Dataset Information

Aversion or Salience Signaling by Ventral Tegmental Area Glutamate Neurons.

ABSTRACT: Ventral tegmental area (VTA) neurons play roles in reward and aversion. The VTA has, in addition to dopamine neurons, glutamatergic neurons expressing VGluT2. Here, by determining the firing patterns of VTA-VGluT2 neurons expressing channelrhodopsin 2, we identified a major subpopulation of VTA-VGluT2 neurons whose firing rates decreased or were unchanged during sucrose consumption and increased during facial airpuff presentation. We identified a small subpopulation of VTA-VGluT2 neurons whose firing rates increased in response to both rewarding and aversive stimuli. We also found that the changes in firing rate of some VTA-VGluT2 neurons were greater following reward delivery compared with reward omission, whereas others did not differ. We conclude that VTA-VGluT2 neurons are responsive to aversive stimuli, but subpopulations of VTA-VGluT2 neurons are differentially affected by sucrose reward. Reward-responsive subpopulations of VTA-VGluT2 neurons are also divided into those affected by reward expectation alone or the real-time delivery of reward.

SUBMITTER: Root DH

PROVIDER: S-EPMC5993057 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Aversion or Salience Signaling by Ventral Tegmental Area Glutamate Neurons.

Root David H DH Estrin David J DJ Morales Marisela M

iScience 20180401

Ventral tegmental area (VTA) neurons play roles in reward and aversion. The VTA has, in addition to dopamine neurons, glutamatergic neurons expressing VGluT2. Here, by determining the firing patterns of VTA-VGluT2 neurons expressing channelrhodopsin 2, we identified a major subpopulation of VTA-VGluT2 neurons whose firing rates decreased or were unchanged during sucrose consumption and increased during facial airpuff presentation. We identified a small subpopulation of VTA-VGluT2 neurons whose f ...[more]

PMID: 29888759

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Project description:A unique population of ventral tegmental area (VTA) neurons co-transmits glutamate and GABA as well as functionally signals rewarding and aversive outcomes. However, the circuit inputs to VTA VGluT2+VGaT+ neurons are unknown, limiting our understanding of the functional capabilities of these neurons. To identify the inputs to VTA VGluT2+VGaT+ neurons, we coupled monosynaptic rabies tracing with intersectional genetic targeting of VTA VGluT2+VGaT+ neurons in mice. We found that VTA VGluT2+VGaT+ neurons received diverse brain-wide inputs. The largest numbers of monosynaptic inputs to VTA VGluT2+VGaT+ neurons were from superior colliculus, lateral hypothalamus, midbrain reticular nucleus, and periaqueductal gray, whereas the densest inputs relative to brain region volume were from dorsal raphe nucleus, lateral habenula, and ventral tegmental area. Based on these and prior data, we hypothesized that lateral hypothalamus and superior colliculus inputs were glutamatergic neurons. Optical activation of glutamatergic lateral hypothalamus neurons robustly activated VTA VGluT2+VGaT+ neurons regardless of stimulation frequency and resulted in flee-like ambulatory behavior. In contrast, optical activation of glutamatergic superior colliculus neurons activated VTA VGluT2+VGaT+ neurons for a brief period of time at high stimulation frequency and resulted in head rotation and arrested ambulatory behavior (freezing). For both pathways, behaviors induced by stimulation were uncorrelated with VTA VGluT2+VGaT+ neuron activity. However, stimulation of glutamatergic lateral hypothalamus neurons, but not glutamatergic superior colliculus neurons, was associated with VTA VGluT2+VGaT+ footshock-induced activity. We interpret these results such that inputs to VTA VGluT2+VGaT+ neurons may integrate diverse signals related to the detection and processing of motivationally-salient outcomes. Further, VTA VGluT2+VGaT+ neurons may signal threat-related outcomes, possibly via input from lateral hypothalamus glutamate neurons, but not threat-induced behavioral kinematics.

Dataset Information

Aversion or Salience Signaling by Ventral Tegmental Area Glutamate Neurons.

Publications

Aversion or Salience Signaling by Ventral Tegmental Area Glutamate Neurons.

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