Mapping synaptic cortico‐claustral connectivity in the mouse

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The claustrum, a thin elongated sheet of neurons located between the insular cortex and the striatum, is the most interconnected structure in the brain per regional volume (Torgerson et al., 2015). The claustrum has been reported to display prominent reciprocal connectivity with essentially the entire cerebral cortex (Narkiewicz, 1964; Riche and Lanoir, 1978; Sanides and Buchholtz, 1979; Olson and Graybiel, 1980; LeVay and Sherk, 1981a; Macchi et al., 1981, 1983; Sherk and LeVay, 1981a, 1983; Pearson et al., 1982; Carey and Neal, 1985, 1986; LeVay, 1986; Sloniewski et al., 1986; Grieve and Sillito, 1995; Sadowski et al., 1997; Beneyto and Prieto, 2001; Tanne‐Gariepy et al., 2002; Alloway et al., 2009; Smith and Alloway, 2010, 2014; Park et al., 2012; Smith et al., 2012; Druga, 2014; Milardi et al., 2015). The broad cortical connections of the claustrum suggest it might serve as a network hub, coordinating activity of the cortical circuitry (Zingg et al., 2014). However, the anatomical structure of the claustrum is restrictive for functional perturbations, leaving the function of the claustrum a mystery.
Excitation of the different sensory modalities elicits responses in claustral neurons, which typically exhibit a low firing rate in the absence of stimuli (Segundo and Machne, 1956; Olson and Graybiel, 1980; Sherk and LeVay, 1981b; Remedios et al., 2010). While some studies have described multimodal responses in the claustrum (Segundo and Machne, 1956; Spector et al., 1974; Clarey and Irvine, 1986), other studies (Olson and Graybiel, 1980; Sherk and LeVay, 1981b; Remedios et al., 2010) failed to find multimodal cells in the claustrum, but rather found clear‐cut regional specialization. This leaves open the issue of whether claustral neurons integrate or segregate sensory information, a crucial issue for understanding the function of the claustrum.
The responses of claustral neurons to visual stimulation display a retinotopic organization in cats (Olson and Graybiel, 1980; LeVay and Sherk, 1981b; Sherk and LeVay, 1981b). Similarly, auditory‐responsive claustral neurons in both cats and primates have been found to be loosely tuned and display broad receptive fields, responding preferentially to the onset of a stimulus (Olson and Graybiel, 1980; Clarey and Irvine, 1986; Neal et al., 1986; Beneyto and Prieto, 2001; Remedios et al., 2010, 2014). Somatosensory responses have also been reported in the claustrum of cats, with reports of somatotopic organization (Spector et al., 1970, 1974; Olson and Graybiel, 1980).
Numerous studies in the past half‐century have addressed the organization of inputs into the claustrum of monkeys, cats, rabbits, and rats (Sanides and Buchholtz, 1979; LeVay and Sherk, 1981b; Sherk and LeVay, 1981b; Witter et al., 1988; Kowianski et al., 1998; Mathur, 2014). The anatomy corresponds well with the physiological studies, such that different cortical inputs map to segregated domains within the claustrum. Thus, both rostrocaudal and dorsoventral segregation have been proposed for the claustrum, albeit with a high degree of overlap. The claustrum also displays asymmetric reciprocal connectivity with the cortex, such that a given cortical modality receives input not only from its corresponding sensory zone in the claustrum, but from adjacent claustral regions as well. This asymmetry suggests that a given sensory zone in the claustrum may exert influence on additional cortical regions beyond those which innervate it (Narkiewicz, 1964; Norita, 1977; Riche and Lanoir, 1978; Olson and Graybiel, 1980; LeVay and Sherk, 1981b; Macchi et al., 1981, 1983; Sherk and LeVay, 1981b; Pearson et al., 1982; Carey and Neal, 1985; Minciacchi et al., 1985; Carey and Neal, 1986; Li et al., 1986; Sloniewski et al., 1986; Sadowski et al., 1997; Beneyto and Prieto, 2001; Tanne‐Gariepy et al., 2002; Alloway et al., 2009; Smith and Alloway, 2010; Park et al.
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