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Review
. 2015 Feb;18(2):170-81.
doi: 10.1038/nn.3917. Epub 2015 Jan 27.

The neocortical circuit: themes and variations

Kenneth D Harris  1 , Gordon M G Shepherd  2
Affiliations
Review

The neocortical circuit: themes and variations

Kenneth D Harris et al. Nat Neurosci. 2015 Feb.

Abstract

Similarities in neocortical circuit organization across areas and species suggest a common strategy to process diverse types of information, including sensation from diverse modalities, motor control and higher cognitive processes. Cortical neurons belong to a small number of main classes. The properties of these classes, including their local and long-range connectivity, developmental history, gene expression, intrinsic physiology and in vivo activity patterns, are remarkably similar across areas. Each class contains subclasses; for a rapidly growing number of these, conserved patterns of input and output connections are also becoming evident. The ensemble of circuit connections constitutes a basic circuit pattern that appears to be repeated across neocortical areas, with area- and species-specific modifications. Such 'serially homologous' organization may adapt individual neocortical regions to the type of information each must process.

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Figures

Figure 1
Figure 1
Dendritic morphology of excitatory neurons in S1 barrel cortex. Modified with permission from Ref. . L4-IT: the 3 morphological classes of L4 intratelencephalic (IT) neurons: pyramidal, star pyramidal, and spiny stellate cells. IT: intratelencephalic neurons of layers 2, 3, 5A/B, and 6. PT: pyramidal tract neurons of L5B. CT: corticothalamic neurons of L6.
Figure 2
Figure 2
Excitatory hodology of ECs in layers 2–5, including intratelencephalic neurons in layer 4 (L4-IT), IT neurons of other layers (L2/3, L5A, L5B; grouped as “IT” here), and pyramidal tract (PT) neurons. L4-IT neurons project mostly unidirectionally to other IT neurons, which in turn project mostly unidirectionally to PT neurons. Each class receives extrinsic inputs, but information flows across classes in a largely directional manner due to asymmetric inter-class connectivity. All classes have recurrent connections with other members of their own class (not shown). The relationship of CT neurons and IT neurons in L6 to this stratified hodology is not yet established.
Figure 3
Figure 3
Thalamocortical (TC) input streams. A, Illustration of the layers of termination of matrix-, core-, and intralaminar (IL)-type TC projections. B, projections to V1 from dorsal lateral geniculate (left) and from lateral posterior and adjoining nuclei (right). Images from Allen connectivity atlas (http://connectivity.brain-map.org/, experiments 293914766 and 267608343). Scale bar: 140 μm. C, Interdigitating laminar profiles in barrel cortex of matrix-type TC axons (green; from POm in thalamus) and core-type TC axons (red; from VPM in thalamus). Modified, with permission, from Ref. .
Figure 4
Figure 4
Hypothesized excitatory hodology of the major EC classes. For clarity, intra-class (recurrent) connections are omitted, but exist for all cell types. This connectivity scheme is derived primarily from rodent barrel and motor cortex (see main text), and the existence of many of these connections in other regions remains to be tested. L5A ITs and L5B ITs have been represented together for simplicity. Additional connections for which only limited and/or conflicting evidence is available, or whose connectivity rates have often been found to be low (e.g. L4 to L6-IT and CT), have been omitted. A, Hypothesized patterns of excitatory input to each major cortical excitatory class. For clarity, many connections are drawn as going to the dendrites of the postsynaptic neurons within the same layer as the presynaptic neurons; however, available evidence suggests that inputs tend to go mostly to the perisomatic dendrites . B, Hypothesized patterns of output from each excitatory class onto other excitatory classes.
Figure 5
Figure 5
Hypothesized homologous hodology of inter-areal connectivity. A, In primate neocortex, FF and FB streams have characteristic layers of origin and termination. B, In mouse visual cortex, FF and FB projections from an intermediate area (LM) arise from distinct IT subclasses that are intermingled within L2/3, as demonstrated by retrograde tracer injections into the upstream and downstream areas (adapted with permission from Ref. ). Scale bar 50 μm. C, In rat secondary sensory cortices, a subclass of L6 neurons expressing latexin project back to the corresponding primary sensory region but not to thalamus, higher-order cortex, or contralateral cortex (adapted with permission from Ref. ). Scale bar 200 μm. D, In mouse S1, two distinct subclasses of L2/3 neurons project to M1 and S2, both of which would be considered FF projections. Reconstructed neurons are adapted with permission from Ref. . Note the callosally projecting axons of both neurons (branches to the right), a defining feature of IT neurons.
Figure 6
Figure 6
Sequential hodology of three major inhibitory cell classes. All classes receive inputs from local ECs. Vip cells (a subclass of Htr3a interneurons) receive input from higher-order cortex, and inhibit primarily other interneuron classes. Sst cells inhibit Pvalb cells and the dendrites of ECs. Pvalb cells receive strong feedforward inputs from thalamus and lower-order cortex, and inhibit ECs perisomatically. Note that multiple additional interneuron classes exist, whose hodology is not yet fully established.
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