Canonical computations of cerebral cortex
Section snippets
A cortical computational unit?
The cerebral cortex performs a wide range of cognitive tasks in mammals — sensory, motor, and everything in between. Yet it processes these diverse tasks with what appears to be a remarkably uniform, primarily six-layer architecture, albeit with significant differences in details across species and cortical areas [1, 2, 3•, 4, 5, 6, 7, 8, 9, 10, 11•, 12, 13, 14]. Dense connectivity is generally restricted to horizontal extents (parallel to the layers) of a few hundred microns [e.g. 15]. This has
Canonical local computations
Here we review ideas for these two canonical computations within a sensory cortical area: computation of selectivity and computation of gain.
Challenges for understanding canonical cortical computations
The unknowns and challenges greatly outweigh our current understandings. Obviously we need to better understand computations within the local circuit, including those specific for cell type and/or layer; the hierarchical computations across cortical areas, including the role in the latter of feedback [e.g. 19, 124, 125, 126, 127, 128] as well as feedforward connections; and the role of structural variations between cortical areas and across species [e.g. 1, 2, 3•, 4, 5, 6, 7, 8, 9]. Additional
Conclusions
The rapid growth of cortical surface area in mammalian evolution suggests the development of a ‘canonical’ computational unit that, deployed in great numbers both within cortical areas and hierarchically across cortical areas, along with some specializations across species and areas, allowed the evolution of mammalian intelligence. We have outlined here some current ideas as to some elements of this computational unit. We can only hope that in coming decades our understandings will grow more
Conflict of interest
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
Thanks to Roozbeh Kiani for helpful comments. Work and writing were supported by the Gatsby Charitable Foundation and R01-EY11001.
References (143)
- et al.
Transcriptional architecture of the primate neocortex
Neuron
(2012) In search of a unifying theory of complex brain evolution
Ann N Y Acad Sci
(2009)Local circuits in primary visual cortex of the macaque monkey
Ann Rev Neurosci
(1998)- et al.
Cortical interneurons that specialize in disinhibitory control
Nature
(2013) - et al.
A disinhibitory circuit mediates motor integration in the somatosensory cortex
Nat Neurosci
(2013) - et al.
Cellular mechanisms of brain state-dependent gain modulation in visual cortex
Nat Neurosci
(2013) Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes
Trends Cogn Sci (Regul Ed)
(2008)- et al.
Is the rostro-caudal axis of the frontal lobe hierarchical?
Nat Rev Neurosci
(2009) - et al.
Tuned thalamic excitation is amplified by visual cortical circuits
Nat Neurosci
(2013) - et al.
Linear transformation of thalamocortical input by intracortical excitation
Nat Neurosci
(2013)
Cortex is driven by weak but synchronously active thalamocortical synapses
Science
Mechanisms of neuronal computation in mammalian visual cortex
Neuron
Contrast-invariant orientation tuning in cat visual cortex: feedforward tuning and correlation-based intracortical connectivity
J Neurosci
Development of spatiotemporal receptive fields of simple cells: II. Simulation and analysis
Biol Cybern
Effects of inhibitory gain and conductance fluctuations in a simple model for contrast-invariant orientation tuning in cat v1
J Neurophysiol
Orientation selectivity in inhibition-dominated networks of spiking neurons: effect of single neuron properties and network dynamics
PLoS Comput Biol
Response facilitation from the “suppressive” receptive field surround of macaque V1 neurons
J Neurophysiol
Contrast's effect on spatial summation by macaque v1 neurons
Nat Neurosci
Membrane potential and conductance changes underlying length tuning of cells in cat primary visual cortex
J Neurosci
General cortical and special prefrontal connections: principles from structure to function
Annu Rev Neurosci
Systematic, cross-cortex variation in neuron numbers in rodents and primates
Cereb Cortex
Microstructure of the neocortex: comparative aspects
J Neurocytol
The basic nonuniformity of the cerebral cortex
Proc Natl Acad Sci U S A
Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species
Brain Res
Predicting visual acuity from the structure of visual cortex
Proc Natl Acad Sci U S A
Different scaling of white matter volume, cortical connectivity, and gyrification across rodent and primate brains
Front Neuroanat
Structural uniformity of neocortex, revisited
Proc Natl Acad Sci U S A
The neocortical circuit: themes and variations
Nat Neurosci
Microcolumns in the cerebral cortex
Proc Natl Acad Sci U S A
Evolution and development of the mammalian cerebral cortex
Brain Behav Evol
Confusing cortical columns
Proc Natl Acad Sci U S A
Principles of connectivity among morphologically defined cell types in adult neocortex
Science
Ferrier lecture: functional architecture of macaque monkey visual cortex
Proc R Soc Lond B
Perceptual Neuroscience: The Cerebral Cortex
On the evolution and geometry of the brain in mammals
Prog Neurobiol
Distributed hierarchical processing in the primate cerebral cortex
Cereb Cortex
Deep cortical layers are activated directly by thalamus
Science
A direct translaminar inhibitory circuit tunes cortical output
Nat Neurosci
Distinct functions for direct and transthalamic corticocortical connections
J Neurophysiol
Three types of cortical layer 5 neurons that differ in brain-wide connectivity and function
Neuron
The stimulus selectivity and connectivity of layer six principal cells reveals cortical microcircuits underlying visual processing
Neuron
A cortical circuit for gain control by behavioral state
Cell
A cortical disinhibitory circuit for enhancing adult plasticity
Elife
Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing
Science
The organization of two new cortical interneuronal circuits
Nat Neurosci
Translaminar inhibitory cells recruited by layer 6 corticothalamic neurons suppress visual cortex
Neuron
From circuit motifs to computations: mapping the behavioral repertoire of cortical interneurons
Curr Opin Neurobiol
Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons
Nat Neurosci
A canonical microcircuit for neocortex
Neural Comput
Normalization as a canonical neural computation
Nat Rev Neurosci
Cited by (71)
What is the dynamical regime of cerebral cortex?
2021, NeuronCitation Excerpt :A third distinction is whether a network goes to a stable fixed rate of firing for a fixed input (with noisy fluctuations about that fixed rate given noisy inputs) or whether it shows more complex behaviors, such as movement between multiple fixed points, oscillations, or chaotic wandering of firing rates. We will focus on the case of a single stable fixed point, which seems likely to reasonably approximate at least awake sensory cortex (see discussion in Miller, 2016). Finally, for a given fixed point, recurrent excitation may be strong enough to destabilize the fixed point in the absence of feedback inhibition.
Encoding of 3D Head Orienting Movements in the Primary Visual Cortex
2020, NeuronCitation Excerpt :Despite the number of various movements animals make to support visual perception, vision has typically been studied by presenting stimuli to restrained animals. In this framework, vision is a passive sense and visual processing is a feedforward computation in which information enters the brain through the retina and is processed one stage at a time as it travels deeper into the brain, through thalamus and cortex (Hubel and Wiesel, 1962; Felleman and Van Essen, 1991; DiCarlo and Cox, 2007; Miller, 2016). Consistent with this view, the majority of neurophysiological experiments on primary sensory cortical areas have found that information in those areas is chiefly sensory in nature.
Rodents’ visual gamma as a biomarker of pathological neural conditions
2024, Journal of PhysiologyDecomposing neural circuit function into information processing primitives
2024, Journal of Neuroscience