Hierarchical Organization of Corticothalamic Projections to the Pulvinar

Abstract

Signals from lower cortical visual areas travel to higher order areas for further processing through corticocortical projections, organized in a hierarchical manner. These signals can also be transferred between cortical areas via alternative cortical transthalamic routes involving higher order thalamic nuclei like the pulvinar. It is unknown whether the organization of transthalamic pathways may reflect the cortical hierarchy. Two axon terminals types have been identified in cortico-thalamic (CT) pathways: the types I (modulators) and II (drivers) characterized by thin axons with small terminals and by thick axons and large terminals, respectively. In cats, projections from V1 to the pulvinar comprise mainly type II terminals whereas those from extrastriate areas include a combination of both terminals suggesting that the nature of CT terminals varies with the hierarchical order of visual areas. To test this hypothesis, distribution of CT terminals from area 21a was charted and compared with three other visual areas located at different hierarchical levels. Results demonstrate that the proportion of modulatory CT inputs increases along the hierarchical level of cortical areas. This organization of transthalamic pathways reflecting cortical hierarchy provides new and fundamental insights for the establishment of more accurate models of cortical signal processing along transthalamic cortical pathways.

Laminar distribution of cortical projection neurons to the pulvinar: A comparative study in cats and mice

“…Contrary to what is shown here in cats and mice, there were no Layer 6 retrogradely labeled neurons in V1 in these monkeys (Levitt et al, 1995). Although retrograde tracing of CT projection neurons to the pulvinar in monkeys does not show labeled neurons in V1 Layer 6, anterograde tracer injections in Area 17 in monkeys (Rockland, 1996) and cats (Abbas Farishta et al, 2020;Huppé-Gourgues et al, 2006 did label two types of terminals in the pulvinar, indicating that CT projection neurons in Area 17 could be found in both Layers 5 and 6. Similarly, retrograde tracer injections in the pulvinar of the prosimian Galago label CT neurons projecting to the pulvinar in Layers 5 and 6 (Conley & Raczkowski, 1990;Raczkowski & Diamond, 1981) while another study reports labeled neurons in Layer 6 only (Moore et al, 2019).…”

“…Our findings corroborate these results showing that labeled neurons in Area 17 were almost exclusively located in Layer 5. Interestingly, the present study and our previous ones (Abbas Farishta et al, 2020;Huppé-Gourgues et al, 2006 demonstrated that despite the large number of Layer 5 inputs from Area 17, there is still some contribution from Layer 6 neurons.…”

“…It is generally accepted that Type II terminals (driver) carry the main information that defines the basic receptive field properties of the postsynaptic neurons whereas Type I (modulator) change the neuron's properties (Sherman & Guillery, 1998). Previous studies have shown that Type II terminals belong to CT neurons that are mainly located in Layer 5 whereas Type I terminals are from neurons located in Layer 6 (Abbas Farishta et al, 2020;Deschênes et al, 1994;Huppé-Gourgues et al, 2006. Here, we showed that CT neurons from the cat Area 17 are almost exclusively from Layer 5, and consequently, it should provide the driver input to the LP.…”

“…Type I and II CT projections also exhibit distinct laminar origins. Type II projections originate from neurons located mainly in Layer 5 whereas Type I projections are located in Layer 6 (Abbas Farishta et al, 2020; Bourassa & Deschênes, 1995; Deschênes et al, 1994; Huppé‐Gourgues et al, 2006, 2019). These anatomical features of CT projections were found not only in the visual cortex but also in other sensory areas such as the somatosensory and auditory cortices, indicating that the connectivity patterns of these projections are an ubiquitous feature of the CT communication (Guillery et al, 2001; Llano & Sherman, 2008; Ojima, 1994; Ojima et al, 1996; Reichova & Sherman, 2004; Theyel et al, 2010).…”

“…Experimental and theoretical studies have shown that the nature of the information transferred between the pulvinar and the visual cortical areas varies across the cortical hierarchy (Cortes & Van Vreeswijk, 2012;de Souza et al, 2019;Jaramillo et al, 2019) thus raising the question whether cortico-thalamo-cortical pathways exhibit a hierarchical organization that parallels the cortico-cortical one (Shipp, 2003). Previous studies from our group have shown that the cat pulvinar receives distinct types of CT projection depending on their cortical source (Abbas Farishta et al, 2020;Huppé-Gourgues et al, 2006. For instance, projections from Area 17 are almost exclusively comprised of Type II terminals whereas inputs from high-level extrastriate areas PMLS (posteromedial lateral T A B L E 1 Count of CTb-labeled neurons in the cat cortex…”