Novelty-Sensitive Dopaminergic Neurons in the Human Substantia Nigra Predict Success of Declarative Memory Formation

Curr Biol. 2018 May 7;28(9):1333-1343.e4. doi: 10.1016/j.cub.2018.03.024. Epub 2018 Apr 12.

Abstract

The encoding of information into long-term declarative memory is facilitated by dopamine. This process depends on hippocampal novelty signals, but it remains unknown how midbrain dopaminergic neurons are modulated by declarative-memory-based information. We recorded individual substantia nigra (SN) neurons and cortical field potentials in human patients performing a recognition memory task. We found that 25% of SN neurons were modulated by stimulus novelty. Extracellular waveform shape and anatomical location indicated that these memory-selective neurons were putatively dopaminergic. The responses of memory-selective neurons appeared 527 ms after stimulus onset, changed after a single trial, and were indicative of recognition accuracy. SN neurons phase locked to frontal cortical theta-frequency oscillations, and the extent of this coordination predicted successful memory formation. These data reveal that dopaminergic neurons in the human SN are modulated by memory signals and demonstrate a progression of information flow in the hippocampal-basal ganglia-frontal cortex loop for memory encoding.

Keywords: DBS; ECoG; Parkinson’s; basal ganglia; dopamine; human single unit; memory; spike-field coherence; substantia nigra; theta.

Publication types

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

MeSH terms

  • Cerebral Cortex / physiopathology*
  • Dopaminergic Neurons / pathology*
  • Electrodes
  • Essential Tremor / physiopathology*
  • Essential Tremor / psychology
  • Humans
  • Memory / physiology*
  • Parkinson Disease / physiopathology*
  • Parkinson Disease / psychology
  • Photic Stimulation
  • Reaction Time*
  • Substantia Nigra / pathology*
  • Task Performance and Analysis