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Memory-specific encoding activities of the ventral tegmental area dopamine and GABA neurons.

ABSTRACT: Although the midbrain dopamine (DA) system plays a crucial role in higher cognitive functions, including updating and maintaining short-term memory, the encoding properties of the somatic spiking activity of ventral tegmental area (VTA) DA neurons for short-term memory computations have not yet been identified. Here, we probed and analyzed the activity of optogenetically identified DA and GABA neurons while mice engaged in short-term memory-dependent behavior in a T-maze task. Single-neuron analysis revealed that significant subpopulations of DA and GABA neurons responded differently between left and right trials in the memory delay. With a series of control behavioral tasks and regression analysis tools, we show that firing rate differences are linked to short-term memory-dependent decisions and cannot be explained by reward-related processes, motivated behavior, or motor-related activities. This evidence provides novel insights into the mnemonic encoding activities of midbrain DA and GABA neurons.

SUBMITTER: Glykos V

PROVIDER: S-EPMC10957172 | biostudies-literature | 2024 Mar

REPOSITORIES: biostudies-literature

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Memory-specific encoding activities of the ventral tegmental area dopamine and GABA neurons.

Glykos Vasileios V Fujisawa Shigeyoshi S

eLife 20240321

Although the midbrain dopamine (DA) system plays a crucial role in higher cognitive functions, including updating and maintaining short-term memory, the encoding properties of the somatic spiking activity of ventral tegmental area (VTA) DA neurons for short-term memory computations have not yet been identified. Here, we probed and analyzed the activity of optogenetically identified DA and GABA neurons while mice engaged in short-term memory-dependent behavior in a T-maze task. Single-neuron anal ...[more]

PMID: 38512339

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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

Memory-specific encoding activities of the ventral tegmental area dopamine and GABA neurons.

Publications

Memory-specific encoding activities of the ventral tegmental area dopamine and GABA neurons.

Similar Datasets

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