Selective Thalamic Innervation of Rat Frontal Cortical Neurons.

Naoki Shigematsu,Alsayed A Mohamed,Yoshifumi Ueta,Takaichi Fukuda,Yasuo Kawaguchi,Sayuri Hatada,Yoshiyuki Kubota

doi:10.1093/cercor/bhv124

Abstract

Most glutamatergic inputs in the neocortex originate from the thalamus or neocortical pyramidal cells. To test whether thalamocortical afferents selectively innervate specific cortical cell subtypes and surface domains, we investigated the distribution patterns of thalamocortical and corticocortical excitatory synaptic inputs in identified postsynaptic cortical cell subtypes using intracellular and immunohistochemical staining combined with confocal laser scanning and electron microscopic observations in 2 thalamorecipient sublayers, lower layer 2/3 (L2/3b) and lower layer 5 (L5b) of rat frontal cortex. The dendrites of GABAergic parvalbumin (PV) cells preferentially received corticocortical inputs in both sublayers. The somata of L2/3b PV cells received thalamic inputs in similar proportions to the basal dendritic spines of L2/3b pyramidal cells, whereas L5b PV somata were mostly innervated by cortical inputs. The basal dendrites of L2/3b pyramidal and L5b corticopontine pyramidal cells received cortical and thalamic glutamatergic inputs in proportion to their local abundance, whereas crossed-corticostriatal pyramidal cells in L5b exhibited a preference for thalamic inputs, particularly in their distal dendrites. Our data demonstrate an exquisite selectivity among thalamocortical afferents in which synaptic connectivity is dependent on the postsynaptic neuron subtype, cortical sublayer, and cell surface domain.

Highlights

The thalamus relays information about peripheral sensations to primary sensory areas, and motor information from the basal ganglia and cerebellum to frontal cortical areas (Jones 2007; Strick et al 2009)
In the M2 area, thalamocortical fiber density is heterogeneous across cortical depth, as shown by the uneven expression of VGluT2 that is present at higher densities in upper layer 1 (L1) (L1a), L2/3b, and L5b of frontal cortex (Fig. 1B; Morishima et al 2011)
When the retrograde tracer CTB555 was injected extensively from L1 to layer 5 (L5) in M2 by pressure, 81.8% of the labeled thalamic cells were in the ventral anterior/ventromedial (VA/VM) nuclei, whereas 18.3% were in the VL nucleus (Fig. 1A,C; whole-depth injection; 5040 thalamic cells from 2 rats)

Summary

Introduction

The thalamus relays information about peripheral sensations to primary sensory areas, and motor information from the basal ganglia and cerebellum to frontal cortical areas (Jones 2007; Strick et al 2009). Comparative analysis of thalamocortical synapse formation between sensory and frontal areas will be critical for understanding the functional roles of thalamic inputs to these different cortical areas. Excitatory inputs to GABAergic cells typically occur on smooth dendritic shafts and somatic surfaces (Gulyás et al 1999). To understand the function of cortical circuits, we need to determine whether excitatory synaptogenesis is specialized based on postsynaptic neuron type ( pyramidal cells, GABAergic cells, or their subtypes), on neuronal surface type (dendritic spines, dendritic shafts, and/ or somata), or on dendritic locations ( proximal or distal portions) (Stepanyants et al 2004; Yuste and Bonhoeffer 2004). A key question is whether thalamocortical synapses are formed purely according to the relative local abundance of thalamocortical fibers, or if thalamic inputs preferentially innervate specific postsynaptic target domains

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