The functional logic of cortico-pulvinar connections

“For example, all 20–30 known visual areas connect with the pulvinar, sometimes in a relatively topographic fashio”

“It receives input from visual cortex (e.g.: V1 and extrastriate cortex) and is connected with the prefrontal cortex, posterior parietal cortex, and superior colliculus (Shipp, 2003).”

“…requirements into a hierarchy of laminar neocortical circuits interacting with first-order (e.g., LGN) and higher-order (e.g., the pulvinar nucleus; Sherman and Guillery (2001) and Shipp (2003)) specific thalamic nuclei, and nonspecific thalamic nuclei (van Der Werf, Witter, & Groenewegen, 2002).”

“As a general principle, directly connected cortical areas will be indirectly connected via the pulvinar (Figure 1C; Sherman and Guillery, 2006; Shipp, 2003).”

“Indeed, sites in the dorsal pulvinar may be connected with relatively distal parts of the brain, such as parietal and frontal cortex [70].”

“The pulvinar is densely connected both structurally (54) and functionally (55) to various cortical regions, including occipital, parietal, temporal, and prefrontal cortices (56, 57).”

“V4 has widespread connections in the ventro-lateral pulvinar, with a given location in the V4 visual field map having connections with a wide zone extending between the anterior and posterior poles of the pulvinar (Shipp, 2003; Kaas and Lyon, 2007; Gattass et al., 2014).”

“…coordinate the gain of ascending pathways through direct effects upon superficial error units, or by regulation of effective connectivity through the induction of coherence in transareal oscillatory relationships (Shipp, 2003; Purushothaman et al., 2012; Saalmann et al., 2012; Kanai et al., 2015).”

“As a general principle, directly connected cortical areas will be indirectly connected via the pulvinar (Jones, 2001; Shipp, 2003).”

“The associative thalamic nuclei have the cortex as their main input and output sources and seem to represent active relay centers of cortical activity with properties well suitable for enhancing cortical coherence (30).”

“In fact, it has been suggested that there is a 'replicating' cortico-pulvinar-cortical linkag”

“In macaques, the dominant inputs to V2 are from PLvl and PIcl, although PIcm and PIm appear to contribute as well (Adams, et al., 2000;O’Brien, et al., 2002;Shipp, 2003).”

“This phenomenon on DWI in an acute peri-ictal state provides further evidence for a potential role of anatomical connections between the thalamus and mesial temporal lobe structures in symptomatic epilepsy and may add to the understanding of the extensive pulvinocortical relationships (Shipp, 2003).”

“This pattern of pulvinar connectivity with the cortex ideally positions the pulvinar to influence information transmission between cortical areas (Shipp, 2003; Sherman and Guillery, 2006; Saalmann and Kastner, 2011).”

“In monkeys, chemical inactivation of the pulvinar, specifically the central dorsal region which likely projects to the PFC (Romanski et al., 1997; Shipp, 2003; Pessoa and Adolphs, 2010), also impairs subjective confidence judgments in a visual task without changing task performance (Komura et al.”

“We also note that both the medial and dorsolateral pulvinar have reciprocal connections with association cortices (33).”

“com sub-cortical sources [25], areas with widespread anatomical connectivity were envisioned to stabilize phase relationships by bringing the oscillations to zero phase across the network despite non-negligible spike transmission times.”

“First, the visual maps in areas of the pulvinar are organized in such a way that neurons representing corresponding parts of the visual field in cortical visual areas project to similar parts of the pulvinar maps (Adams, Hof, Gattass, Webster, & Ungerleider, 2000; Shipp, 2001, 2003 ).”

“It has been theorized that higherorder thalamic nuclei modulate cortico-cortical transmission via cortico-thalamocortical relays and support the formation of synchronous interareal cortical activity (Shipp 2003; Ramcharan et al. 2005; Van Essen 2005).”

“PuM is the main candidate thalamic nucleus (present study; see also Crick and Koch 1998; Shipp 2003), by which information from different sensory modalities can converge to premotor cortex based on its connectivity with numerous cortical areas (e.g., Romanski et al. 1997; Hackett et al. 1998;…”

“There is a general observation that the pulvinar exchanges inputs with neighboring cortical areas that are directly inter-connected via cortico-cortical projections and recent findings show that these thalamic loops serve to drive alpha synchronization between nearby interconnected areas [48,49].”

“Directly connected cortical areas are generally indirectly connected via the pulvinar, through cortico-thalamo-cortical pathways (Sherman et al. 2006, Shipp 2003).”

“…is the main candidate (although other thalamic nuclei such as LP, VPL, MD or CL may also play a role) to represent an alternative to cortico-cortical loops by which information can be transferred between cortical areas belonging to different sensory and sensorimotor modalities (Shipp, 2003).”

“In other primate species, this region of the medial ventral pulvinar also contains some contralateral tuning (Bender, 1981; Li et al., 2013) and is interconnected with motion-sensitive regions (Standage and Benevento, 1983; Ungerleider et al., 1984; Shipp, 2003; Berman and Wurtz, 2010).”

“Note that an additional bottom-up pathway via the pulvinar originates in layer 5, and it might mediate the observed V1-to-V4 GC influences in the beta band (Shipp, 2003; Sherman, 2007; Schmid et al., 2012).”

“The localization of SC–MT relay neurons to PIp reinforces the idea that the architectonic subdivisions of the pulvinar are not devoted exclusively to a single function, and instead may support interaction between specialized cortical visual areas (Guillery and Sherman, 2002; Shipp, 2003).”

“Indeed, the replication principle of Shipp (2003) , according to which the connectivity of indirect transthalamic cortical pathways mimics that of direct corticocortical pathways, is supportive of this possibility.”

“For example, intriguing possibilities include that the pulvinar may facilitate temporal synchronicity in topographically specific areas within occipito-temporal cortex, thereby increasing signal-to-noise ratios (13), or similarly, that it may influence neural coherence on a much broader scale between fronto-parietal a…”

“…fMRI, with the prediction that positive modulations originate in dorsolateral pulvinar, which projects primarily layers 3 and 4 of occipital cortex (Shipp, 2003), while negative modulations originate in dorsomedial pulvinar, which projects primarily to parietal cortex (Behrens et al., 2003;…”

“Much of the dense labeling in the pulvinar can be attributed to its role as a corticocortical relay (Sherman 2005, Shipp 2003).”

“And the relatively precise and systematic organization of connections to and from the cortex and pulvinar (see (Shipp, 2003) for review) suggest that these connections are likely to mediate relatively direct interactions between cortical areas.”

“First, crucial elements of the attention network, such as the prefrontal cortex, posterior parietal cortex, and SC, are connected with the pulvinar [6].”

“Direct cortico-cortical feedback connections commonly project from layer 6 to layer 1 of the lower cortical area; cortical layer 6 also provides feedback connections to the pulvinar, which conveys this information to layer 1.(17)”

“…visual network constituted by the lateral intraparietal area (LIP), the temporal occipital area (TEO), area V4, and the pulvinar, which has been well studied in terms of its anatomical connectivity (e.g., Felleman and Van Essen, 1991; Saalmann et al., 2012; Shipp, 2003; Ungerleider et al., 2008).”

“…between anatomically and functionally defined LP subregions supports an emerging view that the fundamental units of corticothalamic computation are not individual thalamic nuclei but more precise thalamic circuits linking functionally related cortical areas (Halassa and Kastner, 2017; Shipp, 2003).”

“Our functional connectivity data may help to better integrate and emphasize the role of PuM in previous hypothesis about the functional role of the pulvinar nucleus, which is mostly supposed to play a key role in visual attention processing and selectivity (Shipp 2003, 2004).”

“A candidate structure is the dorsal pulvinar (Shipp, 2003).”

“, 2007], and probably trans-thalamic routing of cortico-cortical inputs via the associative thalamus [Cappe et al., 2009; Shipp, 2003].”

“This is strikingly in disaccord with the replication principle (Shipp, 2003), which states that cortical regions that are connected project to the same area of the pulvinar.”

“…in CTC circuits means that separate cortical networks may compete to recruit (or be recruited by) the same elements of thalamic circuitry (Shipp 2003): CTC circuitry may therefore be a vehicle for organizing and sculpting patterns of cortical activity over a more global scale than…”

“For example, the pulvinar, an association nucleus of the thalamus involved in higher-order visual processing, receives projections from BA17 (Grieve et al., 2000; Shipp, 2003).”

“…receives inputs from, and sends afferents to, a number of Frontiers in Neuroanatomy | www.frontiersin.org 3 August 2017 | Volume 11 | Article 71 visual cortical areas, and is therefore a key hub for visual corticocortical communication (Sherman and Guillery, 1996; Grieve et al., 2000; Shipp, 2003).”

“Studies of visual thalamus have revealed important roles for pulvinar and lateral geniculate nucleus in visuospatial perception and attention [4–10] and for mediodorsal thalamus in oculomotor control [11].”

“This organisation has been described as the replication principle where pulvinar connections replicate the cortico-cortical connections but not their functions (Shipp, 2003, 2004).”

“Thalamo-cortical projections targeting mostly the middle or superficial cortical layers have been reported for diverse thalamic nuclei [2,11,19,21,25,62–64].”

“These gradients did not respect the traditional cytoarchitectural subdivisions, but could be reconciled with chemoarchitectural subdivisions [Gutierrez et al., 1995, 2000; Shipp, 2003] that can be recognized in the human pulvinar [Cola et al.”

“6a) and anatomical (Shipp, 2003) connections between Pul and the cortex make Pul well suitable to behave as a thalamic control unit for the widespread cortical alpha activity.”

“The pulvinar, a higher level center of neuronal control, directly connects with the superior colliculus for attentional guidance [54–56].”

“In this integrative role, the broad tuning of pulvinar receptive fields may actually be an advantage: the broader the tuning, the broader the range for potential feature binding (as described by Shipp, 2003 ).”

“In comparison, the pulvinar neurons in the long latency group might receive inputs from some other structures, such as the temporal association cortices, prefrontal cortex or the amygdala, which project to the pulvinar (Shipp, 2003).”

“This layer specific input is shared with other structures with a role in salience computations, including the basal ganglia (Shipp, 2007) and the pulvinar nucleus of the thalamus (Shipp, 2003).”

“The cortico-PUL-cortical circuits are involved in amplifying signals and improving signal-to-noise ratios (Shipp, 2003; Pessoa and Adolphs, 2010), as well as modulating interactions between oscillatory processes in different cortical areas, which contributes to visual attention (Serences and Yantis, 2006; Saalmann and…”

“45,46 Given these widespread projections and innervations, we speculate that increased GM volume in TS may relate to multisensory integration in the thalamus, or to the linking of sensory input to cognitive, motivational-and movement-related areas of cortex.”

“Furthermore, the corticothalamic connections within the pulvinar are organized according to the topographical organization of the cortical areas themselves [8], which will enable the pulvinar to simultaneously coordinate communication between different cortical areas.”

“…are not only involved in projecting incoming sensory information to appropriate cortical regions, but also in feedback loops between cortex and “higher-level” thalamic nuclei that serve to modulate attention and coordinate sensory processing [John, Zikopoulos, Bullock, & Barbas, 2016; Shipp, 2003].”

“Whether this functional gradient exists also for the other sensory modalities and how it maps onto our current knowledge of the pulvino-cortical connectivity and the well-established topographically organized dorso-ventral gradient (Baizer et al., 1993; Shipp, 2003) remains to”

“…depicted in Figure 2, by Frontiers in Psychology | Cognition August 2013 | Volume 4 | Article 501 | 12 noting that the principal elements and connections of Stewart Shipp’s proposed functional anatomy of the brain’s attention system lie embedded in that connectivity (see Shipp, 2003, 2004).”

“…findings are consistent with the neuroanatomical hypothesis that the dorsal stream is responsible for processing nonconscious information (Lyon, Nassi, & Callaway, 2010; Shipp, 2003), particularly when it has affective value (Barrett & Bar, 2009; Pessoa & Adolphs, 2010; Tamietto et al., 2009).”

“Such an organization of connectivity between PuM and cortex would allow the modulation of cortico-cortical networks (52).”

“It should be noted however that these layers are also the targets of connections from the pulvinar nucleus of the thalamus (Benevento and Rezak, 1976; Gambino et al., 2014; Shipp, 2003).”

“Being the largest of the “association” nuclei (Shipp, 2003), the PUL receives the majority of its input directly from the cerebral cortex and participates primarily in reciprocal cortico-corical interactions.”

“It is clear that the pulvinar in the normal brain connects mainly to the striate cortex (Shipp, 2003), as well as the extrastriate visual and sensory multimodal association areas (Yeterian & Pandya, 1997).”

“In contrast, a large number of layer 6 neurons terminate with divergent axon arborizations (>1.0mm), having a large number (~1,000) of small, stalked boutons (reminiscent of dendritic spines) at distal locations (Rockland, 1996; Shipp, 2003; Sherman, 2017).”

“The medial pulvinar is a multimodal associative nucleus: it has extensive connectivity with high-order cortical systems (but not with early sensory areas) [78], it forms the subcortical component of the attentional network of the brain [79, 80] and is involved in visuospatial processing and reward-based decision makin…”