The functional logic of cortico–pulvinar connections

Abstract

The pulvinar is an 'associative' thalamic nucleus, meaning that most of its input and output relationships are formed with the cerebral cortex. The function of this circuitry is little understood and its anatomy, though much investigated, is notably recondite. This is because pulvinar connection patterns disrespect the architectural subunits (anterior, medial, lateral and inferior pulvinar nuclei) that have been the traditional reference system. This article presents a simplified, global model of the organization of cortico-pulvinar connections so as to pursue their structure-function relationships. Connections between the cortex and pulvinar are topographically organized, and as a result the pulvinar contains a 'map' of the cortical sheet. However, the topography is very blurred. Hence the pulvinar connection zones of nearby cortical areas overlap, allowing indirect transcortical communication via the pulvinar. A general observation is that indirect cortico-pulvino-cortical circuits tend to mimic direct cortico-cortical pathways: this is termed 'the replication principle'. It is equally apt for certain pairs (or groups) of nearby cortical areas that happen not to connect with each other. The 'replication' of this non-connection is achieved by discontinuities and dislocations of the cortical topography within the pulvinar, such that the associated pair of connection zones do not overlap. Certain of these deformations can be used to divide the global cortical topography into specific sub-domains, which form the natural units of a connectional subdivision of the pulvinar. A substantial part of the pulvinar also expresses visual topography, reflecting visual maps in occipital cortex. There are just two well-ordered visual maps in the pulvinar, that both receive projections from area V1, and several other occipital areas; the resulting duplication of cortical topography means that each visual map also acts as a separate connection domain. In summary, the model identifies four topographically ordered connection domains, and reconciles the coexistence of visual and cortical maps in two of them. The replication principle operates at and below the level of domain structure. It is argued that cortico-pulvinar circuitry replicates the pattern of cortical circuitry but not its function, playing a more regulatory role instead. Thalamic neurons differ from cortical neurons in their inherent rhythmicity, and the pattern of cortico-thalamic connections must govern the formation of specific resonant circuits. The broad implication is that the pulvinar acts to coordinate cortical information processing by facilitating and sustaining the formation of synchronized trans-areal assemblies; a more pointed suggestion is that, owing to the considerable blurring of cortical topography in the pulvinar, rival cortical assemblies may be in competition to recruit thalamic elements in order to outlast each other in activity.

Multisensory anatomical pathways

“…Thalamic nuclei which contain cortico-thalamic connections (giant and small endings) from area 5 are also indicated below the diagram. medial part of the pulvinar nucleus 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). Interestingly, PuM also receives direct inputs from the superior colliculus (Stepniewska, 2004); information which is already multimodal.…”

Spikes, synchrony, and attentive learning by laminar thalamocortical circuits

“…The Synchronous Matching Adaptive Resonance Theory (SMART) model that is presented here shows how bottom-up and top-down pathways work together to accomplish this goal by coordinating processes of learning, attention, expectation, resonance, and synchrony. In particular, SMART explains how attentive learning requirements are realized by detailed brain circuits, notably the layered organization of cells in neocortical circuits and how they interact with first-order (e.g., the lateral geniculate nucleus, LGN) and higher-order (e.g., the pulvinar nucleus, PULV; Sherman and Guillery, 2001;Shipp, 2003), and nonspecific thalamic nuclei (van Der Werf et al, 2002).…”

“…As noted above, layer 5 pyramidal cells send driving inputs directly to higher cortices through the thalamus (e.g., the pulvinar; Sherman and Guillery, 2002;Shipp, 2003;see Figure 3a), indirectly control corticothalamic feedback at their own cortical level through layer 6 II ( Figures 2b and 3a), and also control corticocortical feedback to layer 4 at their own cortical level via layer 6 I (Figure 2c and 3c). Layer 5 can hereby generate widespread bursts of synchronized activity throughout the neocortex mediated by driving layer 5 terminations on higher-order thalamic nuclei (including pathological epileptogenic activity; Williams and Stuart, 1999), and selectively reset multiple cortical areas by relaying from the nonspecific thalamus layer 5 bursts to layer 4 via the 6 I →4 pathway.…”

“…The Synchronous Matching Adaptive Resonance Theory (SMART) model that is presented here shows how bottom-up and top-down pathways work together to accomplish this goal by coordinating processes of learning, attention, expectation, resonance, and synchrony. In particular, SMART explains how attentive learning requirements are realized by detailed brain circuits, notably the layered organization of cells in neocortical circuits and how they interact with first-order (e.g., the lateral geniculate nucleus, LGN) and higher-order (e.g., the pulvinar nucleus, PULV; Sherman and Guillery, 2001;Shipp, 2003), and nonspecific thalamic nuclei (van Der Werf et al, 2002).Corticothalamocortical pathways work in parallel with corticocortical routes (Maunsell and Van Essen, 1991;Salin and Bullier, 1995;Sherman and Guillery, 2002). Specific first-order thalamic nuclei relay sensory information to the cerebral cortex, whereas specific second-order thalamic nuclei receive their main input from layer 5 of lower-order cortical areas and relay this information to higherorder cortical areas (Sherman and Guillery, 2002, Figure 1a).…”

“…Most of its inputs originate from the cerebral cortex and the superior colliculus (SC). The LGN receives a massive cortical projection from V1 cortical layer 6, and the PULV receives afferents from layers 5 and 6 of several cortical areas (Rockland, 1998;Wang et al, 2002;Shipp, 2003 Fitzpatrick at al. (1985); Callaway and Wiser (1996) Layer 2/3 cells V1 → Layer 2/3 cells V1 D Recurrent connections (grouping) in 2/3.…”