A Tradeoff in the Neural Code across Regions and Species

Cell. 2019 Jan 24;176(3):597-609.e18. doi: 10.1016/j.cell.2018.12.032. Epub 2019 Jan 17.

Abstract

Many evolutionary years separate humans and macaques, and although the amygdala and cingulate cortex evolved to enable emotion and cognition in both, an evident functional gap exists. Although they were traditionally attributed to differential neuroanatomy, functional differences might also arise from coding mechanisms. Here we find that human neurons better utilize information capacity (efficient coding) than macaque neurons in both regions, and that cingulate neurons are more efficient than amygdala neurons in both species. In contrast, we find more overlap in the neural vocabulary and more synchronized activity (robustness coding) in monkeys in both regions and in the amygdala of both species. Our findings demonstrate a tradeoff between robustness and efficiency across species and regions. We suggest that this tradeoff can contribute to differential cognitive functions between species and underlie the complementary roles of the amygdala and the cingulate cortex. In turn, it can contribute to fragility underlying human psychopathologies.

Keywords: amygdala; anxiety/mood disorders; cingulate-cortex; cognition; efficiency; evolution; neural code; primates; robustness.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Amygdala / physiology*
  • Animals
  • Biological Evolution
  • Child
  • Child, Preschool
  • Cognition / physiology
  • Emotions / physiology
  • Female
  • Gyrus Cinguli / physiology*
  • Humans
  • Macaca
  • Macaca mulatta
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Nerve Net / metabolism
  • Nerve Net / physiology
  • Neurons / physiology*
  • Prefrontal Cortex / physiology
  • Species Specificity