An inhibitory corticostriatal pathway

Rock, Crystal; Zurita, Hector; Wilson, Charles J.; Apicella, Alfonso junior

doi:10.7554/elife.15890

Cited by 67 publications

(83 citation statements)

References 66 publications

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“…Moreover, when combined with the finding that the activities in the frontal cortex and dorsal striatum are negatively coupled, it suggests that impulsivity‐associated prefrontostriatal circuits could be a type of inhibitory connection (Fig. F) mediated by long‐range GABAergic projections, as recently discovered, or simply mediated by frontal excitatory inputs to striatal GABAergic interneurons . However, it remains imperative to demonstrate the necessity of the frontostriatal circuit maturation for the top‐down cognitive control of choice impulsivity.…”

Section: Evidence From Human Neuroimaging Studiesmentioning

confidence: 81%

The role of the dorsal striatum in choice impulsivity

Kim

2018

Annals of the New York Academy of Sciences

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It has long been recognized that the dorsal striatum is an essential brain region for control of action selection based on action–outcome contingency learning, particularly when the available actions are bound to rewarding outcomes. In principle, intertemporal choice in the delay‐discounting task—a validated measure of choice impulsivity—involves reward‐associated actions that require the recruitment of the dorsal striatum. Here, we conjecture about ways the dorsal striatum is involved in choice impulsivity. Based on a selective body of studies, we begin with a brief history of research on choice impulsivity and the dorsal striatum, and then provide a comprehensive summary of contemporary studies utilizing human neuroimaging and animal models to search for links between choice impulsivity and the dorsal striatum. In particular, we discuss in‐depth the converging evidence for the associations of choice impulsivity with the reward valuation coded by the caudate, a ventral‐to‐dorsal gradient in the dorsal striatum, the origins of striatal afferents, and developmental maturation of frontostriatal connectivity during adolescence.

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Section: Evidence From Human Neuroimaging Studiesmentioning

confidence: 81%

The role of the dorsal striatum in choice impulsivity

Kim

2018

Annals of the New York Academy of Sciences

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“…However, our approach is not able to exclude other possible sources that might contribute to the observed decorrelation effect, such as inputs from diverse striatal IN classes or from a newly described corticostriatal inhibitory pathway [71]. While cell–specific manipulations can be achieved in striatal SPNs and INs using optogenetic techniques in transgenic mice [67,72], changing SPN firing to precisely test whether inhibition between SPN maintains an intrastriatal low-correlation resting state currently faces two caveats.…”

Section: Discussionmentioning

confidence: 99%

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

Klaus

Plenz

2016

PLoS Biol

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During quiet resting behavior, involuntary movements are suppressed. Such movement control is attributed to cortico-basal ganglia loops, yet population dynamics within these loops during resting and their relation to involuntary movements are not well characterized. Here, we show by recording cortical and striatal ongoing population activity in awake rats during quiet resting that intrastriatal inhibition maintains a low-correlation striatal resting state in the presence of cortical neuronal avalanches. Involuntary movements arise from disturbed striatal resting activity through two different population dynamics. Nonselectively reducing intrastriatal γ-aminobutyric acid (GABA) receptor-A inhibition synchronizes striatal dynamics, leading to involuntary movements at low rate. In contrast, reducing striatal interneuron (IN)-mediated inhibition maintains decorrelation and induces intermittent involuntary movements at high rate. This latter scenario was highly effective in modulating cortical dynamics at a subsecond timescale. To distinguish intrastriatal processing from loop dynamics, cortex-striatum-midbrain cultures, which lack feedback to cortex, were used. Cortical avalanches in vitro were accompanied by low-correlated resting activity in the striatum and nonselective reduction in striatal inhibition synchronized striatal neurons similar to in vivo. Importantly, reduction of inhibition from striatal INs maintained low correlations in the striatum while reorganizing functional connectivities among striatal neurons. Our results demonstrate the importance of two major striatal microcircuits in distinctly regulating striatal and cortical resting state dynamics. These findings suggest that specific functional connectivities of the striatum that are maintained by local inhibition are important in movement control.

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“…If they exist in adult visual cortex, they might have been missed in our study because of their low prevalence. Long-range GABAergic cells in the neocortex are also rare (<0.5% of all interneurons), and 60 to 90% of them are located in L6 and the white matter (30)(31)(32), neither of which were targeted in our study. If they do exist in L1 to L5, they could be easily missed in our study because their main axon may be cut during slicing.…”

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confidence: 99%

Response to Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

Jiang

Shen

Sinz

et al. 2016

Science

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The critique of Barth et al. centers on three points: (i) the completeness of our study is overstated; (ii) the connectivity matrix we describe is biased by technical limitations of our brain-slicing and multipatching methods; and (iii) our cell classification scheme is arbitrary and we have simply renamed previously identified interneuron types. We address these criticisms in our Response. W e will address Barth et al.'s (1) three critiques of our Research Article (2) in turn.(i) The strength of our study is the number of connections tested (>11,000) in one species, cortical area, and age range, using the same experimental protocol. We agree that our study is not exhaustive, because it is focused on synaptic connectivity between interneurons in layers 1, 2/3, and 5, and we point this out in the abstract of the original paper. However, we do believe that no single study to date has presented a more complete wiring diagram of the adult neocortical microcircuit.(ii) Severed connections are a well-known limitation of slice recordings, which we discussed explicitly on p. 3 of the supplementary materials (SM) for (2). However, we do not agree that our study is substantially more susceptible to connection loss than previous patching studies, most of which also used 300-to 350-mm slices [we found fewer than half a dozen multipatching studies using 450-to 500-mm slices (3-5)]. Although cell depth is not reported in many of these studies, the depths at which we recorded (15 to 60 mm) seem typical (6). We patched cells at a wide range of intersomatic distances [see fig. S13A in (2)]; this range reflects the sparsity of labeled interneurons and is not a limitation of octuple patching.Like many previous studies, we used currentclamp mode to measure connectivity, which suffers less distance-dependent voltage attenuation compared with voltage clamp (7). Using potassium internal solution allowed us to characterize spiking properties and test bidirectional connectivity, whereas cesium-based internal solutions would prevent the patched neuron from firing. We discussed potential problems of voltage attenuation [SM for (2), p. 9], such as the underestimation of synaptic event amplitudes and potential nondetection of small synaptic events on the distal dendrites [e.g., connections from Martinotti cells onto layer 5 (L5) pyramidal neurons].To directly address Barth et al.'s concern that the connectivity matrix may be distorted due to slice cutting, we simulated the effect of slicing based on interneuron morphology (8) (Fig. 1A) [see also (6)] for the worst-case scenario where two neurons (pre-and postsynaptic) are both located 15-mm deep from the cutting surface. The resulting correction factor was similar across pairs of cell types (Fig. 1B), more or less scaling the entire connectivity matrix by a factor of 1.36 ± 0.10 (mean ± SD) (Fig. 1, C and D). Given these results and the fact that our connectivity principles mostly rely on the presence or absence of connectivity between specific types regardless of its magnitude, we believe ...

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An inhibitory corticostriatal pathway

Cited by 67 publications

References 66 publications

The role of the dorsal striatum in choice impulsivity

The role of the dorsal striatum in choice impulsivity

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

Response to Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

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