Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences

Nat Neurosci. 2014 Mar;17(3):423-30. doi: 10.1038/nn.3632. Epub 2014 Jan 26.

Abstract

Chunking allows the brain to efficiently organize memories and actions. Although basal ganglia circuits have been implicated in action chunking, little is known about how individual elements are concatenated into a behavioral sequence at the neural level. Using a task in which mice learned rapid action sequences, we uncovered neuronal activity encoding entire sequences as single actions in basal ganglia circuits. In addition to neurons with activity related to the start/stop activity signaling sequence parsing, we found neurons displaying inhibited or sustained activity throughout the execution of an entire sequence. This sustained activity covaried with the rate of execution of individual sequence elements, consistent with motor concatenation. Direct and indirect pathways of basal ganglia were concomitantly active during sequence initiation, but behaved differently during sequence performance, revealing a more complex functional organization of these circuits than previously postulated. These results have important implications for understanding the functional organization of basal ganglia during the learning and execution of action sequences.

Publication types

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

MeSH terms

  • Animals
  • Basal Ganglia / cytology
  • Basal Ganglia / physiology*
  • Basal Ganglia / surgery
  • Behavior, Animal / physiology
  • Electrodes, Implanted
  • Female
  • Globus Pallidus / cytology
  • Globus Pallidus / physiology
  • Globus Pallidus / surgery
  • Learning / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nerve Tissue Proteins / genetics
  • Neural Pathways / cytology
  • Neural Pathways / physiology
  • Neurons / cytology
  • Neurons / physiology*
  • Psychomotor Performance / physiology*
  • Receptors, N-Methyl-D-Aspartate / genetics
  • Substantia Nigra / cytology
  • Substantia Nigra / physiology
  • Substantia Nigra / surgery
  • Time Factors

Substances

  • Gprin1 protein, mouse
  • Nerve Tissue Proteins
  • Receptors, N-Methyl-D-Aspartate