Morphology of visual sector thalamic reticular neurons in the macaque monkey suggests retinotopically specialized, parallel stream‐mixed input to the lateral geniculate nucleus

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The thalamic reticular nucleus (TRN) is a thin, shell‐like structure wrapping around the thalamus and forming an interface between the thalamus and the cortex that is present in all mammals (Pinault, 2004). Neurons in the TRN receive collateral input from thalamic relay neurons and corticothalamic neurons (Jones, 1985). All TRN neurons are GABAergic and make inhibitory connections with thalamic relay neurons (Jones, 1985; Ohara and Lieberman, 1985; Sanches‐Vives and McCormick, 1997; Pinault and Deschenes, 1998; Uhlrich et al., 2003). Based on the organization of thalamic and cortical inputs, the TRN is organized into different sectors, many of which are associated with first‐order sensory thalamic nuclei (Jones, 1985). Some sectors of the TRN receive inputs from additional brain areas including the pulvinar (Conley and Diamond, 1990; Baldauf, 2010), the brainstem and basal forebrain (Guillery and Harting, 2003), and the prefrontal cortex (Zikopoulos and Barbas, 2006). Accordingly, the TRN could serve as an integration hub for bottom‐up sensory and top‐down cognitive signals (Guillery and Harting, 2003). Along these lines, Crick (1984) proposed that the TRN controls the flow of perceptual signals from the thalamus to the cortex. Subsequent studies have provided evidence that TRN neurons are modulated by attention and facilitate interactions between sensory and cognitive signals (McAlonan et al., 2006; Halassa et al., 2014; Wimmer et al., 2015). Recent studies have even outlined specific genetic contributions to the TRN's role in sensory selection and attention (Ahrens et al., 2015; Wells et al., 2016).
While it is clear that the TRN is important for a number of broadly defined functions such as sensory selection, attention, and arousal, how circuits connecting TRN neurons with their thalamic targets mediate these functions remains unknown. The specific organization and function of TRN neurons is especially intriguing in the context of highly specialized sensory systems, such as the visual system of the primate. Neurons in the primate retina and dorsal lateral geniculate nucleus of the thalamus (dLGN) are optimized for acuity and color vision—unique specializations among mammals—and also form distinct parallel processing streams to encode a rich representation of the visual world. Primate retinal and dLGN neurons in the magnocellular (M), parvocellular (P), and koniocellular (K) streams are morphologically and physiologically distinct in order to convey information about visual motion, form/acuity, and color in parallel (Kaplan, 2004). M, P, and K neurons are physically segregated into separate layers in the dLGN and synapse in specific laminar compartments within the visual cortex. Given the strict segregation of feedforward visual signals into parallel streams, it remains an open question whether TRN inputs to the dLGN in the primate maintain this stream‐specific segregation or provide a more global input that is not stream‐specific. More is known about the morphology, physiology, and organization of TRN neurons in nonprimate species; these findings provide clues about possible primate TRN‐dLGN connectivity schemes, discussed below.
Neurons in the visual sector of the TRN receive inputs from and project axons to the dLGN (Sherman and Guillery, 2006). These afferent inputs and efferent projections are retinotopically organized, consistent with the topographic organization of afferent and efferent connections between TRN sectors and their associated sensory thalamic nuclei (Montero et al., 1977; Crabtree and Killackey, 1989; Conley and Diamond, 1990; Uhlrich et al., 2003; Fitzgibbon et al., 2007). Evidence from carnivores, rodents, and Galagos suggests that sectors of the TRN, including the visual sector, are organized into adjacent stripes or tiers including “inner” and “outer” tiers that receive input from higher‐order and first‐order thalamic nuclei, respectively (Conley and Diamond, 1990; Sherman and Guillery, 2006; Baldauf, 2010; Lam and Sherman, 2011).
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