Abstract

Many theories propose recurrent interactions across the cortical hierarchy, but it is unclear if cortical circuits are selectively wired to implement looped computations. Using subcellular channelrhodopsin-2-assisted circuit mapping in mouse visual cortex, we compared feedforward (FF) or feedback (FB) cortico-cortical (CC) synaptic input to cells projecting back to the input source (looped neurons) with cells projecting to a different cortical or subcortical area. FF and FB afferents showed similar cell-type selectivity, making stronger connections with looped neurons than with other projection types in layer (L)5 and L6, but not in L2/3, resulting in selective modulation of activity in looped neurons. In most cases, stronger connections in looped L5 neurons were located on their apical tufts, but not on their perisomatic dendrites. Our results reveal that CC connections are selectively wired to form monosynaptic excitatory loops and support a differential role of supragranular and infragranular neurons in hierarchical recurrent computations.

Highlights

  • The complex network of cortical areas can be hierarchically ordered based on the anatomy of interareal cortico-cortical (CC) projections

  • Neurons with different projection patterns are intermingled in visual areas We studied CC connections between primary visual cortex (V1), the lowest-order area of mouse visual cortex, and either the lateral visual areas (V2L) or the medial visual areas (V2M)

  • We compared the laminar distribution of V2L- or V1-projecting IT neurons with either IT neurons projecting to V2M, pyramidal tract (PT) neurons projecting to the superior colliculus (SC), or CT neurons projecting to the visual thalamus

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Summary

Introduction

The complex network of cortical areas can be hierarchically ordered based on the anatomy of interareal cortico-cortical (CC) projections. Using a combination of subcellular channelrhodopsin-2 (ChR2)-assisted circuit mapping (sCRACM) (Petreanu et al, 2009) and injections of multiple retrograde tracers, we found that FF and FB axons selectively provide stronger inputs to looped neurons in layer (L) 5 and L6, while in L2/ 3, they remain either unselective for projection type or provide stronger inputs to non-looped neurons. Both ascending and descending hierarchical streams display the same selectivity for specific looped projection neurons despite their different anatomical profiles. Preferential innervation of looped L5 neurons often involved synapses made on their apical, but not basal, dendrites

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