Elsevier

Biological Psychiatry

Volume 81, Issue 10, 15 May 2017, Pages 832-837
Biological Psychiatry

Review
Vision as a Beachhead

https://doi.org/10.1016/j.biopsych.2016.09.019Get rights and content

Abstract

When neural circuits develop abnormally due to different genetic deficits and/or environmental insults, neural computations and the behaviors that rely on them are altered. Computational theories that relate neural circuits with specific quantifiable behavioral and physiological phenomena, therefore, serve as extremely useful tools for elucidating the neuropathological mechanisms that underlie different disorders. The visual system is particularly well suited for characterizing differences in neural computations; computational theories of vision are well established, and empirical protocols for measuring the parameters of those theories are well developed. In this article, we examine how psychophysical and neuroimaging measurements from human subjects are being used to test hypotheses about abnormal neural computations in autism, with an emphasis on hypotheses regarding potential excitation/inhibition imbalances. We discuss the complexity of relating specific computational abnormalities to particular underlying mechanisms given the diversity of neural circuits that can generate the same computation, and we discuss areas of research in which computational theories need to be further developed to provide useful frameworks for interpreting existing results. A final emphasis is placed on the need to extend existing ideas into developmental frameworks that take into account the dramatic developmental changes in neurophysiology (e.g., changes in excitation/inhibition balance) that take place during the first years of life, when autism initially emerges.

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.

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