The dorsal lateral geniculate nucleus (dLGN) in carnivores and primates is a laminated structure, where each layer gets visual input from only one eye [1, 2]. By contrast, in rodents such as mice and rats, the dLGN is not overtly laminated, the retinal terminals from the two eyes are only partially segregated [3, 4], and many cells in the binocular segment of dLGN get excitatory inputs from both eyes [5, 6]. Here, we show that the evolutionary ancient koniocellular (K) division of primate dLGN, like rodent dLGN, forms a subcortical site of binocular integration. We recorded single-cell activity in dLGN of anesthetized marmoset monkeys. As expected, cells in the parvocellular (P) and magnocellular (M) layers received monocular excitatory inputs. By contrast, many cells in the K layers received excitatory inputs from both eyes. The specialized properties of distinct K sub-populations (for example, blue-yellow color selectivity) were preserved across the two eye inputs, and where tested, the contrast sensitivity of each eye input was roughly matched. The results argue that evolutionarily widely separated orders such as rodents and primates have a shared strategy of integrating signals from the two eyes in subcortical circuits.
Slow rhythmic changes in nerve-cell activity are characteristic of unconscious brain states and also may contribute to waking brain function by coordinating activity between cortical and subcortical structures. Here we show that slow rhythms are exhibited by the koniocellular (K) pathway, one of three visual pathways beginning in the eye and projecting through the lateral geniculate visual relay nucleus to the cerebral cortex. We recorded activity in pairs and ensembles of neurons in the lateral geniculate nucleus of anesthetized marmoset monkeys. We found slow rhythms are common in K cells but are rare in parvocellular and magnocellular cell pairs. The time course of slow K rhythms corresponds to subbeta (<10 Hz) EEG frequencies, and high spike rates in K cells are associated with low power in the theta and delta EEG bands. By contrast, spontaneous activity in the parvocellular and magnocellular pathways is neither synchronized nor strongly linked to EEG state. These observations suggest that parallel visual pathways not only carry different kinds of visual signals but also contribute differentially to brain circuits at the first synapse in the thalamus. Differential contribution of sensory streams to rhythmic brain circuits also raises the possibility that sensory stimuli can be tailored to modify brain rhythms.parallel pathways | visual system | sleep-wake cycles | anesthesia | epilepsy T he thalamus is central to brain networks that generate slow rhythmic neural activity in sleep-wake cycles, anesthesia, and epilepsy (1-5). However, the thalamus also provides parallel pathways to cerebral cortex for conscious sensation. These two aspects of thalamic function are not independent, as shown, for example, when repetitive visual stimuli induce epileptic seizures (6). Anatomical studies of the dorsal lateral geniculate nucleus (LGN) show preferential inputs to the LGN koniocellular (K) layers from midbrain centers regulating eye movements and vigilance state (1, 2, 7-9), suggesting that activity in the K system is concerned with brain state as well as with faithful transmission of retinal signals. We found evidence supporting this idea from an unexpected observation on K cells. Results During extracellular recordings fromLGN in anesthetized marmoset monkeys (Fig.1 A-D), we found that in the absence of patterned visual stimuli the spike rate of K cells showed slow fluctuations over the course of several seconds to minutes. An example of these slow intrinsic rhythms in three simultaneously recorded K cells is shown in Fig. 1E. By contrast the spike rate of parvocellular (P) cells (Fig. 1F) and magnocellular (M) cells (Fig. 1G) was stable in the absence of patterned visual stimulus. Retinal ganglion cell inputs to K, P, and M layers show low variation in steady discharges at frequencies below 3 Hz (10); this fact implies that the fluctuations do not arise in the retina. Frequency analysis of maintained spike rates showed that below 1 Hz, K-cell spike rates (n = 56) on average were 33% more variable than P-cell spike ...
Solomon SG, Tailby C, Cheong SK, Camp AJ. Linear and nonlinear contributions to the visual sensitivity of neurons in primate lateral geniculate nucleus. J Neurophysiol 104: 1884 -1898, 2010. First published August 4, 2010 doi:10.1152/jn.01118.2009. Several parallel pathways convey retinal signals to the visual cortex of primates. The signals of the parvocellular (P) and magnocellular (M) pathways are well characterized; the properties of other rarely encountered cell types are distinctive in many ways, but it is not clear that they can provide signals with the same fidelity. Here we study this by characterizing the temporal receptive field of neurons in the lateral geniculate nucleus of anesthetized marmosets. For each neuron, we measured the response to a flickering uniform field, and, from this, estimated the linear and nonlinear receptive fields using spike-triggered average (STA) and spike-triggered covariance (STC) analyses. As expected the response of most P-cells was dominated by the STA, but the response of most M-cells required additional nonlinear components, and these usually acted to suppress cell responses. The STC analysis showed stronger suppressive axes in suppressed-by-contrast cells, and both suppressive and excitatory axes in ON-OFF cells. Together, the STA and the STC analyses form a model of the temporal response to a large uniform field: under this model, the information that was provided by suppressed-by-contrast cells or ON-OFF cells approached that provided by the P-and M-cells. However, whereas Pand M-cells provided more information about luminance, the nonlinear cells provided more information about the contrast energy. This suggests that the nonlinear cells provide complimentary signals to those of P-and M-cells, with reasonably high fidelity, and may play an important role in normal visual processing.
Key points• In addition to supplying signals for conscious visual perception, the pathways from eye to brain serve visual functions such as reflex eye movements, which are controlled by a brain area called the superior colliculus (SC).• It is known that short-wavelength sensitive (S or 'blue') cone photoreceptors serve an evolutionary ancient pathway for colour vision but whether S cones also contribute to reflex eye movements is poorly understood.• We show that in recordings from anaesthetised marmoset monkeys, S cones do not contribute to visual responses in the SC. Thus, although S cones are a primitive part of the visual system their signals are selectively directed to thalamo-cortical pathways serving colour vision.• The result also implies that colour-selective responses reported in SC of awake monkeys must arrive through indirect (non-retinal) inputs to the SC. AbstractThe main subcortical visual targets of retinal output neurones (ganglion cells) are the parvocellular and magnocellular layers of the dorsal lateral geniculate nucleus (LGN) in the thalamus. In addition, a small and heterogeneous collection of ganglion cell axons projects to the koniocellular layers of the LGN, to the superior colliculus (SC), and to other subcortical targets. The functional (receptive field) properties and target specificity of these non-parvocellular, non-magnocellular populations remain poorly understood. It is known that one population of koniocellular layer cells in the LGN (blue-On cells) receives dominant functional input from short-wavelength sensitive (S or 'blue') cones. Here we asked whether SC neurones also receive S cone inputs. We made extracellular recordings from single neurones (n = 38) in the SC of anaesthetised marmoset monkeys. Responses to drifting and flashed gratings providing defined levels of cone contrast were measured. The SC receptive fields we recorded were often binocular, showed 'complex cell' like responses (On-Off responses), strong bandpass spatial frequency tuning, direction selectivity, and many showed strong and rapid habituation to repeatedly presented stimuli. We found no evidence for dominant S cone input to any SC neurone recorded. These data suggest that S cone signals may reach cortical pathways for colour vision exclusively through the koniocellular division of the lateral geniculate nucleus.
Visual perception requires integrating signals arriving at different times from parallel visual streams. For example, signals carried on the phasic-magnocellular (MC) pathway reach the cerebral cortex pathways some tens of milliseconds before signals traveling on the tonic-parvocellular (PC) pathway. Visual latencies of cells in the koniocellular (KC) pathway have not been specifically studied in simian primates. Here we compared MC and PC cells to "blue-on" (BON) and "blue-off" (BOF) KC cells; these cells carry visual signals originating in short-wavelength-sensitive (S) cones. We made extracellular recordings in the lateral geniculate nucleus (LGN) of anesthetized marmosets. We found that BON visual latencies are 10-20 ms longer than those of PC or MC cells. A small number of recorded BOF cells (n = 7) had latencies 10-20 ms longer than those of BON cells. Within all cell groups, latencies of foveal receptive fields (<10° eccentricity) were longer (by 3-8 ms) than latencies of peripheral receptive fields (>10°). Latencies of yellow-off inputs to BON cells lagged the blue-on inputs by up to 30 ms, but no differences in visual latency were seen on comparing marmosets expressing dichromatic ("red-green color-blind") or trichromatic color vision phenotype. We conclude that S-cone signals leaving the LGN on KC pathways are delayed with respect to signals traveling on PC and MC pathways. Cortical circuits serving color vision must therefore integrate across delays in (red-green) chromatic signals carried by PC cells and (blue-yellow) signals carried by KC cells.
Key points r We measured fractal (self-similar) fluctuations in ongoing spiking activity in subcortical (lateral geniculate nucleus, LGN) and cortical (area MT) visual areas in anaesthetised marmosets. r Cells in the evolutionary ancient koniocellular LGN pathway and in area MT show high-amplitude fractal fluctuations, whereas evolutionarily newer parvocellular and magnocellular LGN cells do not. r Spiking activity in koniocellular cells and MT cells shows substantial correlation to the local population activity, whereas activity in parvocellular and magnocellular cells is less correlated with local activity.r We develop a model consisting of a fractal process and a global rate modulation which can reproduce and explain the fundamental relationship between fractal fluctuations and population coupling in LGN and MT.r The model provides a unified account of apparently disparate aspects of neural spiking activity and can improve our understanding of information processing in evolutionary ancient and modern visual pathways.Abstract The brain represents and processes information through patterns of spiking activity, which is influenced by local and widescale brain circuits as well as intrinsic neural dynamics. Whether these influences have independent or linked effects on spiking activity is, however, not known. Here we measured spiking activity in two visual centres, the lateral geniculate nucleus Brandon Munn received his PhD in Physics from the University of Sydney in 2019, and he is currently employed as a postdoctoral researcher at the University of Sydney, Brain and Mind Centre. His PhD research investigated mesoscale dynamics, within the early visual system. His interests are in utilising Physics methodology with a particular interest in criticality and how the brain has evolved to decode the statistics of natural scenes optimally. 1552B. Munn and others J Physiol 598.8 (LGN) and cortical area MT, in marmoset monkeys. By combining the Fano-factor time curve, power spectral analysis and rescaled range analysis, we reveal inherent fractal fluctuations of spiking activity in LGN and MT. We found that the evolutionary ancient koniocellular (K) pathway in LGN and area MT exhibits strong fractal fluctuations at short (<1 s) time scales. Parvocellular (P) and magnocellular (M) LGN cells show weaker fractal fluctuations at longer (multi-second) time scales. In both LGN and MT, the amplitude and time scale of fractal fluctuations can explain short and long time scale spiking dynamics. We further show differential neuronal coupling of LGN and MT cells to local population spiking activity. The population coupling is intrinsically linked to fractal fluctuations: neurons showing stronger fluctuations are more strongly correlated to the local population activity. To understand this relationship, we modelled spiking activity using a fractal inhomogeneous Poisson process with dynamic rate, which is the product of an intrinsic stochastic fractal rate and a global modulatory gain. Our model explains the intrinsic links betwee...
Here we demonstrate the application of a method that could accelerate the development of novel therapies by allowing direct and repeatable visualization of cellular function in the living eye, to study loss of vision in animal models of retinal disease, as well as evaluate the time course of retinal function following therapeutic intervention. We use high-resolution adaptive optics scanning light ophthalmoscopy to image fluorescence from the calcium sensor GCaMP6s. In mice with photoreceptor degeneration (rd10), we measured restored visual responses in ganglion cell layer neurons expressing the red-shifted channelrhodopsin ChrimsonR over a six-week period following significant loss of visual responses. Combining a fluorescent calcium sensor, a channelrhodopsin, and adaptive optics enables all-optical stimulation and recording of retinal neurons in the living eye. Because the retina is an accessible portal to the central nervous system, our method also provides a novel non-invasive method of dissecting neuronal processing in the brain.
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