Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons

Ben Engelhard, Joel Finkelstein, Julia Cox, Weston Fleming, Hee Jae Jang, Sharon Ornelas, Sue Ann Koay, Stephan Y. Thiberge, Nathaniel Douglass Daw, David W. Tank, Ilana Basya Witten

Research output: Contribution to journalLetter

2 Citations (Scopus)

Abstract

There is increased appreciation that dopamine neurons in the midbrain respond not only to reward1 and reward-predicting cues1,2, but also to other variables such as the distance to reward3, movements4–9 and behavioural choices10,11. An important question is how the responses to these diverse variables are organized across the population of dopamine neurons. Whether individual dopamine neurons multiplex several variables, or whether there are subsets of neurons that are specialized in encoding specific behavioural variables remains unclear. This fundamental question has been difficult to resolve because recordings from large populations of individual dopamine neurons have not been performed in a behavioural task with sufficient complexity to examine these diverse variables simultaneously. Here, to address this gap, we used two-photon calcium imaging through an implanted lens to record the activity of more than 300 dopamine neurons from the ventral tegmental area of the mouse midbrain during a complex decision-making task. As mice navigated in a virtual-reality environment, dopamine neurons encoded an array of sensory, motor and cognitive variables. These responses were functionally clustered, such that subpopulations of neurons transmitted information about a subset of behavioural variables, in addition to encoding reward. These functional clusters were spatially organized, with neighbouring neurons more likely to be part of the same cluster. Together with the topography between dopamine neurons and their projections, this specialization and anatomical organization may aid downstream circuits in correctly interpreting the wide range of signals transmitted by dopamine neurons.

Original languageEnglish (US)
Pages (from-to)509-513
Number of pages5
JournalNature
Volume570
Issue number7762
DOIs
StatePublished - Jun 27 2019

Fingerprint

Dopaminergic Neurons
Mesencephalon
Reward
Neurons
Ventral Tegmental Area
Photons
Population
Lenses
Decision Making
Calcium

All Science Journal Classification (ASJC) codes

  • General

Cite this

Engelhard, B., Finkelstein, J., Cox, J., Fleming, W., Jang, H. J., Ornelas, S., ... Witten, I. B. (2019). Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons. Nature, 570(7762), 509-513. https://doi.org/10.1038/s41586-019-1261-9
Engelhard, Ben ; Finkelstein, Joel ; Cox, Julia ; Fleming, Weston ; Jang, Hee Jae ; Ornelas, Sharon ; Koay, Sue Ann ; Thiberge, Stephan Y. ; Daw, Nathaniel Douglass ; Tank, David W. ; Witten, Ilana Basya. / Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons. In: Nature. 2019 ; Vol. 570, No. 7762. pp. 509-513.
@article{e13f05ccbb70492baff8e9e8e9c4ada8,
title = "Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons",
abstract = "There is increased appreciation that dopamine neurons in the midbrain respond not only to reward1 and reward-predicting cues1,2, but also to other variables such as the distance to reward3, movements4–9 and behavioural choices10,11. An important question is how the responses to these diverse variables are organized across the population of dopamine neurons. Whether individual dopamine neurons multiplex several variables, or whether there are subsets of neurons that are specialized in encoding specific behavioural variables remains unclear. This fundamental question has been difficult to resolve because recordings from large populations of individual dopamine neurons have not been performed in a behavioural task with sufficient complexity to examine these diverse variables simultaneously. Here, to address this gap, we used two-photon calcium imaging through an implanted lens to record the activity of more than 300 dopamine neurons from the ventral tegmental area of the mouse midbrain during a complex decision-making task. As mice navigated in a virtual-reality environment, dopamine neurons encoded an array of sensory, motor and cognitive variables. These responses were functionally clustered, such that subpopulations of neurons transmitted information about a subset of behavioural variables, in addition to encoding reward. These functional clusters were spatially organized, with neighbouring neurons more likely to be part of the same cluster. Together with the topography between dopamine neurons and their projections, this specialization and anatomical organization may aid downstream circuits in correctly interpreting the wide range of signals transmitted by dopamine neurons.",
author = "Ben Engelhard and Joel Finkelstein and Julia Cox and Weston Fleming and Jang, {Hee Jae} and Sharon Ornelas and Koay, {Sue Ann} and Thiberge, {Stephan Y.} and Daw, {Nathaniel Douglass} and Tank, {David W.} and Witten, {Ilana Basya}",
year = "2019",
month = "6",
day = "27",
doi = "10.1038/s41586-019-1261-9",
language = "English (US)",
volume = "570",
pages = "509--513",
journal = "Nature",
issn = "0028-0836",
publisher = "Nature Publishing Group",
number = "7762",

}

Engelhard, B, Finkelstein, J, Cox, J, Fleming, W, Jang, HJ, Ornelas, S, Koay, SA, Thiberge, SY, Daw, ND, Tank, DW & Witten, IB 2019, 'Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons', Nature, vol. 570, no. 7762, pp. 509-513. https://doi.org/10.1038/s41586-019-1261-9

Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons. / Engelhard, Ben; Finkelstein, Joel; Cox, Julia; Fleming, Weston; Jang, Hee Jae; Ornelas, Sharon; Koay, Sue Ann; Thiberge, Stephan Y.; Daw, Nathaniel Douglass; Tank, David W.; Witten, Ilana Basya.

In: Nature, Vol. 570, No. 7762, 27.06.2019, p. 509-513.

Research output: Contribution to journalLetter

TY - JOUR

T1 - Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons

AU - Engelhard, Ben

AU - Finkelstein, Joel

AU - Cox, Julia

AU - Fleming, Weston

AU - Jang, Hee Jae

AU - Ornelas, Sharon

AU - Koay, Sue Ann

AU - Thiberge, Stephan Y.

AU - Daw, Nathaniel Douglass

AU - Tank, David W.

AU - Witten, Ilana Basya

PY - 2019/6/27

Y1 - 2019/6/27

N2 - There is increased appreciation that dopamine neurons in the midbrain respond not only to reward1 and reward-predicting cues1,2, but also to other variables such as the distance to reward3, movements4–9 and behavioural choices10,11. An important question is how the responses to these diverse variables are organized across the population of dopamine neurons. Whether individual dopamine neurons multiplex several variables, or whether there are subsets of neurons that are specialized in encoding specific behavioural variables remains unclear. This fundamental question has been difficult to resolve because recordings from large populations of individual dopamine neurons have not been performed in a behavioural task with sufficient complexity to examine these diverse variables simultaneously. Here, to address this gap, we used two-photon calcium imaging through an implanted lens to record the activity of more than 300 dopamine neurons from the ventral tegmental area of the mouse midbrain during a complex decision-making task. As mice navigated in a virtual-reality environment, dopamine neurons encoded an array of sensory, motor and cognitive variables. These responses were functionally clustered, such that subpopulations of neurons transmitted information about a subset of behavioural variables, in addition to encoding reward. These functional clusters were spatially organized, with neighbouring neurons more likely to be part of the same cluster. Together with the topography between dopamine neurons and their projections, this specialization and anatomical organization may aid downstream circuits in correctly interpreting the wide range of signals transmitted by dopamine neurons.

AB - There is increased appreciation that dopamine neurons in the midbrain respond not only to reward1 and reward-predicting cues1,2, but also to other variables such as the distance to reward3, movements4–9 and behavioural choices10,11. An important question is how the responses to these diverse variables are organized across the population of dopamine neurons. Whether individual dopamine neurons multiplex several variables, or whether there are subsets of neurons that are specialized in encoding specific behavioural variables remains unclear. This fundamental question has been difficult to resolve because recordings from large populations of individual dopamine neurons have not been performed in a behavioural task with sufficient complexity to examine these diverse variables simultaneously. Here, to address this gap, we used two-photon calcium imaging through an implanted lens to record the activity of more than 300 dopamine neurons from the ventral tegmental area of the mouse midbrain during a complex decision-making task. As mice navigated in a virtual-reality environment, dopamine neurons encoded an array of sensory, motor and cognitive variables. These responses were functionally clustered, such that subpopulations of neurons transmitted information about a subset of behavioural variables, in addition to encoding reward. These functional clusters were spatially organized, with neighbouring neurons more likely to be part of the same cluster. Together with the topography between dopamine neurons and their projections, this specialization and anatomical organization may aid downstream circuits in correctly interpreting the wide range of signals transmitted by dopamine neurons.

UR - http://www.scopus.com/inward/record.url?scp=85066777754&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85066777754&partnerID=8YFLogxK

U2 - 10.1038/s41586-019-1261-9

DO - 10.1038/s41586-019-1261-9

M3 - Letter

VL - 570

SP - 509

EP - 513

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7762

ER -

Engelhard B, Finkelstein J, Cox J, Fleming W, Jang HJ, Ornelas S et al. Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons. Nature. 2019 Jun 27;570(7762):509-513. https://doi.org/10.1038/s41586-019-1261-9