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Increased brain signal variability accompanies lower behavioral variability in development.

ABSTRACT: As the brain matures, its responses become optimized. Behavioral measures show this through improved accuracy and decreased trial-to-trial variability. The question remains whether the supporting brain dynamics show a similar decrease in variability. We examined the relation between variability in single trial evoked electrical activity of the brain (measured with EEG) and performance of a face memory task in children (8-15 y) and young adults (20-33 y). Behaviorally, children showed slower, more variable response times (RT), and less accurate recognition than adults. However, brain signal variability increased with age, and showed strong negative correlations with intrasubject RT variability and positive correlations with accuracy. Thus, maturation appears to lead to a brain with greater functional variability, which is indicative of enhanced neural complexity. This variability may reflect a broader repertoire of metastable brain states and more fluid transitions among them that enable optimum responses. Our results suggest that the moment-to-moment variability in brain activity may be a critical index of the cognitive capacity of the brain.

SUBMITTER: McIntosh AR

PROVIDER: S-EPMC2429973 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

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Increased brain signal variability accompanies lower behavioral variability in development.

McIntosh Anthony Randal AR Kovacevic Natasa N Itier Roxane J RJ

PLoS computational biology 20080704 7

As the brain matures, its responses become optimized. Behavioral measures show this through improved accuracy and decreased trial-to-trial variability. The question remains whether the supporting brain dynamics show a similar decrease in variability. We examined the relation between variability in single trial evoked electrical activity of the brain (measured with EEG) and performance of a face memory task in children (8-15 y) and young adults (20-33 y). Behaviorally, children showed slower, mor ...[more]

PMID: 18604265

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Project description:The analysis of brain signal variability is a promising approach to understand pathological brain function related to chronic pain. This study investigates whether blood-oxygen-level-dependent signal variability (BOLDSV) in specific frequency bands is altered in temporomandibular disorder (TMD) and correlated to its clinical features. Twelve patients with chronic myofascial TMD and 24 healthy controls (HCs) underwent resting-state functional magnetic resonance imaging. The BOLDSV was measured as the standard deviation of the BOLD time series at each voxel and compared between groups. We also examined the potential relationship between the BOLDSV and the catechol-O-methyltransferase (COMT) Val158Met polymorphism. We assessed sensory-discriminative pain in the craniofacial region, pain sensitivity to sustained masseteric pain challenge, and TMD pain frequency for clinical correlation. Patients displayed reduced BOLDSV in the dorsolateral prefrontal cortex (dlPFC) as compared with HC in all frequency bands. In the slow-3 band, patients also showed reduced BOLDSV in the medial dorsal thalamus, primary motor cortex (M1), and primary somatosensory cortex (S1) and heightened BOLDSV in the temporal pole. Notably, we found a significant correlation between lower BOLDSV (slow-3) in the orofacial M1/S1 regions and higher clinical pain (intensity/area) and higher sensitivity of the masseter muscle pain. Moreover, lower BOLDSV (slow-3) in the dlPFC and ventrolateral PFC was associated with a higher TMD pain frequency. Participants who had the COMT 158Met substitution exhibited lower BOLDSV in the dlPFC and higher BOLDSV in the temporal pole as compared with participants without the COMT 158Met substitution. An increasing number of Met alleles was associated with lower dlPFC and greater temporal pole BOLDSV in both HC and TMD groups. Together, we demonstrated that chronic TMD patients exhibit aberrant BOLDSV in the top-down pain modulatory and sensorimotor circuits associated with their pain frequency and severity. COMT Val158Met polymorphism might affect clinical symptoms in association with regional brain signal variability, specifically involved in cognitive and emotional regulation of pain.

Project description:Animals engaged in naturalistic behavior can exhibit a large degree of behavioral variability even under sensory invariant conditions. Such behavioral variability can include not only variations of the same behavior, but also variability across qualitatively different behaviors driven by divergent cognitive states, such as fight-or-flight decisions. However, the neural circuit mechanisms that generate such divergent behaviors across trials are not well understood. To investigate this question, here we studied the visual-evoked responses of larval zebrafish to moving objects of various sizes, which we found exhibited highly variable and divergent responses across repetitions of the same stimulus. Given that the neuronal circuits underlying such behaviors span sensory, motor, and other brain areas, we built a novel Fourier light field microscope which enables high-resolution, whole-brain imaging of larval zebrafish during behavior. This enabled us to screen for neural loci which exhibited activity patterns correlated with behavioral variability. We found that despite the highly variable activity of single neurons, visual stimuli were robustly encoded at the population level, and the visual-encoding dimensions of neural activity did not explain behavioral variability. This robustness despite apparent single neuron variability was due to the multi-dimensional geometry of the neuronal population dynamics: almost all neural dimensions that were variable across individual trials, i.e. the "noise" modes, were orthogonal to those encoding for sensory information. Investigating this neuronal variability further, we identified two sparsely-distributed, brain-wide neuronal populations whose pre-motor activity predicted whether the larva would respond to a stimulus and, if so, which direction it would turn on a single-trial level. These populations predicted single-trial behavior seconds before stimulus onset, indicating they encoded time-varying internal modulating behavior, perhaps organizing behavior over longer timescales or enabling flexible behavior routines dependent on the animal's internal state. Our results provide the first whole-brain confirmation that sensory, motor, and internal variables are encoded in a highly mixed fashion throughout the brain and demonstrate that de-mixing each of these components at the neuronal population level is critical to understanding the mechanisms underlying the brain's remarkable flexibility and robustness.

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Increased brain signal variability accompanies lower behavioral variability in development.

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Increased brain signal variability accompanies lower behavioral variability in development.

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