The Stimulus Selectivity and Connectivity of Layer Six Principal Cells Reveals Cortical Microcircuits Underlying Visual Processing

• Published in: Neuron (Cambridge, Mass.) Mass.), 2014-09, Vol.83 (6), p.1431-1443
• Main Authors: Vélez-Fort, Mateo, Rousseau, Charly V., Niedworok, Christian J., Wickersham, Ian R., Rancz, Ede A., Brown, Alexander P.Y., Strom, Molly, Margrie, Troy W.
• Format: Article
• Language: English
• Subjects: Animals; Brain; Image Processing, Computer-Assisted; Imaging, Three-Dimensional; Mice; Mice, Inbred C57BL; Neurons; Patch-Clamp Techniques; Photic Stimulation; Physiology; Visual Cortex - cytology; Visual Cortex - physiology; Visual Pathways - cytology; Visual Pathways - physiology; Visual Perception - physiology
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2014.08.001

Sensory computations performed in the neocortex involve layer six (L6) cortico-cortical (CC) and cortico-thalamic (CT) signaling pathways. Developing an understanding of the physiological role of these circuits requires dissection of the functional specificity and connectivity of the underlying individual projection neurons. By combining whole-cell recording from identified L6 principal cells in the mouse primary visual cortex (V1) with modified rabies virus-based input mapping, we have determined the sensory response properties and upstream monosynaptic connectivity of cells mediating the CC or CT pathway. We show that CC-projecting cells encompass a broad spectrum of selectivity to stimulus orientation and are predominantly innervated by deep layer V1 neurons. In contrast, CT-projecting cells are ultrasparse firing, exquisitely tuned to orientation and direction information, and receive long-range input from higher cortical areas. This segregation in function and connectivity indicates that L6 microcircuits route specific contextual and stimulus-related information within and outside the cortical network. •L6 cortico-cortical neurons are broadly tuned to stimulus orientation•L6 cortico-thalamic neurons are sparse firing and highly tuned to stimulus orientation•L6 cortico-cortical neurons receive input from cells located mostly within V1•L6 cortico-thalamic neurons receive input from higher order cortical areas Vélez-Fort et al. combine in vivo whole-cell recordings with transsynaptic retrograde tracing of monosynaptic connectivity from cortical layer six neurons to delineate functionally distinct microcircuits underlying sensory processing in the mouse primary visual cortex.