Neuron
Volume 109, Issue 21, 3 November 2021, Pages 3473-3485.e5
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Article
Bottom-up inputs are required for establishment of top-down connectivity onto cortical layer 1 neurogliaform cells

https://doi.org/10.1016/j.neuron.2021.08.004Get rights and content
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Highlights

  • During development, L1 NGF cells receive strong dLGN inputs but weak ACC connectivity

  • ACC inputs onto L1 NGF cells, but not onto “canopy” cells, strengthen in the adult

  • Sensory deprivation blocked the strengthening of ACC afferents onto L1 NGF cells

  • Early ACC is strengthened precociously by stimulation in a thalamus-dependent manner

Summary

Higher-order projections to sensory cortical areas converge on layer 1 (L1), the primary site for integration of top-down information via the apical dendrites of pyramidal neurons and L1 GABAergic interneurons. Here we investigated the contribution of early thalamic inputs onto L1 interneurons for establishment of top-down connectivity in the primary visual cortex. We find that bottom-up thalamic inputs predominate during L1 development and preferentially target neurogliaform cells. We show that these projections are critical for the subsequent strengthening of top-down inputs from the anterior cingulate cortex onto L1 neurogliaform cells. Sensory deprivation or selective removal of thalamic afferents blocked this phenomenon. Although early activation of the anterior cingulate cortex resulted in premature strengthening of these top-down afferents, this was dependent on thalamic inputs. Our results demonstrate that proper establishment of top-down connectivity in the visual cortex depends critically on bottom-up inputs from the thalamus during postnatal development.

Keywords

Layer 1
NDNF
inhibitory interneurons
neurogliaform cells
bottom-up
top-down
dLGN
ACC
development

Data and code availability

  • Microscopy and electrophysiology data reported in this paper will be shared by the lead contact upon request.

  • Software used for data analysis are included in the Key resources table

  • Any additional information required to reanalyze the data reported in this work paper is available from the Lead Contact upon request.

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