Cerebral cortical processing time is elongated in human brain evolution

Kosuke Itoh,Satoshi Hirata,Hironaka Igarashi,Katsuki Nakamura,Haruhiko Iwaoki,Masafumi Nejime,Naho Konoike

doi:10.1038/s41598-022-05053-w

Abstract

An increase in number of neurons is presumed to underlie the enhancement of cognitive abilities in brain evolution. The evolution of human cognition is then expected to have accompanied a prolongation of net neural-processing time due to the accumulation of processing time of individual neurons over an expanded number of neurons. Here, we confirmed this prediction and quantified the amount of prolongation in vivo, using noninvasive measurements of brain responses to sounds in unanesthetized human and nonhuman primates. Latencies of the N1 component of auditory-evoked potentials recorded from the scalp were approximately 40, 50, 60, and 100 ms for the common marmoset, rhesus monkey, chimpanzee, and human, respectively. Importantly, the prominent increase in human N1 latency could not be explained by the physical lengthening of the auditory pathway, and therefore reflected an extended dwell time for auditory cortical processing. A longer time window for auditory cortical processing is advantageous for analyzing time-varying acoustic stimuli, such as those important for speech perception. A novel hypothesis concerning human brain evolution then emerges: the increase in cortical neuronal number widened the timescale of sensory cortical processing, the benefits of which outweighed the disadvantage of slow cognition and reaction.

Highlights

An increase in number of neurons is presumed to underlie the enhancement of cognitive abilities in brain evolution
Recent studies have shown that brain size is not a reliable predictor of the number of cortical neurons when compared across c lade[3], cerebral neuronal number increases with brain size within a clade, and primates have the highest density of cortical neurons among other mammals of similar brain size[4]
The total neural-processing time for executing a brain function is expected to become longer unless (1) all evolutionarily acquired cortical neurons operate in parallel with previously existing neural circuits, or unless (2) the temporal integration time of individual neurons is shortened with the increase in the total neuronal number

Summary

Introduction

An increase in number of neurons is presumed to underlie the enhancement of cognitive abilities in brain evolution. We used scalp electroencephalogram (EEG) to measure the speed at which neural circuits in the cerebral cortex process sensory information in four living primates: the human (Homo sapiens), chimpanzee (Pan troglodytes), rhesus monkey (Macaca mulatta), and common marmoset (Callithrix jacchus). These species have vastly different brain sizes and considerably different number of neurons (Table 1). Scalp EEG has recently been applied to nonhuman primates as a novel and powerful tool in comparative neurophysiology, as it reveals species differences in neural processing that underpin the evolution of cognition and b ehavior[8,9,10,11,12,13,14]

Methods

Results

Conclusion