The Striatum Organizes 3D Behavior via Moment-to-Moment Action Selection

• Published in: Cell 2018-06, Vol.174 (1), p.44-58.e17
• Main Authors: Markowitz, Jeffrey E., Gillis, Winthrop F., Beron, Celia C., Neufeld, Shay Q., Robertson, Keiramarie, Bhagat, Neha D., Peterson, Ralph E., Peterson, Emalee, Hyun, Minsuk, Linderman, Scott W., Sabatini, Bernardo L., Datta, Sandeep Robert
• Format: Article
• Language: English
• Subjects: Animals; basal ganglia; behavior; Behavior, Animal - drug effects; Calcium - metabolism; coding; Corpus Striatum - drug effects; Corpus Striatum - metabolism; direct pathway; Electrodes, Implanted; ethology; Female; indirect pathway; machine learning; Male; Mice; Mice, Inbred C57BL; Mice, Transgenic; mouse; N-Methylaspartate - pharmacology; Neurons - drug effects; Neurons - physiology; Photometry; Receptors, Dopamine D1 - deficiency; Receptors, Dopamine D1 - genetics; striatum
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2018.04.019

Many naturalistic behaviors are built from modular components that are expressed sequentially. Although striatal circuits have been implicated in action selection and implementation, the neural mechanisms that compose behavior in unrestrained animals are not well understood. Here, we record bulk and cellular neural activity in the direct and indirect pathways of dorsolateral striatum (DLS) as mice spontaneously express action sequences. These experiments reveal that DLS neurons systematically encode information about the identity and ordering of sub-second 3D behavioral motifs; this encoding is facilitated by fast-timescale decorrelations between the direct and indirect pathways. Furthermore, lesioning the DLS prevents appropriate sequence assembly during exploratory or odor-evoked behaviors. By characterizing naturalistic behavior at neural timescales, these experiments identify a code for elemental 3D pose dynamics built from complementary pathway dynamics, support a role for DLS in constructing meaningful behavioral sequences, and suggest models for how actions are sculpted over time. [Display omitted] •Dorsolateral striatum systematically represents behavioral syllables and grammar•Complementary direct and indirect pathway activity encodes fast 3D pose dynamics•Dorsolateral striatum flexibly assembles behavioral sequences from sub-second components•MoSeq enables precise alignment of neural activity and naturalistic behaviors The striatum concatenates sub-second 3D behavioral motifs into action sequences during naturalistic behaviors.