Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6

Abstract

Ascending sensory information is conveyed from the thalamus to layers 4 and 6 of sensory cortical areas. Interestingly, receptive field properties of cortical layer 6 neurons are different from those in layer 4. Do such differences reflect distinct inheritance patterns from the thalamus or are they derived instead from local cortical circuits? To distinguish between these possibilities, we utilized in vitro slice preparations containing the thalamocortical pathways in the auditory and somatosensory systems. Responses from neurons in layers 4 and 6 that resided in the same column were recorded using whole-cell patch clamp. Laser-scanning photostimulation via uncaging of glutamate in the thalamus and cortex was used to map the functional topography of thalamocortical and intracortical inputs to each layer. In addition, we assessed the functional divergence of thalamocortical inputs by optical imaging of flavoprotein autofluorescence. We found that the thalamocortical inputs to layers 4 and 6 originated from the same thalamic domain, but the intracortical projections to the same neurons differed dramatically. Our results suggest that the intracortical projections, rather than the thalamic inputs, to each layer contribute more to the differences in their receptive field properties.

Nicotinic alteration of functional thalamocortical topography

“…1B) and latencies (Figs. 1C) were also consistent with our prior examinations of these pathways [25,26]. …”

“…These results are in agreement with previous studies indicating robust connectivity between the thalamus and cortex in the auditory and somatosensory thalamocortical slice [18,19,25,26]. However, our current results demonstrate that the thalamic regions eliciting photostimulation-evoked EPSCs from layer 4 neurons expanded in the presence of bath- and locally-applied nicotine in the cortex.…”

“…Neurons were recorded in layer 4 of either the primary somatosensory barrel cortex (S1) or the primary auditory cortex (A1) respectively using whole-cell patch clamp to measure evoked postsynaptic currents in voltage-clamp mode [25,26]. We characterized the functional thalamocortical topography of regular-spiking neurons in layer 4 of each sensory cortical area (A1: n=9; S1; n=7) (average resting potentials: −64.9 ± 5.2 mV; average input resistance: 258.3 ± 102.0 MΩ) that were connected to the thalamus in the relevant thalamocortical slice preparations.…”

“…1A) thalamocortical slice preparations [25,26]. In the case of the somatosensory thalamocortical slice, EPSCs were elicited from focal regions in the ventroposterior medial nucleus (not shown).…”

“…We utilized in vitro slice preparations that maintain the intact connections from the principal sensory thalamic nuclei to primary sensory cortical areas [18,19] and assessed the functional topography of projections using whole-cell patch clamp recorded responses of cortical neurons to laser-scanning photostimulation via uncaging of glutamate in the thalamus [25,26]. In this manner, we mapped the functional thalamocortical inputs in juvenile mice following activation of nicotinic acetylcholine receptors (nAChRs).…”