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• W2914291213 abstract "The basal ganglia integrate motivation and action across their circuits; neurons in anatomical modules called striosomes could contribute strongly to this merger. A new method focusing on network interconnections will allow a better understanding of the functional role of striosomes. The basal ganglia integrate motivation and action across their circuits; neurons in anatomical modules called striosomes could contribute strongly to this merger. A new method focusing on network interconnections will allow a better understanding of the functional role of striosomes. Motivation plays an important role in our daily actions. For example in sports, let’s say you’re about to serve for a key point in a tennis match: you really want to get that first serve in. Motivation and action circuits in the brain will need to quickly interact. On a longer timescale, say you must decide if you’re going to exercise your right on election day — you are, and you will make sure to give your support to your best candidate. Both these examples show that motivation plays a major role in shaping behavioral actions: every day we make motivated decisions that begin with cognition and end with action. The brain’s basal ganglia are an important nexus for this motivation/action interface. The input structure of the basal ganglia, the striatum, contains neurons that receive information about both motivation and action, located in a compartment called striosomes. Distributed sinuously across the striatum like spaces in swiss cheese, this compartment shows a distinct scattered anatomical pattern (Figure 1B). While striosomes have been well characterized anatomically in many species, data concerning their electrophysiology and functionality have been elusive. In the non-human primate, where much knowledge of the cognition/action interface has been explored at the neuronal level, the scattering of striosomes and their depth in the brain present a localization challenge (see Figure 1B). A new study by Hong et al. [1Hong S. Amemori S. Chung E. Gibson D.J. Amemori K.I. Graybiel A.M. Predominant striatal input to the lateral habenula in macaques comes from striosomes.Curr. Biol. 2019; 29: 51-61Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar], reported recently in Current Biology, delivers important new insight into how neural activity from striosomes can be localized, permitting us to address their functionality. The authors devised a novel way to determine neuronal activity corresponding to striosomal sites in the awake behaving monkey, by using an approach based on neural interconnection patterns. This study opens further avenues for research on striatal compartments to help better understand their role in mood and action. On a larger scale, for optimized performance, motivated actions require contributions from multiple interacting cortical brain areas, complemented by critical subcortical loops [2Cisek P. Kalaska J.F. Neural mechanisms for interacting with a world full of action choices.Annu. Rev. Neurosci. 2010; 33: 269-298Crossref PubMed Scopus (906) Google Scholar]. These interconnected loops bring together important calculations from the cerebellum and basal ganglia in decision, planning, and execution of actions [3Bostan A.C. Strick P.L. The basal ganglia and the cerebellum: nodes in an integrated network.Nat. Rev. Neurosci. 2018; 19: 338-350Crossref PubMed Scopus (317) Google Scholar]. In their overall network, the basal ganglia bring together the motivational and purpose-driven aspects of successful action plans, as well as playing a critical role in the formation of habits [4Smith K.S. Graybiel A.M. Habit formation. Dialogues Clin.Neuro. 2016; 18: 33-43Google Scholar]. The striatum and its compartments, the striosomes and the matrix (Figure 1C) are well-established subdivisions, largely due to detailed anatomical work from the same laboratory [5Flaherty A.W. Graybiel A.M. Output architecture of the primate putamen.J. Neurosci. 1993; 13: 3222-3237Crossref PubMed Google Scholar, 6Graybiel A.M. Templates for neural dynamics in the striatum: striosomes and matrisomes.in: Shepherd G.M. Grillner S. Handbook of Brain Microcircuits. Oxford University Press, New York, NY2010: 120-126Crossref Google Scholar, 7Graybiel A.M. Ragsdale Jr., C.W. Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining.Proc. Natl. Acad. Sci. USA. 1978; 75: 5723-5726Crossref PubMed Scopus (686) Google Scholar], with neurons being part of striosomes or part of the matrix (which is sometimes further parcellated into matrisomes) [6Graybiel A.M. Templates for neural dynamics in the striatum: striosomes and matrisomes.in: Shepherd G.M. Grillner S. Handbook of Brain Microcircuits. Oxford University Press, New York, NY2010: 120-126Crossref Google Scholar]. The striosomes in particular were first identified by their neurochemical properties [7Graybiel A.M. Ragsdale Jr., C.W. Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining.Proc. Natl. Acad. Sci. USA. 1978; 75: 5723-5726Crossref PubMed Scopus (686) Google Scholar], being linked with motivational aspects via dopamine neurotransmission [8Yoshizawa T. Ito M. Doya K. Reward-predictive neural activities in striatal striosome compartments.eNeuro. 2018; 5 (5. pii: ENEURO.0367-17.2018)https://doi.org/10.1523/ENEURO.0367-17.2018Crossref PubMed Scopus (29) Google Scholar, 9Friedman A. Homma D. Gibb L.G. Amemori K.I. Rubin S.J. Hood A.S. Riad M.H. Graybiel A.M. A Corticostriatal path targeting striosomes controls decision-making under conflict.Cell. 2015; 161: 1320-1333Abstract Full Text Full Text PDF PubMed Scopus (182) Google Scholar]; a schematic rendering of striosomes is shown in Figure 1A,B. Neurons in the matrix compartment of the striatum combine information from many cortical regions to optimize actions [6Graybiel A.M. Templates for neural dynamics in the striatum: striosomes and matrisomes.in: Shepherd G.M. Grillner S. Handbook of Brain Microcircuits. Oxford University Press, New York, NY2010: 120-126Crossref Google Scholar]. But due to technical difficulties in determining which neurons are part of striosomes during behavioral electrophysiology [9Friedman A. Homma D. Gibb L.G. Amemori K.I. Rubin S.J. Hood A.S. Riad M.H. Graybiel A.M. A Corticostriatal path targeting striosomes controls decision-making under conflict.Cell. 2015; 161: 1320-1333Abstract Full Text Full Text PDF PubMed Scopus (182) Google Scholar], much remains to be uncovered concerning the function of striosomes. More knowledge on the operation of these circuits would provide important insight on how the brain programs motivated actions. To determine which parts of the striatum consist of striosomes, Hong et al. [1Hong S. Amemori S. Chung E. Gibson D.J. Amemori K.I. Graybiel A.M. Predominant striatal input to the lateral habenula in macaques comes from striosomes.Curr. Biol. 2019; 29: 51-61Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar] recorded neuronal activity in the lateral habenula, connected downstream of the striatum via a two-synapse interconnection (see the pathway representation in Figure 1C, identifying the striato-pallidal and pallido-habenular links), while using repeated stimulations to map the striatum. The striatal stimulations activate the pallido-habenular circuit, inhibiting globus pallidus neurons, which in contrast send excitatory projections to the lateral habenula [10Stephenson-Jones M. Yu K. Ahrens S. Tucciarone J.M. van Huijstee A.N. Mejia L.A. Penzo M.A. Tai L.H. Wilbrecht L. Li B. A basal ganglia circuit for evaluating action outcomes.Nature. 2016; 539: 289-293Crossref PubMed Scopus (110) Google Scholar]. By stimulating this pathway, Hong et al. [1Hong S. Amemori S. Chung E. Gibson D.J. Amemori K.I. Graybiel A.M. Predominant striatal input to the lateral habenula in macaques comes from striosomes.Curr. Biol. 2019; 29: 51-61Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar] affected the balance in this disynaptic connection. Located near and having evolved alongside the pineal gland, the lateral habenula serves as an important juncture between the basal ganglia and limbic system, and it responds to negative events to aid in emotive decisions and movement in potentially threatening situations [11Namboodiri V.M.K. Rodriguez-Ronnaguera J. Stuber G.D. The habenula.Curr. Biol. 2016; 26: R873-R877Abstract Full Text Full Text PDF PubMed Scopus (69) Google Scholar, 12Hikosaka O. The habenula: from stress evasion to value-based decision-making.Nat. Rev. Neurosci. 2010; 11: 503-513Crossref PubMed Scopus (644) Google Scholar]. It signals negative possible outcomes to other brainstem neuromodulatory areas, including the ventral tegmental area, substantia nigra pars compacta, dorsal/medial raphe nuclei, and laterodorsal tegmentum, by acting upon dopamine, serotonin, and norepinephrine receptors [12Hikosaka O. The habenula: from stress evasion to value-based decision-making.Nat. Rev. Neurosci. 2010; 11: 503-513Crossref PubMed Scopus (644) Google Scholar]. The lateral habenula plays an important role in decision-making by labelling experiences as either aversive or rewarding in comparison to expectations. Over-activation of the habenula can lead to a negative bias, and to beliefs that outcomes are worse than they really are. In a potentially threatening situation, the habenula will increase its inhibitory activity on dopamine neurons in the ventral tegmental area and the substantia nigra pars compacta. Conversely, a tonic under-activation of the habenula can do the opposite, giving individuals a positive bias and beliefs that outcomes are less negative than in reality, leading to increased risk-taking and disinhibited behaviors [13Epstein E.L. Hurley R.A. Taber K.H. The habenula's role in adaptive behaviors: Contributions from neuroimaging.J. Neuropsych. Clin. N. 2018; 30: 1-4Crossref Scopus (3) Google Scholar]. Dysregulation of the habenula has been associated with depression, sleep disorders, anxiety, and schizophrenia [11Namboodiri V.M.K. Rodriguez-Ronnaguera J. Stuber G.D. The habenula.Curr. Biol. 2016; 26: R873-R877Abstract Full Text Full Text PDF PubMed Scopus (69) Google Scholar]. In their experiments, Hong et al. [1Hong S. Amemori S. Chung E. Gibson D.J. Amemori K.I. Graybiel A.M. Predominant striatal input to the lateral habenula in macaques comes from striosomes.Curr. Biol. 2019; 29: 51-61Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar] used a precise combination of striatal stimulation coupled with lateral habenula recordings, along with detailed histologic identification. This served to determine if the stimulated sites were within striosomes, via the response in the lateral habenula. The first step was to isolate neural activity in the lateral habenula, whose localization was determined via magnetic resonance imaging and targeted electrode penetrations. The experimenters trained monkeys to make eye movements (saccades) to a visual target presented on a computer screen; green targets providing a juice reward, and white targets providing no reward. The monkey would still make saccades to the white targets, as trials without saccades would have to be repeated. Once the profile of the lateral habenula response was known, the stimulation part of the experiment would start. By systematically stimulating the striatum every 200 μm and recording the response in the lateral habenula, particular locations along the track were found to elicit a stronger response. This enabled the authors to localize striosomes, and is schematically represented in Figure 1A. It provided high-probability sites along the track to be considered as part of the striosomal system. The careful and dense mapping constitutes an important component of establishing the method, as the size of striosomes is around 500 μm wide; by advancing in the track too quickly, some striosome sites could be missed. Following this mapping, a detailed quantitative analysis revealed ‘hotspots’ along the track, which represented high-probability sites for putative striosome locations. These were then compared with the anatomical localization of striosomes, using classical micro-anatomical methods. This last comparison completed the elegant work of localization, relating the anatomical compartment with the physiological signals. The final step in the Hong et al. [1Hong S. Amemori S. Chung E. Gibson D.J. Amemori K.I. Graybiel A.M. Predominant striatal input to the lateral habenula in macaques comes from striosomes.Curr. Biol. 2019; 29: 51-61Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar] study involved further characterization of the electrophysiological responses, to better understand the place of striosomes within the local and overall networks of the basal ganglia and limbic system. Following striosome stimulation, multi-unit activity in the lateral habenula would present a rhythm in the beta (12–30 Hz) range. As similar rhythmic phenomena have already been uncovered in basal ganglia circuits (for example [14Hammond C. Bergman H. Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments.Trends Neurosci. 2007; 30: 357-364Abstract Full Text Full Text PDF PubMed Scopus (1118) Google Scholar, 15Brittain J.S. Sharott A. Brown P. The highs and lows of beta activity in cortico-basal ganglia loops.Eur. J. Neurosci. 2014; 39: 1951-1959Crossref PubMed Scopus (87) Google Scholar, 16Courtemanche R. Fujii N. Graybiel A.M. Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys.J. Neurosci. 2003; 23: 11741-11752Crossref PubMed Google Scholar]), this means that the habenula could show reverberating properties in response to basal ganglia output. This rhythmic interaction could represent a temporal mode of communication between the basal ganglia and habenula. Basal ganglia oscillatory activity is amplified under dopamine depletion, enough to pathologically affect the striato-pallidal output (for example [17Lemaire N. Hernandez L.F. Hu D. Kubota Y. Howe M.W. Graybiel A.M. Effects of dopamine depletion on LFP oscillations in striatum are task- and learning-dependent and selectively reversed by L-DOPA.Proc. Natl. Acad. Sci. USA. 2012; 109: 18126-18131Crossref PubMed Scopus (62) Google Scholar]). As its activity sometimes responds with a rhythm to striosome stimulation, the lateral habenula could be recruited when basal ganglia afferents oscillate. It remains to be determined if this is limited to stimulation experiments, or if such recruitment would occur in normal and/or neuropathological networks. Two other interesting findings from the same laboratory can be related to rhythmic network interactions affecting striosomes: first, medial prefrontal cortex (AMFC, Figure 1C) activation to striosome circuits shapes cost/benefit decision-making [9Friedman A. Homma D. Gibb L.G. Amemori K.I. Rubin S.J. Hood A.S. Riad M.H. Graybiel A.M. A Corticostriatal path targeting striosomes controls decision-making under conflict.Cell. 2015; 161: 1320-1333Abstract Full Text Full Text PDF PubMed Scopus (182) Google Scholar], and this cortex also shows strong oscillations in response to rewarded actions [18Amarante L.M. Caetano M.S. Laubach M. Medial frontal theta is entrained to rewarded actions.J. Neurosci. 2017; 37: 10757-10769Crossref PubMed Scopus (24) Google Scholar]; also second, stimulation of small striatal zones — which could correspond to striosomes — can elicit an anxious state in a monkey, a phenomenon related to beta-band oscillations [19Amemori K.I. Amemori S. Gibson D.J. Graybiel A.M. Striatal microstimulation induces persistent and repetitive negative decision-making predicted by striatal beta-band oscillation.Neuron. 2018; 99: 829-841Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar]. These elements provide evidence that oscillatory signals flowing through striosomes could represent a mechanism of influence on the expression of mood and actions. Overall, using a finely-tuned methodology, Hong et al. [1Hong S. Amemori S. Chung E. Gibson D.J. Amemori K.I. Graybiel A.M. Predominant striatal input to the lateral habenula in macaques comes from striosomes.Curr. Biol. 2019; 29: 51-61Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar] complemented their detailed seminal work on striosomes with an innovative electrophysiological approach to tease out the details of striatal modularity and connectivity. This study paves the way for future efforts in striosome population coding and its relation to complex motivated behaviours. By revealing which neurons belong to striatal compartments, this methodology will allow us to determine the sensorimotor, cognitive and motivation-based neural populations involved in behavior, and their computational interactions. Perhaps, further along the way, we will also be able to determine for sure the optimal neural state — and involved networks — to perfectly hit (but not over-hit!) that winning tennis serve, or to be fully engaged in the electoral process." @default.
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• W2914291213 title "Basal Ganglia: Striosomes and the Link between Motivation and Action" @default.
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