Claustral afferents of superior parietal areas PEc and PE in the macaque

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The claustrum forms a relatively thin, folded sheet of gray matter, inserted between the striatum and the insular cortex, which is surrounded by white matter (Crick and Koch, 2005). The claustrum has been classically considered as a component of the basal ganglia, but its direct projections to the cortex suggest a very different role. However, there are still relatively few data on which to build detailed hypotheses about its function (for comprehensive reviews, consult Smythies et al., 2012; Baizer et al., 2014; Mathur, 2014). Neuroanatomical studies in New and Old World monkeys have revealed widespread connections between the claustrum and neocortical regions in the frontal, occipital, and temporal lobes, as well as in the parietooccipital and posterior parietal regions, and somatosensory areas (Carman et al., 1964; Druga 1968, 1966; Kemp and Powell, 1970; Chadzypanagiotis and Narkiewicz, 1971; Pearson et al., 1982; Baizer et al., 1993; Tanné‐Gariepy et al., 2002; Burman et al., 2011; Reser et al., 2014; Milardi et al., 2015).
Here we investigated the claustral projections to cortical areas PEc and PE located on the exposed cortex of the superior parietal lobule. Area PEc contains visual, somatosensory, and bimodal neurons (Breveglieri et al., 2006, 2008), most of which are sensitive to the movement and position of hand and eye (Ferraina et al., 2001; Battaglia‐Mayer et al., 2001). This area contains an incomplete representation of the body, mainly focused on upper and lower limbs, without an evident topographic organization (Breveglieri et al., 2006, 2008). It has been recently demonstrated that a large percentage of PEc neurons encodes both direction and depth information during arm reaching movements (Hadjidimitrakis et al., 2015), and contributes to hand–target transformations for reaching (Piserchia et al., 2016). In contrast, area PE (which has been traditionally equated to Brodmann's area 5) contains an almost complete representation of the body, with a coarse topographic organization (Taoka et al., 1998, 2000; Padberg et al., 2007). The majority of its neurons respond to proprioceptive stimulation, while fewer cells are activated by tactile stimuli, and even fewer by visual stimuli (Duffy and Burchfiel, 1971; Sakata et al., 1973; Mountcastle et al., 1975). Area PE is involved in the preparation of limb movements (Burbaud et al., 1991) and in the generation of different types of reference systems for encoding reaching movements (Ferraina and Bianchi, 1994; Lacquaniti et al., 1995; Kalaska, 1996; Batista et al., 1999; Bremner and Andersen, 2012).
Very few studies have investigated the claustrum in macaque monkeys in the context of sensorimotor integration. Neuronal activity recorded in the claustrum while macaques performed arm movements, either visually guided or triggered by memorized information, suggested that claustral neurons could play a role in arm movement execution (Shima et al., 1996). A comparison with neuronal activity in the primary motor cortex showed that neurons of the claustrum, in contrast to those of the motor cortex, showed little selectivity to the type of movement (Shima et al., 1996). Other studies have suggested that the claustrum integrates multisensory information from different sensory cortices (Ettlinger and Wilson, 1990). The present study defines the origin of projections from the claustrum to the PEc and PE, and links these results to previous observations on claustral projections to other nodes of the cortical network of areas involved in movement planning and visuomotor integration.
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