoked Potential Study Across Cortical and Subcortical Visual Pathways

Rapid detection and response to visual threats are critical for survival in animals. The amygdala (AMY) is hypothesized to be involved in this process, but how it interacts with the visual system to do this remains unclear. By recording flash-evoked potentials simultaneously from the superior colliculus (SC), lateral posterior nucleus of the thalamus, AMY, lateral geniculate nucleus (LGN) and visual cortex, which belong to the cortical and subcortical pathways for visual fear processing, we investigated the temporal relationship between these regions in visual processing in rats. A quick flash-evoked potential (FEP) component was identified in the AMY. This emerged as early as in the LGN and was approximately 25 ms prior to the earliest component recorded in the SC, which was assumed to be an important area in visual fear. This quick P1 component in the AMY was not affected by restraint stress or corticosterone injection, but was diminished by RU38486, a glucocorticoid receptor blocker. By injecting a monosynaptic retrograde AAV tracer into the AMY, we found that it received a direct projection from the retina. These results confirm the existence of a direct connection from the retina to the AMY, that the latency in the AMY to flashes is equivalent to that in the sensory thalamus, and that the response is modulated by glucocorticoids.     

Dorsal raphe nucleus projecting retinal ganglion cells: Why Y cells?

Retinal ganglion Y (alpha) cells are found in retinas ranging from frogs to mice to primates. The highly conserved nature of the large, fast conducting retinal Y cell is a testament to its fundamental task, although precisely what this task is remained ill-defined. The recent discovery that Y-alpha retinal ganglion cells send axon collaterals to the serotonergic dorsal raphe nucleus (DRN) in addition to the lateral geniculate nucleus (LGN), medial interlaminar nucleus (MIN), pretectum and the superior colliculus (SC) has offered new insights into the important survival tasks performed by these cells with highly branched axons. We propose that in addition to its role in visual perception, the Y-alpha retinal ganglion cell provides concurrent signals via axon collaterals to the DRN, the major source of serotonergic afferents to the forebrain, to dramatically inhibit 5-HT activity during orientation or alerting/escape responses, which dis-facilitates ongoing tonic motor activity while dis-inhibiting sensory information processing throughout the visual system. The new data provide a fresh view of these evolutionarily old retinal ganglion cells.     

Stimulus Contrast Affects Spatial Integration in the Lateral Geniculate Nucleus of Macaque Monkeys

Gain-control mechanisms adjust neuronal responses to accommodate the wide range of stimulus conditions in the natural environment. Contrast gain control and extraclassical surround suppression are two manifestations of gain control that govern the responses of neurons in the early visual system. Understanding how these two forms of gain control interact has important implications for the detection and discrimination of stimuli across a range of contrast conditions. Here, we report that stimulus contrast affects spatial integration in the lateral geniculate nucleus of alert macaque monkeys (male and female), whereby neurons exhibit a reduction in the strength of extraclassical surround suppression and an expansion in the preferred stimulus size with low-contrast stimuli compared with high-contrast stimuli. Effects were greater for magnocellular neurons than for parvocellular neurons, indicating stream-specific interactions between stimulus contrast and stimulus size. Within the magnocellular pathway, contrast-dependent effects were comparable for ON-center and OFF-center neurons, despite ON neurons having larger receptive fields, less pronounced surround suppression, and more pronounced contrast gain control than OFF neurons. Together, these findings suggest that the parallel streams delivering visual information from retina to primary visual cortex, serve not only to broaden the range of signals delivered to cortex, but also to provide a substrate for differential interactions between stimulus contrast and stimulus size that may serve to improve stimulus detection and stimulus discrimination under pathway-specific lower and higher contrast conditions, respectively.SIGNIFICANCE STATEMENT Stimulus contrast is a salient feature of visual scenes. Here we examine the influence of stimulus contrast on spatial integration in the lateral geniculate nucleus (LGN). Our results demonstrate that increases in contrast generally increase extraclassical suppression and decrease the size of optimal stimuli, indicating a reduction in the extent of visual space from which LGN neurons integrate signals. Differences between magnocellular and parvocellular neurons are noteworthy and further demonstrate that the feedforward parallel pathways to cortex increase the range of information conveyed for downstream cortical processing, a range broadened by diversity in the ON and OFF pathways. These results have important implications for more complex visual processing that underly the detection and discrimination of stimuli under varying natural conditions.     

BRAINSTEM INPUT MODULATES GLOBALLY THE TRANSMISSION THROUGH THE LATERAL GENICULATE NUCLEUS

The transmission of visual information from the retina to the visual cortex through the lateral geniculate nucleus (LGN) is a complex process, which involves several neuronal mechanisms, elements, and circuits. The authors investigated this process in anesthetized, paralyzed cats by recording from LGN relay neurons, together with their retinal input, which appeared as slow (S) potentials. The major findings are: (1) The transfer ratio (LGN firing/retinal firing) fluctuated slowly and (2) these fluctuations in transfer ratio were synchronized across the nucleus, did not depend on visual stimulation, and were highly correlated with neural activity in the parabrachial nucleus of the brainstem (PBN). Electrical stimulation of the PBN increased transmission from retina to cortex through the LGN. It is concluded that the PBN, which is part of the Ascending Arousal System, can modulate globally the transmission of information through the thalamus.     

Brainstem input modulates globally the transmission through the lateral geniculate nucleus

The transmission of visual information from the retina to the visual cortex through the lateral geniculate nucleus (LGN) is a complex process, which involves several neuronal mechanisms, elements, and circuits. The authors investigated this process in anesthetized, paralyzed cats by recording from LGN relay neurons, together with their retinal input, which appeared as slow (S) potentials. The major findings are: (1) The transfer ratio (LGN firing/retinal firing) fluctuated slowly and (2) these fluctuations in transfer ratio were synchronized across the nucleus, did not depend on visual stimulation, and were highly correlated with neural activity in the parabrachial nucleus of the brainstem (PBN). Electrical stimulation of the PBN increased transmission from retina to cortex through the LGN. It is concluded that the PBN, which is part of the Ascending Arousal System, can modulate globally the transmission of information through the thalamus.     

Effects of bicuculline on receptive field center sensitivity of relay cells in the lateral geniculate nucleus

The lateral geniculate nucleus (LGN) receives input from the retina that is spatially organized into a receptive-field center and surround. It maintains this organization in the signal that it sends to the visual cortex. Previous studies have focused on changes in the receptive-field 'surround' that are generated at the LGN, possibly as a local contrast enhancement mechanism. The present study suggests a role for the LGN in regulating the receptive-field center sensitivity under the control of GABAergic circuitry. Local microiontophoresis of the GABAA receptor antagonist bicuculline increased the contrast sensitivity of LGN relay cells to many spatial frequencies. Difference of Gaussians analysis showed that the increased was due to an increased sensitivity of the receptive-field center. Similar increases in receptive-field center sensitivity may be produced during behavioral arousal by the action of pontine and mesencephalic pathways upon the activity of the LGN GABAergic circuitry.     

Spatial receptive field properties of lateral geniculate cells in the owl monkey (Aotus azarae) at different contrasts: a comparative study

Several physiological properties of owl monkey lateral geniculate nucleus (LGN) cells were studied to verify whether its nocturnal habit has an influence on the organization of its subcortical visual system. Receptive field (RF) dimensions were measured using drifting gratings and bipartite field stimuli. We found that owl monkey cells LGN have larger RFs and were on average more non-linear than those of diurnal monkeys. But, as in other anthropoids, there is an increase in RF centre size with increasing eccentricity, and there is a limited correlation between these centre sizes and retinal ganglion cell dendritic tree sizes. The influence of contrast on sizes and peak sensitivities of RF centres and surrounds and on the response phases was studied. Both the sizes and peak sensitivities of the RF centres and surrounds decrease as contrast increases. As a result, the responses to low spatial frequency stimuli saturate with increasing contrast. Estimates of contrasts at half-maximal responses confirm the presence of saturation. It was found that the magnocellular cells saturate more strongly than parvocellular cells. The response phase increases with increasing contrast. These data resemble those obtained in the common marmoset, indicating that these are basic features of the primate visual system. We conclude that during evolution and as an adaptation to a nocturnal lifestyle, cells in the owl monkey LGN display an increased spatial integration in comparison with diurnal primate species, without a change in the basic organization common to the primate subcortical visual system.     

Monoclonal antibody Cat-301 identifies Y-cells in the dorsal lateral geniculate nucleus of the cat

In mammalian visual pathways, information is carried in parallel channels from the retina through the visual thalamus to visual cortex. The cat's visual pathway comprises at least three major channels that begin with the X, Y, and W ganglion cells in the retina. In the dorsal lateral geniculate nucleus (LGN) of the thalamus, neurons in the X, Y, and W channels receive input from their retinal counterparts and can be discriminated from one another on the basis of their anatomical and physiological properties. The search for molecular properties that might correlate with anatomically or physiologically defined classes of neuron has been a major area of research in recent years. Monoclonal antibody Cat-301 recognizes a neuronal surface-associated proteoglycan in many areas of the mammalian central nervous system. In the cat LGN Cat-301 immunoreactivity is restricted to a subset of neurons. We show here that the distribution, size, morphology, and cortical projection pattern of Cat-301-positive LGN neurons match those previously described for Y-cells. Taken together with our previous studies of the development of immunoreactivity and the sensitivity of Cat-301 staining to visual deprivation, these studies suggest that Cat-301 specifically recognizes Y-cells in the cat LGN. These results indicate that neurons within a physiologically and anatomically defined cell class share a molecular property. They further suggest that differences in molecular traits may reflect, and possibly subserve, differences in anatomical and physiological characteristics.     

Retinal ganglion cell inputs to the koniocellular pathway

To understand the transmission of sensory signals in visual pathways we studied the morphology and central projection of ganglion cell populations in marmoset monkeys. Retinal ganglion cells were labeled by photofilling following injections of retrograde tracer in the lateral geniculate nucleus (LGN), or by intracellular injection with neurobiotin. Ganglion cell morphology was analyzed using hierarchical cluster analysis. In addition to midget and parasol ganglion cells, this method distinguished three main clusters of wide-field cells that correspond to small bistratified, sparse, and broad thorny cells identified previously. The small bistratified and sparse cells occupy neighboring positions on the hierarchical (linkage distance) tree. These cell types are presumed to carry signals originating in short-wavelength sensitive (S or "blue") cones in the retina. The linkage distance from these putative S-cone pathway ganglion cells to other wide-field cells is similar to the linkage distance from midget cells to parasol cells, suggesting that S-cone cells form a distinct functional subgroup of ganglion cells. Small bistratified cells and large sparse cells were the most commonly labeled wide-field cells following LGN injections in koniocellular layer K3. This is consistent with physiological evidence that the role of this layer includes transmission of S-cone signals to the visual cortex. Other wide-field cell types were also labeled following injections including K3, and other koniocellular LGN layers; these cell types may correspond to "non-blue koniocellular" receptive fields recorded in physiological studies.     

Ventral lateral geniculate nucleus projects to the dorsal lateral geniculate nucleus in the cat

The lamina C3 of the dorsal lateral geniculate nucleus of the cat does not receive retinal projections but instead receives visual information from the small subpopulation of W-type ganglion cells via the upper substratum of the stratum griseum superficiale of the superior colliculus. We herein report a projection from the lateral division of the ventral lateral geniculate nucleus into the lamina C3 of the dorsal lateral geniculate nucleus. As the lateral division receives projections from the contralateral retina and the ipsilateral upper stratum griseum superficiale of the superior colliculus, we suggest that these regions make up a small cell type W-cell neuronal network that provides visual information to layer I of the striate cortex via the lamina C3.     

Electrophysiological study of synaptic connections between a transplanted lateral geniculate nucleus and the visual cortex of the host rat

The lateral geniculate nucleus (LGN) of a fetal rat was transplanted to the visual cortex (VC) of a neonatal rat. A current source-density analysis of field potentials and an intracellular study of neuronal responses were conducted in slice preparations by electrical stimulation of transplanted LGN and host VC. The results indicated that synaptic connections were established reciprocally between the transplanted LGN and the host VC.     

Relationship between response latency and amplitude for ganglion and geniculate X- and Y-cells in the cat.

This study investigates the relationship between visual response latency and amplitude in the retina and dorsal lateral geniculate nucleus (dLGN) of the anesthetized, paralyzed cat. The discharge rate profiles of retinal ganglion and dLGN X- and Y-cells were measured on a trial by trial basis during repeated stimulation with sinusoidal grating patterns. Latencies of response onsets and peaks were regressed linearly against different measures of response amplitude to determine the extent of covariance. In general, response amplitude was a poor predictor of response latency for both retinal ganglion and geniculate cells. The results suggest that response latency, which changes systematically with stimulus spatial frequency and/or contrast, is not a trivial consequence of discharge rate at either level of the visual system.