The columnar and laminar organization of inhibitory connections to neocortical excitatory cells

Abstract

The cytoarchitectonic similarities of different neocortical regions have given rise to the idea of “canonical” connectivity between excitatory neurons of different layers within a column. It is unclear whether similarly general organizational principles also exist for inhibitory neocortical circuits. Here, we delineate and compare local inhibitory-to-excitatory wiring patterns in all principal layers of primary motor (M1), somatosensory (S1), and visual cortex (V1), using genetically targeted photostimulation in a mouse knock-in line that conditionally expresses channelrhodopsin-2 in GABAergic neurons. Inhibitory inputs to excitatory neurons derive largely from the same cortical layer within a three-column diameter. However, subsets of pyramidal cells in layers 2/3 and 5B receive extensive translaminar inhibition. These neurons are prominent in V1, where they might correspond to complex cells, less numerous in barrel cortex, and absent in M1. Although inhibitory connection patterns are stereotypical, the abundance of individual motifs varies between regions and cells, potentially reflecting functional specializations.

Strength and duration of perisomatic GABAergic inhibition depend on distance between synaptically connected cells

“…However, our data contrast the canonical model established by these studies, that PIIs show a high local intracolumnar connectivity with uniform functional properties of their output synapses including strength, duration, and reliability of GABAergic transmission in the entire target cell population (21,24,45). However, most neocortical studies disregarded the functional synaptic properties in their analysis.…”

“…To test whether inhibition provided by single PIIs is uniform over space and time (21,24,25), we performed sequential paired whole-cell patchclamp recordings between a single PII and multiple consecutively recorded target GCs in the dentate gyrus of postnatal day 17 (P17) to P23 rats (Fig. 1).…”

“…In fact, quantitative analysis of the PII axon morphology shows a gradual decline in axon collateral density with distance from the soma (17)(18)(19) frequently interpreted as a reduction in connection probability at larger distances (20,21), comparable to observations from excitatory glutamatergic neurons in the neocortex (22,23). However, conclusive physiological data on the functional properties of output synapses from one PII to several postsynaptic partners are lacking.…”

A computational model of fMRI activity in the intraparietal sulcus that supports visual working memory

“…The output excitatory node projects to the Layer 5 (L5) node, x ij ', and forms a recurrent connection with it. The excitatory node in L5 contacts Martinotti cells that project back to the dendrites of the input excitatory nodes in L2/3, consistent with recent anatomical data (Kapfer et al, 2007;Kätzel et al, 2011). Selfinhibition for L5 excitatory nodes might arise from a distinct population of inhibitory interneurons in L5, denoted as z ij '…”

“…However, they have not been employed in simulating and understanding the neural basis of VWM. In the present article, the basic CQ network is extended by distinguishing two populations of inhibitory interneurons with distinct functions (Kätzel, Zemelman, Buetfering, Wölfel, & Miesenböck, 2011;Markram et al, 2004). Furthermore, every excitatory node is divided into three distinct computational subunits, consistent with recent findings about dendritic computation (Polsky, Mel, & Schiller, 2004;Spruston, 2008;Spruston & Kath, 2004;Wei et al, 2001).…”