Canonical Cortical Microcircuit Research Articles

Exploring the Architectural Biases of the Canonical Cortical Microcircuit.

The cortex plays a crucial role in various perceptual and cognitive functions, driven by its basic unit, the canonical cortical microcircuit. Yet, we remain short of a framework that definitively explains the structure-function relationships of this fundamental neuroanatomical motif. To better understand how physical substrates of cortical circuitry facilitate their neuronal dynamics, we employ a computational approach using recurrent neural networks and representational analyses. We examine the differences manifested by the inclusion and exclusion of biologically-motivated inter-areal laminar connections on the computational roles of different neuronal populations in the microcircuit of two hierarchically-related areas, throughout learning. Our findings show that the presence of feedback connections correlates with the functional modularization of cortical populations in different layers, and provides the microcircuit with a natural inductive bias to differentiate expected and unexpected inputs at initialization. Furthermore, when testing the effects of training the microcircuit and its variants with a predictive-coding inspired strategy, we find that doing so helps better encode noisy stimuli in areas of the cortex that receive feedback, all of which combine to suggest evidence for a predictive-coding mechanism serving as an intrinsic operative logic in the cortex.

Synaptic connectivity to L2/3 of primary visual cortex measured by two-photon optogenetic stimulation.

Understanding cortical microcircuits requires thorough measurement of physiological properties of synaptic connections formed within and between diverse subclasses of neurons. Towards this goal, we combined spatially precise optogenetic stimulation with multicellular recording to deeply characterize intralaminar and translaminar monosynaptic connections to supragranular (L2/3) neurons in the mouse visual cortex. The reliability and specificity of multiphoton optogenetic stimulation were measured across multiple Cre lines, and measurements of connectivity were verified by comparison to paired recordings and targeted patching of optically identified presynaptic cells. With a focus on translaminar pathways, excitatory and inhibitory synaptic connections from genetically defined presynaptic populations were characterized by their relative abundance, spatial profiles, strength, and short-term dynamics. Consistent with the canonical cortical microcircuit, layer 4 excitatory neurons and interneurons within L2/3 represented the most common sources of input to L2/3 pyramidal cells. More surprisingly, we also observed strong excitatory connections from layer 5 intratelencephalic neurons and potent translaminar inhibition from multiple interneuron subclasses. The hybrid approach revealed convergence to and divergence from excitatory and inhibitory neurons within and across cortical layers. Divergent excitatory connections often spanned hundreds of microns of horizontal space. In contrast, divergent inhibitory connections were more frequently measured from postsynaptic targets near each other.

Laminar processing of numerosity supports a canonical cortical microcircuit in human parietal cortex

As neural signals travel through the visual hierarchy, spatial precision decreases and specificity for stimulus features increases.1-4 A similar hierarchy has been found for laminar processing in V1, where information from the thalamus predominantly targets the central layers, while spatial precision decreases and feature specificity increases toward superficial and deeper layers.5-17 This laminar processing scheme is proposed to represent a canonical cortical microcircuit that is similar across the cortex.11,18-21 Here, we go beyond early visual cortex and investigate whether processing of numerosity (the set size of a group of items) across cortical depth in the parietal association cortex follows this hypothesis. Numerosity processing is implicated in many tasks such as multiple object tracking,22 mathematics,23-25 decision making,26 and dividing attention.27 Neurons in the parietal association cortex are tuned to numerosity, with both a preferred numerosity tuning and tuning width (i.e., specificity).28-30 We quantified preferred numerosity responses across cortical depth in the parietal association cortex with ultra-high field fMRI and population receptive field-based numerosity modeling.1,28,31 We find that numerosity responses sharpen, i.e., become increasingly specific, moving away from the central layers. This suggests that the laminar processing scheme for numerosity processing in the parietal cortex is similar to primary visual cortex, providing support for the canonical cortical microcircuit hypothesis beyond primary visual cortex.

Layer 4 Gates Plasticity in Visual Cortex Independent of a Canonical Microcircuit

Disrupting binocular vision during a developmental critical period can yield enduring changes to ocular dominance (OD) in primary visual cortex (V1). Here we investigated how this experience-dependent plasticity is coordinated within the laminar circuitry of V1 by deleting separately in each cortical layer (L) a gene required to close the critical period, nogo-66 receptor (ngr1). Deleting ngr1 in excitatory neurons in L4, but not in L2/3, L5, or L6, prevented closure of the critical period, and adult mice remained sensitive to brief monocular deprivation. Intracortical disinhibition, but not thalamocortical disinhibition, accompanied this OD plasticity. Both juvenile wild-type mice and adult mice lacking ngr1 in L4 displayed OD plasticity that advanced more rapidly L4 than L2/3 or L5. Interestingly, blocking OD plasticity in L2/3 with the drug AM-251 did not impair OD plasticity in L5. We propose that L4 restricts disinhibition and gates OD plasticity independent of a canonical cortical microcircuit.

The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina

The canonical cortical microcircuit has principally been defined by interlaminar excitatory connections among the six layers of the neocortex. However, excitatory neurons in layer 6 (L6), a layer whose functional organization is poorly understood, form relatively rare synaptic connections with other cortical excitatory neurons. Here, we show that the vast majority of parvalbumin inhibitory neurons in a sublamina within L6 send axons through the cortical layers toward the pia. These interlaminar inhibitory neurons receive local synaptic inputs from both major types of L6 excitatory neurons and receive stronger input from thalamocortical afferents than do neighboring pyramidal neurons. The distribution of these interlaminar interneurons and their synaptic connectivity further support a functional subdivision within the standard six layers of the cortex. Positioned to integrate local and long-distance inputs in this sublayer, these interneurons generate an inhibitory interlaminar output. These findings call for a revision to the canonical cortical microcircuit.

Coding principles of the canonical cortical microcircuit in the avian brain

Mammalian neocortex is characterized by a layered architecture and a common or "canonical" microcircuit governing information flow among layers. This microcircuit is thought to underlie the computations required for complex behavior. Despite the absence of a six-layered cortex, birds are capable of complex cognition and behavior. In addition, the avian auditory pallium is composed of adjacent information-processing regions with genetically identified neuron types and projections among regions comparable with those found in the neocortex. Here, we show that the avian auditory pallium exhibits the same information-processing principles that define the canonical cortical microcircuit, long thought to have evolved only in mammals. These results suggest that the canonical cortical microcircuit evolved in a common ancestor of mammals and birds and provide a physiological explanation for the evolution of neural processes that give rise to complex behavior in the absence of cortical lamination.

Microcircuitry of Agranular Frontal Cortex: Testing the Generality of the Canonical Cortical Microcircuit

We investigated whether a frontal area that lacks granular layer IV, supplementary eye field, exhibits features of laminar circuitry similar to those observed in primary sensory areas. We report, for the first time, visually evoked local field potentials (LFPs) and spiking activity recorded simultaneously across all layers of agranular frontal cortex using linear electrode arrays. We calculated current source density from the LFPs and compared the laminar organization of evolving sinks to those reported in sensory areas. Simultaneous, transient synaptic current sinks appeared first in layers III and V followed by more prolonged current sinks in layers I/II and VI. We also found no variation of single- or multi-unit visual response latency across layers, and putative pyramidal neurons and interneurons displayed similar response latencies. Many units exhibited pronounced discharge suppression that was strongest in superficial relative to deep layers. Maximum discharge suppression also occurred later in superficial than in deep layers. These results are discussed in the context of the canonical cortical microcircuit model originally formulated to describe early sensory cortex. The data indicate that agranular cortex resembles sensory areas in certain respects, but the cortical microcircuit is modified in nontrivial ways.

Coherent Infomax as a Computational Goal for Neural Systems

Signal processing in the cerebral cortex is thought to involve a common multi-purpose algorithm embodied in a canonical cortical micro-circuit that is replicated many times over both within and across cortical regions. Operation of this algorithm produces widely distributed but coherent and relevant patterns of activity. The theory of Coherent Infomax provides a formal specification of the objectives of such an algorithm. It also formally derives specifications for both the short-term processing dynamics and for the learning rules whereby the connection strengths between units in the network can be adapted to the environment in which the system finds itself. A central assumption of the theory is that the local processors can combine reliable signal coding with flexible use of those codes because they have two classes of synaptic connection: driving connections which specify the information content of the neural signals, and contextual connections which modulate that signal processing. Here, we make the biological relevance of this theory more explicit by putting more emphasis upon the contextual guidance of ongoing processing, by showing that Coherent Infomax is consistent with a particular Bayesian interpretation for the contextual guidance of learning and processing, by explicitly specifying rules for on-line learning, and by suggesting approximations by which the learning rules can be made computationally feasible within systems composed of very many local processors.

The quantum brain: the search for freedom and the next generation of man

THE QUANTUM BRAIN. Introduction: The Quantum Crisis. Mind Out of Matter--The Machinery of the Fourth Brain. Opening the Mind's Eye. Death and Birth. Teaching a Young Dog Old Tricks. The Wet Net. Spinning the Glass Fantastic. The Game of Life, or How the Leopard Gets Its Spots. By Your Bootstraps. Is Man a Machine? MIRACLES. The Insoluble Solution. EPR: Wanted: Dead or Alive. E Unus Pluribum--Out of One Mystery, Many. Stranger in a Strange Land (The Stranger the Better). In the Matter of Mind. The Protean Computer. To Fickle Chance, and Chaos Judge the Strife. Quantum Ripples. Appendix A: The Simplest Hopfield Net and the Canonical Cortical Microcircuit. Appendix B: The Tuszynski Microtubule Model. Appendix C: Coherence and Decoherence. Notes. Credits. Index.