Journal Article

Dopamine neuron activity before action initiation gates and invigorates future movements

Tecuapetla, Fatuel, Paixão, Vitor, da Silva, Joaquim Alves, Costa, Rui M.

2018

Overview

The activity of dopamine neurons in the substantia nigra pars compacta before movement initiation affects the probability and vigour of future movements. How dopamine neurons forge future movements Loss of dopamine neurons in a specific area of the brain, the substantia nigra pars compacta (SNc), causes failure to initiate and slowness of movement in patients with Parkinson's disease. Rui Costa and colleagues explore the role of these neurons in movement and reward. In mice, SNc dopamine neurons are transiently active before a self-initiated movement. The neurons affect movement initiation, but they are not selective for specific actions. Manipulation of dopamine neuron activity alters the probability of future movement initiation and the speed of movement, but does not affect ongoing movements. These findings suggest that dopamine signals serve as a general signal for gating and invigorating self-paced movements. Deciding when and whether to move is critical for survival. Loss of dopamine neurons (DANs) of the substantia nigra pars compacta (SNc) in patients with Parkinson’s disease causes deficits in movement initiation and slowness of movement 1 . The role of DANs in self-paced movement has mostly been attributed to their tonic activity, whereas phasic changes in DAN activity have been linked to reward prediction 2 , 3 . This model has recently been challenged by studies showing transient changes in DAN activity before or during self-paced movement initiation 4 , 5 , 6 , 7 . Nevertheless, the necessity of this activity for spontaneous movement initiation has not been demonstrated, nor has its relation to initiation versus ongoing movement been described. Here we show that a large proportion of SNc DANs, which did not overlap with reward-responsive DANs, transiently increased their activity before self-paced movement initiation in mice. This activity was not action-specific, and was related to the vigour of future movements. Inhibition of DANs when mice were immobile reduced the probability and vigour of future movements. Conversely, brief activation of DANs when mice were immobile increased the probability and vigour of future movements. Manipulations of dopamine activity after movement initiation did not affect ongoing movements. Similar findings were observed for the initiation and execution of learned action sequences. These findings causally implicate DAN activity before movement initiation in the probability and vigour of future movements.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 13 / 14 / 14/63 / 42 / 42/41 / 42/44 / 59 / 59/5 / 631/378 / 631/378/2632/1323 / Animals / Dopamine / Dopamine - metabolism / Dopaminergic Neurons - metabolism / Gene expression / Humanities and Social Sciences / letter / Male / Mice / Movement - physiology / Movement disorders / multidisciplinary / Neural circuitry / Neurodegenerative diseases / Neurons / Parkinson Disease - metabolism / Parkinson Disease - pathology / Parkinson Disease - physiopathology / Parkinson's disease / Physiological aspects / Probability / Psychomotor Performance / Reward / Science / Studies / Substantia nigra / Substantia Nigra - cytology / Substantia Nigra - physiology