Thalamic Input to Distal Apical Dendrites in Neocortical Layer 1 Is Massive and Highly Convergent

Abstract

Input to apical dendritic tufts is now deemed crucial for associative learning, attention, and similar "feedback" interactions in the cerebral cortex. Excitatory input to apical tufts in neocortical layer 1 has been traditionally assumed to be predominantly cortical, as thalamic pathways directed to this layer were regarded relatively scant and diffuse. However, the sensitive tracing methods used in the present study show that, throughout the rat neocortex, large numbers (mean approximately 4500/mm(2)) of thalamocortical neurons converge in layer 1 and that this convergence gives rise to a very high local density of thalamic terminals. Moreover, we show that the layer 1-projecting neurons are present in large numbers in most, but not all, motor, association, limbic, and sensory nuclei of the rodent thalamus. Some layer 1-projecting axons branch to innervate large swaths of the cerebral hemisphere, whereas others arborize within only a single cortical area. Present data imply that realistic modeling of cortical circuitry should factor in a dense axonal canopy carrying highly convergent thalamocortical input to pyramidal cell apical tufts. In addition, they are consistent with the notion that layer 1-projecting axons may be a robust anatomical substrate for extensive "feedback" interactions between cortical areas via the thalamus.

Optical coherence microscopy for deep tissue imaging of the cerebral cortex with intrinsic contrast

“…5. In particular, the morphology and distribution of horizontal myelinated processes in layer I are very similar to the axons of Mtype thalamus cells [20]. Finer processes were seen more superficially, while thicker processes were seen at greater depths (Fig.…”

“…To further illustrate this concept, Fig. 2(f) shows virtual coronal slices of different thicknesses (20,50, and 200 microns), obtained from the same volumetric OCM data set. These images could, in principle, be repeated longitudinally in the same animal over time.…”

Highly Differentiated Projection-Specific Cortical Subnetworks

“…Because thalamic relay nuclei participating in the basal ganglia and cerebellum pathways innervate different sublaminae of L5 in the frontal cortex (Jones, 2001(Jones, , 2007Kuramoto et al, 2009;RubioGarrido et al, 2009), L5 pyramidal neurons in different sublaminae likely receive differential thalamic drive. The basal ganglia and cerebellar pathways go to the rostromedial and caudolateral parts of the ventral anterior (VA) and ventral lateral (VL) thalamic nuclei (VA-VL complex), respectively, from which the former send axons to L1, while the latter project to middle cortical layers (Jones, 2001(Jones, , 2007Kuramoto et al, 2009;Rubio-Garrido et al, 2009). We found dendritic branching differences of CPn and CCS cells to be correlated with the sublaminar distributions of the thalamic inputs, suggesting that L5 pyramidal projection neurons are specialized according to their participation in corticobasal ganglia and corticocerebellar loops.…”

Lateralization of observational fear learning at the cortical but not thalamic level in mice

“…The sensitivity of social fear to the manipulation of the left thalamus but not the left ACC suggests a possibility that left cortical targets other than the ACC may be involved in this form of emotional learning. Recently it has been demonstrated that the anteromedial thalamic nucleus of mice is one of the few thalamic regions that have quite widespread cortical outputs (22). This suggests a possibility that the anteromedial thalamus has the potential to influence many cortical regions.…”