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

Jan Kamiński; Adam N Mamelak; Kurtis Birch; Clayton P Mosher; Michele Tagliati; Ueli Rutishauser

doi:10.1016/j.cub.2018.03.024

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.

Authors

Jan Kamiński¹, Adam N Mamelak², Kurtis Birch², Clayton P Mosher², Michele Tagliati³, Ueli Rutishauser⁴

Affiliations

¹ Department of Neurosurgery, Cedars-Sinai Medical Center, 8700 Beverly Boulevard, Los Angeles, CA 90048, USA; Computation and Neural Systems, Division of Biology and Biological Engineering, California Institute of Technology, 1200 E California Boulevard, Pasadena, CA 91125, USA. Electronic address: jan.kaminski@cshs.org.
² Department of Neurosurgery, Cedars-Sinai Medical Center, 8700 Beverly Boulevard, Los Angeles, CA 90048, USA.
³ Department of Neurology, Cedars-Sinai Medical Center, 8700 Beverly Boulevard, Los Angeles, CA 90048, USA.
⁴ Department of Neurosurgery, Cedars-Sinai Medical Center, 8700 Beverly Boulevard, Los Angeles, CA 90048, USA; Department of Neurology, Cedars-Sinai Medical Center, 8700 Beverly Boulevard, Los Angeles, CA 90048, USA; Center for Neural Science and Medicine, Department of Biomedical Sciences, Cedars-Sinai Medical Center, 8700 Beverly Boulevard, Los Angeles, CA 90048, USA; Computation and Neural Systems, Division of Biology and Biological Engineering, California Institute of Technology, 1200 E California Boulevard, Pasadena, CA 91125, USA. Electronic address: ueli.rutishauser@cshs.org.

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

Abstract

Publication types

MeSH terms

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