ReviewVision as a Beachhead
Section snippets
Computational theory
The neocortex has a modular design with modular circuits and with modular computations. Anatomical evidence suggests the existence of canonical microcircuits that are replicated across cortical areas (32, 33). Consequently, it has been hypothesized that the brain relies on a set of canonical neural computations, repeating them across brain regions and sensory modalities and thereby applying similar operations of the same form, hierarchically, to achieve different behavioral goals (34, 35, 36, 37
Binocular rivalry
A perceptual phenomenon called binocular rivalry occurs when incompatible monocular images are presented to the two eyes (46, 47). For example, when one eye is presented with an oriented grating and the other eye is presented with an orthogonally oriented grating, separate neural populations in early visual cortex represent each of the stimuli and actively compete, such that observers experience alternating periods of dominance in which one grating is visible and the other is invisible or
Normalization
Divisive normalization is a canonical computation that explains stimulus-evoked neural responses apparent in many brain systems across multiple species (38, 55). The defining characteristic of normalization is that the response of each neuron is divided by a factor that includes the summed activity of a pool of neurons. For example, in V1, the normalization pool (the neurons that contribute to the denominator) may include neurons selective for a range of orientations and spatial positions
Reliability of sensory-evoked responses
The original E/I imbalance hypothesis of autism proposed that E/I imbalances would generate abnormally noisy/variable neural activity (1). Several psychophysics studies have indeed reported greater trial-to-trial variability in ratings of tactile pleasantness (68) or roughness (69). Individuals with autism also exhibit more variable movement kinematics, as documented by several motor control studies (70). Furthermore, high-functioning adults with autism exhibit excessive trial-to-trial
Minimizing energy, maximizing information transfer
Maintaining a gross E/I balance in the brain is a fundamental necessity due to the limited availability of energy. The human brain consumes about 20% of the body’s energy during rest in adulthood and about 50% in childhood (77). Most of this energy is used for neural signaling/spiking (78), which requires maintaining and restoring ionic balances (Na+/K+ and Ca2+) and recycling the glutamate that is released by excitatory neurons that comprise 80–90% of the neurons in the cortex (79). The energy
Conclusions
Although there is indeed evidence that larger E/I ratios may contribute to the abnormal development of autism, it is important to remember that other studies have reported decreased E/I ratios in autism. These include reports of several autism animal models that exhibit abnormally low excitation (93), abnormally high inhibition (94), or a mixture of different imbalances in different brain areas (95). These findings demonstrate the heterogeneity of underlying etiologies in different subgroups of
Acknowledgments and disclosures
This work was supported by the U.S.-Israel Binational Science Foundation (Grant No. 2011242 to MB) and the Israeli Science Foundation (Grant No. 961/14 to ID).
All authors report no biomedical financial interests or potential conflicts of interest.
References (95)
- et al.
A computational model for cerebral cortical dysfunction in autism spectrum disorders
Biol Psychiatry
(2010) - et al.
Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism
Neuron
(2011) - et al.
Genetic analysis of GABRB3 as a candidate gene of autism spectrum disorders
Mol Autism
(2014) - et al.
Review Epilepsy in autism
(2002) - et al.
Excitatory/inhibitory balance and circuit homeostasis in autism spectrum disorders
Neuron
(2015) - et al.
Interictal epileptiform activity and autism
Epilepsy Behav
(2015) - et al.
Chronic epilepsy and cognition
Lancet Neurol
(2004) - et al.
Effect of age of onset of temporal lobe epilepsy on the severity and the nature of preoperative memory deficits
Neuropsychologia
(2002) - et al.
Neurodevelopmental outcome of infantile spasms: A systematic review and meta-analysis
Epilepsy Res
(2015) - et al.
Neural mechanisms of object recognition
Curr Opin Neurobiol
(2002)
A model of neuronal responses in visual area MT
Vision Res
Canonical computations of cerebral cortex
Curr Opin Neurobiol
Adaptive rescaling maximizes information transmission
Neuron
Canonical microcircuits for predictive coding
Neuron
Mapping early brain development in autism
Neuron
Normal binocular rivalry in autism: Implications for the excitation/inhibition imbalance hypothesis
Vision Res
Reduced GABAergic action in the autistic brain
Curr Biol
Divisive normalization in olfactory population codes
Neuron
Unreliable evoked responses in autism
Neuron
Neural variability: Friend or foe?
Trends Cogn Sci
Intra-individual variability in behavior: Links to brain structure, neurotransmission and neuronal activity
Trends Neurosci
The cost of cortical computation
Curr Biol
Synaptic energy use and supply
Neuron
Model of autism: Increased ratio of excitation/inhibition in key neural systems
Genes, Brain Behav
The Intense World Syndrome – An alternative hypothesis for autism
Front Neurosci
Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism
Proc Natl Acad Sci U S
Investigation of autism and GABA receptor subunit genes in multiple ethnic groups
Neurogenetics
GABA(A) receptor downregulation in brains of subjects with autism
J Autism Dev Disord
Downregulation of GABAA receptor protein subunits α6, β2, δ, ε, γ2, θ, and ρ2 in superior frontal cortex of subjects with autism
J Autism Dev Disord
Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes
Nature
Common circuit defect of excitatory-inhibitory balance in mouse models of autism
J Neurodev Disord
Neocortical excitation/inhibition balance in information processing and social dysfunction
Nature
Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid
Cereb Cortex
The neurobiology of epilepsy
Curr Neurol Neurosci Rep
Autism spectrum disorder and epilepsy: Two sides of the same coin?
J Child Neurol
Impaired excitability of somatostatin- and parvalbumin-expressing cortical interneurons in a mouse model of Dravet syndrome
Proc Natl Acad Sci U S A
The Landau-Kleffner Syndrome
Epilepsy Curr
Critical period plasticity in local cortical circuits
Nat Rev Neurosci
The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation
Nature
Functional role of ambient GABA in refining neuronal circuits early in postnatal development
Front Neural Circuits
Development of the human cerebral cortex: Boulder Committee revisited
Nat Rev Neurosci
Developmental sensory experience balances cortical excitation and inhibition
Nature
Is birth a critical period in the pathogenesis of autism spectrum disorders?
Nat Rev Neurosci
Changing Brains: Applying Brain Plasticity to Advance and Recover Human Ability
Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement
Annu Rev Neurosci
A functional microcircuit for cat visual cortex
J Physiol
Recurrent excitation in neocortical circuits
Science
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