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Article ; Online: Restoring the youthful state of striatal plasticity in aged mice re-enables cognitive control of action.

Bertran-Gonzalez, Jesus / Dinale, Caroline / Matamales, Miriam

2023 Volume 33, Issue 10, Page(s) 1997–2007.e5

Abstract: Multidisciplinary evidence suggests that the control of voluntary action arbitrates between two major forms of behavioral processing: cognitively guided (or goal directed) and autonomously guided (or habitual). Brain-state irregularities affecting the ... ...

Abstract	Multidisciplinary evidence suggests that the control of voluntary action arbitrates between two major forms of behavioral processing: cognitively guided (or goal directed) and autonomously guided (or habitual). Brain-state irregularities affecting the striatum-such as aging-commonly shift control toward the latter, although the responsible neural mechanisms remain unknown. Combining instrumental conditioning with cell-specific mapping and chemogenetics in striatal neurons, we explored strategies that invigorate goal-directed capacity in aged mice. We found that, under conditions favoring goal-directed control, aged animals resiliently expressed autonomously guided behavior, a response that was underpinned by a characteristic one-to-one functional engagement of the two main neuronal populations in the striatum-D1- and D2-dopamine receptor-expressing spiny projection neurons (SPNs). Chemogenetically induced desensitization of D2-SPN signaling in aged transgenic mice recapitulated the striatal plasticity state observed in young mice, an effect that shifted behavior toward vigorous, goal-directed action. Our findings contribute to the understanding of the neural bases of behavioral control and propose neural system interventions that enhance cognitive functioning in habit-prone brains.
MeSH term(s)	Mice ; Animals ; Corpus Striatum/physiology ; Neurons/physiology ; Mice, Transgenic ; Conditioning, Operant/physiology ; Cognition
Language	English
Publishing date	2023-05-03
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2023.04.020
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Article ; Online: Adaptation of sequential action benefits from timing variability related to lateral basal ganglia circuitry.

Ferguson, Lachlan A / Matamales, Miriam / Nolan, Christopher / Balleine, Bernard W / Bertran-Gonzalez, Jesus

iScience

2024 Volume 27, Issue 3, Page(s) 109274

Abstract: Streamlined action sequences must remain flexible should stable contingencies in the environment change. By combining analyses of behavioral structure with a circuit-specific manipulation in mice, we report on a relationship between action timing ... ...

Abstract	Streamlined action sequences must remain flexible should stable contingencies in the environment change. By combining analyses of behavioral structure with a circuit-specific manipulation in mice, we report on a relationship between action timing variability and successful adaptation that relates to post-synaptic targets of primary motor cortical (M1) projections to dorsolateral striatum (DLS). In a two-lever instrumental task, mice formed successful action sequences by, first, establishing action scaffolds and, second, smoothly extending action duration to adapt to increased task requirements. Interruption of DLS neurons in M1 projection territories altered this process, evoking higher-rate actions that were more stereotyped in their timing, reducing opportunities for success. Based on evidence from neuronal tracing experiments, we propose that DLS neurons in M1 projection territories supply action timing variability to facilitate adaptation, a function that may involve additional downstream subcortical processing relating to collateralization of descending motor pathways to multiple basal ganglia centers.
Language	English
Publishing date	2024-02-20
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2024.109274
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Article ; Online: The Thalamostriatal Pathway and the Hierarchical Control of Action.

Bradfield, Laura A / Matamales, Miriam / Bertran-Gonzalez, Jesus

Neuron

2018 Volume 100, Issue 3, Page(s) 521–523

Abstract: Sequential ordering of motor commands is required for the simplest of our daily activities. In this issue of Neuron, Díaz-Hernández et al. (2018) show that distinct thalamic inputs to different regions of the dorsal striatum critically modulate the ... ...

Abstract	Sequential ordering of motor commands is required for the simplest of our daily activities. In this issue of Neuron, Díaz-Hernández et al. (2018) show that distinct thalamic inputs to different regions of the dorsal striatum critically modulate the initiation and execution of action sequences.
MeSH term(s)	Corpus Striatum ; Neurons ; Thalamus
Language	English
Publishing date	2018-11-08
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Comment
ZDB-ID	808167-0
ISSN	1097-4199 ; 0896-6273
ISSN (online)	1097-4199
ISSN	0896-6273
DOI	10.1016/j.neuron.2018.10.041
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Zs.A 2496: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Amygdala-Cortical Control of Striatal Plasticity Drives the Acquisition of Goal-Directed Action.

Fisher, Simon D / Ferguson, Lachlan A / Bertran-Gonzalez, Jesus / Balleine, Bernard W

Current biology : CB

2020 Volume 30, Issue 22, Page(s) 4541–4546.e5

Abstract: In mammalian species, the capacity for goal-directed action relies on a process of cognitive-emotional integration, which melds the causal and incentive learning processes that link action-goal associations with the current value of the goal [1]. Recent ... ...

Abstract	In mammalian species, the capacity for goal-directed action relies on a process of cognitive-emotional integration, which melds the causal and incentive learning processes that link action-goal associations with the current value of the goal [1]. Recent evidence suggests that such integration depends on a cortical-limbic-striatal circuit centered on the posterior dorsomedial striatum (pDMS) [2]. Learning-related plasticity has been described at both classes of principal neuron in the pDMS, the direct (dSPNs) and indirect (iSPNs) pathway spiny projection neurons [3-5], and is thought to depend on inputs from prelimbic cortex (PL) [6] and the basolateral amygdala (BLA) [7]. Nevertheless, the relative contribution of these structures to the cellular changes associated with goal-directed learning has not been assessed, nor is it known whether any plasticity specific to the PL and BLA inputs to the pDMS is localized to dSPNs, iSPNs, or both cell types. Here, by combining instrumental conditioning with circuit-specific manipulations and ex vivo optogenetics in mice, we discovered that the PL and not the BLA input to pDMS is pivotal for goal-directed learning and that plasticity in the PL-pDMS pathway was bilateral and specific to dSPNs in the pDMS. Subsequent experiments revealed the BLA is critically but indirectly involved in striatal plasticity via its input to the PL; inactivation of the BLA projection to PL blocked goal-directed learning and prevented learning-related plasticity at dSPNs in pDMS.
MeSH term(s)	Animals ; Basolateral Nuclear Complex/cytology ; Basolateral Nuclear Complex/physiology ; Conditioning, Operant ; Corpus Striatum/cytology ; Corpus Striatum/physiology ; Female ; Goals ; Learning/physiology ; Male ; Mice ; Models, Animal ; Neural Pathways/physiology ; Neuronal Plasticity/physiology ; Neurons/physiology ; Optogenetics ; Prefrontal Cortex/cytology ; Prefrontal Cortex/physiology
Language	English
Publishing date	2020-10-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2020.08.090
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Article ; Online: Single Dose of Amphetamine Induces Delayed Subregional Attenuation of Cholinergic Interneuron Activity in the Striatum.

Ztaou, Samira / Oh, Soo Jung / Tepler, Sophia / Fleury, Sixtine / Matamales, Miriam / Bertran-Gonzalez, Jesus / Chuhma, Nao / Rayport, Stephen

eNeuro

2021 Volume 8, Issue 5

Abstract: Psychostimulants such as amphetamine (AMPH) target dopamine (DA) neuron synapses to engender drug-induced plasticity. While DA neurons modulate the activity of striatal (Str) cholinergic interneurons (ChIs) with regional heterogeneity, how AMPH affects ... ...

Abstract	Psychostimulants such as amphetamine (AMPH) target dopamine (DA) neuron synapses to engender drug-induced plasticity. While DA neurons modulate the activity of striatal (Str) cholinergic interneurons (ChIs) with regional heterogeneity, how AMPH affects ChI activity has not been elucidated. Here, we applied quantitative fluorescence imaging approaches to map the dose-dependent effects of a single dose of AMPH on ChI activity at 2.5 and 24 h after injection across the mouse Str using the activity-dependent marker phosphorylated ribosomal protein S6 (p-rpS6
MeSH term(s)	Amphetamine/pharmacology ; Animals ; Cholinergic Agents ; Dopamine ; Interneurons ; Mice ; Nucleus Accumbens
Chemical Substances	Cholinergic Agents ; Amphetamine (CK833KGX7E) ; Dopamine (VTD58H1Z2X)
Language	English
Publishing date	2021-09-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2800598-3
ISSN	2373-2822 ; 2373-2822
ISSN (online)	2373-2822
ISSN	2373-2822
DOI	10.1523/ENEURO.0196-21.2021
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Article ; Online: The DDHD2-STXBP1 interaction mediates long-term memory via generation of saturated free fatty acids.

The EMBO journal

2024 Volume 43, Issue 4, Page(s) 533–567

Abstract: The phospholipid and free fatty acid (FFA) composition of neuronal membranes plays a crucial role in learning and memory, but the mechanisms through which neuronal activity affects the brain's lipid landscape remain largely unexplored. The levels of ... ...

Abstract	The phospholipid and free fatty acid (FFA) composition of neuronal membranes plays a crucial role in learning and memory, but the mechanisms through which neuronal activity affects the brain's lipid landscape remain largely unexplored. The levels of saturated FFAs, particularly of myristic acid (C14:0), strongly increase during neuronal stimulation and memory acquisition, suggesting the involvement of phospholipase A1 (PLA1) activity in synaptic plasticity. Here, we show that genetic ablation of the PLA1 isoform DDHD2 in mice dramatically reduces saturated FFA responses to memory acquisition across the brain. Furthermore, DDHD2 loss also decreases memory performance in reward-based learning and spatial memory models prior to the development of neuromuscular deficits that mirror human spastic paraplegia. Via pulldown-mass spectrometry analyses, we find that DDHD2 binds to the key synaptic protein STXBP1. Using STXBP1/2 knockout neurosecretory cells and a haploinsufficient STXBP1
MeSH term(s)	Animals ; Mice ; Brain/metabolism ; Fatty Acids, Nonesterified/metabolism ; Memory/physiology ; Memory, Long-Term ; Munc18 Proteins/genetics ; Phospholipases/genetics
Chemical Substances	Fatty Acids, Nonesterified ; Munc18 Proteins ; Phospholipases (EC 3.1.-) ; DDHD2 protein, mouse (EC 3.1.-) ; Stxbp1 protein, mouse
Language	English
Publishing date	2024-02-05
Publishing country	England
Document type	Journal Article
ZDB-ID	586044-1
ISSN	1460-2075 ; 0261-4189
ISSN (online)	1460-2075
ISSN	0261-4189
DOI	10.1038/s44318-024-00030-7
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Zs.A 1808: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Quantitative Imaging of Cholinergic Interneurons Reveals a Distinctive Spatial Organization and a Functional Gradient across the Mouse Striatum.

Matamales, Miriam / Götz, Jürgen / Bertran-Gonzalez, Jesus

PloS one

2016 Volume 11, Issue 6, Page(s) e0157682

Abstract: Information processing in the striatum requires the postsynaptic integration of glutamatergic and dopaminergic signals, which are then relayed to the output nuclei of the basal ganglia to influence behavior. Although cellularly homogeneous in appearance, ...

Abstract	Information processing in the striatum requires the postsynaptic integration of glutamatergic and dopaminergic signals, which are then relayed to the output nuclei of the basal ganglia to influence behavior. Although cellularly homogeneous in appearance, the striatum contains several rare interneuron populations which tightly modulate striatal function. Of these, cholinergic interneurons (CINs) have been recently shown to play a critical role in the control of reward-related learning; however how the striatal cholinergic network is functionally organized at the mesoscopic level and the way this organization influences striatal function remains poorly understood. Here, we systematically mapped and digitally reconstructed the entire ensemble of CINs in the mouse striatum and quantitatively assessed differences in densities, spatial arrangement and neuropil content across striatal functional territories. This approach demonstrated that the rostral portion of the striatum contained a higher concentration of CINs than the caudal striatum and that the cholinergic content in the core of the ventral striatum was significantly lower than in the rest of the regions. Additionally, statistical comparison of spatial point patterns in the striatal cholinergic ensemble revealed that only a minor portion of CINs (17%) aggregated into cluster and that they were predominantly organized in a random fashion. Furthermore, we used a fluorescence reporter to estimate the activity of over two thousand CINs in naïve mice and found that there was a decreasing gradient of CIN overall function along the dorsomedial-to-ventrolateral axis, which appeared to be independent of their propensity to aggregate within the striatum. Altogether this work suggests that the regulation of striatal function by acetylcholine across the striatum is highly heterogeneous, and that signals originating in external afferent systems may be principally determining the function of CINs in the striatum.
MeSH term(s)	Acetylcholine/metabolism ; Animals ; Basal Ganglia/physiology ; Cholinergic Neurons/physiology ; Corpus Striatum/diagnostic imaging ; Corpus Striatum/physiology ; Dopamine/metabolism ; Interneurons/physiology ; Learning/physiology ; Mice ; Reward
Chemical Substances	Acetylcholine (N9YNS0M02X) ; Dopamine (VTD58H1Z2X)
Language	English
Publishing date	2016-06-17
Publishing country	United States
Document type	Journal Article
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0157682
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Article ; Online: Basolateral Amygdala Drives a GPCR-Mediated Striatal Memory Necessary for Predictive Learning to Influence Choice.

Morse, Ashleigh K / Leung, Beatrice K / Heath, Emily / Bertran-Gonzalez, Jesus / Pepin, Elise / Chieng, Billy C / Balleine, Bernard W / Laurent, Vincent

Neuron

2020 Volume 106, Issue 5, Page(s) 855–869.e8

Abstract: Predictive learning exerts a powerful influence over choice between instrumental actions. Nevertheless, how this learning is encoded in a sufficiently stable manner to influence choices that can occur much later in time is unclear. Here, we report that ... ...

Abstract	Predictive learning exerts a powerful influence over choice between instrumental actions. Nevertheless, how this learning is encoded in a sufficiently stable manner to influence choices that can occur much later in time is unclear. Here, we report that the basolateral amygdala (BLA) encodes predictive learning and establishes the memory necessary for future choices by driving the accumulation of delta-opioid receptors (DOPRs) on the somatic membrane of cholinergic interneurons in the nucleus accumbens shell (NAc-S). We found that the BLA controls DOPR accumulation via its influence on substance P release in the NAc-S, and that although DOPR accumulation is not necessary for predictive learning per se, it is necessary for the influence of this learning on later choice between actions. This study uncovers, therefore, a novel GPCR-based form of memory that is established by predictive learning and is necessary for such learning to guide the selection and execution of specific actions.
MeSH term(s)	Animals ; Basolateral Nuclear Complex/physiology ; Choice Behavior/physiology ; Cholinergic Neurons/metabolism ; Conditioning, Classical/physiology ; Conditioning, Operant/physiology ; Interneurons/metabolism ; Learning/physiology ; Memory/physiology ; Mice ; Nucleus Accumbens/metabolism ; Receptors, G-Protein-Coupled/metabolism ; Receptors, Opioid, delta/metabolism ; Substance P/metabolism ; Ventral Striatum
Chemical Substances	Receptors, G-Protein-Coupled ; Receptors, Opioid, delta ; Substance P (33507-63-0)
Language	English
Publishing date	2020-04-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	808167-0
ISSN	1097-4199 ; 0896-6273
ISSN (online)	1097-4199
ISSN	0896-6273
DOI	10.1016/j.neuron.2020.03.007
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Zs.A 2496: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Local D2- to D1-neuron transmodulation updates goal-directed learning in the striatum.

Matamales, Miriam / McGovern, Alice E / Mi, Jia Dai / Mazzone, Stuart B / Balleine, Bernard W / Bertran-Gonzalez, Jesus

Science (New York, N.Y.)

2020 Volume 367, Issue 6477, Page(s) 549–555

Abstract: Extinction learning allows animals to withhold voluntary actions that are no longer related to reward and so provides a major source of behavioral control. Although such learning is thought to depend on dopamine signals in the striatum, the way the ... ...

Abstract	Extinction learning allows animals to withhold voluntary actions that are no longer related to reward and so provides a major source of behavioral control. Although such learning is thought to depend on dopamine signals in the striatum, the way the circuits that mediate goal-directed control are reorganized during new learning remains unknown. Here, by mapping a dopamine-dependent transcriptional activation marker in large ensembles of spiny projection neurons (SPNs) expressing dopamine receptor type 1 (D1-SPNs) or 2 (D2-SPNs) in mice, we demonstrate an extensive and dynamic D2- to D1-SPN transmodulation across the striatum that is necessary for updating previous goal-directed learning. Our findings suggest that D2-SPNs suppress the influence of outdated D1-SPN plasticity within functionally relevant striatal territories to reshape volitional action.
MeSH term(s)	Animals ; Corpus Striatum/drug effects ; Corpus Striatum/physiology ; Dopamine Antagonists/pharmacology ; Dopaminergic Neurons/drug effects ; Dopaminergic Neurons/physiology ; Female ; Goals ; Learning/physiology ; Male ; Mice ; Mice, Inbred C57BL ; Nucleosomes/metabolism ; Raclopride/pharmacology ; Receptors, Dopamine D1/antagonists & inhibitors ; Receptors, Dopamine D1/physiology ; Receptors, Dopamine D2/physiology
Chemical Substances	DRD2 protein, mouse ; Dopamine Antagonists ; Drd1 protein, mouse ; Nucleosomes ; Receptors, Dopamine D1 ; Receptors, Dopamine D2 ; Raclopride (430K3SOZ7G)
Language	English
Publishing date	2020-01-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	128410-1
ISSN	1095-9203 ; 0036-8075
ISSN (online)	1095-9203
ISSN	0036-8075
DOI	10.1126/science.aaz5751
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Zs.A 27: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Disease-associated tau impairs mitophagy by inhibiting Parkin translocation to mitochondria.

Cummins, Nadia / Tweedie, Andrea / Zuryn, Steven / Bertran-Gonzalez, Jesus / Götz, Jürgen

The EMBO journal

2018 Volume 38, Issue 3

Abstract: Accumulation of the protein tau characterises Alzheimer's disease and other tauopathies, including familial forms of frontotemporal dementia (FTD) that carry pathogenic tau mutations. Another hallmark feature of these diseases is the accumulation of ... ...

Abstract	Accumulation of the protein tau characterises Alzheimer's disease and other tauopathies, including familial forms of frontotemporal dementia (FTD) that carry pathogenic tau mutations. Another hallmark feature of these diseases is the accumulation of dysfunctional mitochondria. Although disease-associated tau is known to impair several aspects of mitochondrial function, it is still unclear whether it also directly impinges on mitochondrial quality control, specifically Parkin-dependent mitophagy. Using the mito-QC mitophagy reporter, we found that both human wild-type (hTau) and FTD mutant tau (hP301L) inhibited mitophagy in neuroblastoma cells, by reducing mitochondrial translocation of Parkin. In the
MeSH term(s)	Animals ; Caenorhabditis elegans ; Male ; Membrane Potential, Mitochondrial ; Mice ; Mice, Transgenic ; Mitochondria/genetics ; Mitochondria/metabolism ; Mitochondria/pathology ; Mitophagy ; Neuroblastoma/genetics ; Neuroblastoma/metabolism ; Neuroblastoma/pathology ; Neurons/metabolism ; Neurons/pathology ; Protein Transport ; Tumor Cells, Cultured ; Ubiquitin-Protein Ligases/genetics ; Ubiquitin-Protein Ligases/metabolism ; tau Proteins/genetics ; tau Proteins/metabolism
Chemical Substances	tau Proteins ; Ubiquitin-Protein Ligases (EC 2.3.2.27) ; parkin protein (EC 2.3.2.27)
Language	English
Publishing date	2018-12-11
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	586044-1
ISSN	1460-2075 ; 0261-4189
ISSN (online)	1460-2075
ISSN	0261-4189
DOI	10.15252/embj.201899360
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