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 ...
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