Role of Oscillations in Auditory Temporal Processing: A General Model for Temporal Processing of Sensory Information in the Brain?

Abstract

We review the role of oscillations in the brain and in the auditory system showing that the ability of humans to distinguish changes in pitch can be explained as a precise analysis of temporal information in auditory signals by neural oscillations. The connections between auditory brain stem chopper neurons construct neural oscillators, which discharge spikes at various constant intervals that are integer multiples of 0.4 ms, contributing to the temporal processing of auditory cochlear output. This is subsequently spatially mapped in the inferior colliculus. Electrophysiological measurements of auditory chopper neurons in different species show oscillations with periods which are integer multiples of 0.4 ms. The constant intervals of 0.4 ms can be attributed to the smallest synaptic delay between interconnected simulated chopper neurons. We also note the patterns of similarities between microcircuits in the brain stem and other parts of the brain (e.g., the pallidum, reticular formation, locus coeruleus, oculomotor nuclei, limbic system, amygdala, hippocampus, basal ganglia and substantia nigra), dedicated to the processing of temporal information. Similarities in microcircuits across the brain reflect the importance of one of the key mechanisms in the information processing in the brain, namely the temporal coupling of different neural events via coincidence detection.

Increase in Mutual Information During Interaction of the Brain with Environment Contributes to Perception

“…This reduction in the total entropy of multiple pairs of circuits in networks, by an amount equal to the increase of mutual information among them, occurs as sensory information is processed successively from lower to higher cortical areas or between different areas at the same hierarchical level but belonging to different networks. The increase in mutual information is partly accounted by temporal coupling as well as synaptic connections as proposed by Bahmer and Gupta [1]. We propose that robust increases in mutual information, measuring the association between the characteristics of sensory inputs and neural circuits connectivity patterns, are partly responsible for perception and successful motor interactions with physical surroundings.…”

“…We also consider sparse coding as a source of large amount of information available for processing perception and motor interaction. Bahmer and Gupta [1] have argued that dense coding from gamma oscillations, such as those present in lower cortical areas can be transformed into sparse codes with the help of an integration process that involves coincidence detection by at least two other neural events, namely, low frequency oscillations that synchronizes different circuits [11] and commonly observed ramping activities of cortical neurons [12][13][14]. This integration process, which generates a sparse code from a dense code via coincidence detection, would be responsible for generating information that underlies perception.…”

“…Although an increase in mutual information parallels a dynamic representation of external environment, information representing external stimuli and perceptual objects, such as for working memory and episodic memory could be generated by sparse coding for online perception and action [1].…”

“…This schematic (adapted from Bahmer and Gupta [1]) depicts the coincidence detection (D) leading to the activation of a set of neurons. This sparse set of neurons are activated (D) when excitatory phase of low frequency oscillation (B) coincides with gamma synchronized synaptic discharge [65] from ramping neurons (A).…”

“…However, experimental evidences supporting the role of synchronization in the temporal coupling of neuronal responses in processing stimulusspecific features were provided later by Singer laboratory [31][32][33]. Neuenschwander and Singer [32] demonstrated that temporal coupling among responses of spatially segregated ganglion cells can be exploited to convey information relevant for perceptual grouping [1]. Bahmer and Gupta [1] have recently argued based on studies of other perceptual functions, including auditory, olfactory and interval-timing that temporal correlations between neural events form an important basis of perception.…”