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Article ; Online: Untangling the cortico-thalamo-cortical loop: cellular pieces of a knotty circuit puzzle.

Shepherd, Gordon M G / Yamawaki, Naoki

2021 Volume 22, Issue 7, Page(s) 389–406

Abstract: Functions of the neocortex depend on its bidirectional communication with the thalamus, via cortico-thalamo-cortical (CTC) loops. Recent work dissecting the synaptic connectivity in these loops is generating a clearer picture of their cellular ... ...

Abstract	Functions of the neocortex depend on its bidirectional communication with the thalamus, via cortico-thalamo-cortical (CTC) loops. Recent work dissecting the synaptic connectivity in these loops is generating a clearer picture of their cellular organization. Here, we review findings across sensory, motor and cognitive areas, focusing on patterns of cell type-specific synaptic connections between the major types of cortical and thalamic neurons. We outline simple and complex CTC loops, and note features of these loops that appear to be general versus specialized. CTC loops are tightly interlinked with local cortical and corticocortical (CC) circuits, forming extended chains of loops that are probably critical for communication across hierarchically organized cerebral networks. Such CTC-CC loop chains appear to constitute a modular unit of organization, serving as scaffolding for area-specific structural and functional modifications. Inhibitory neurons and circuits are embedded throughout CTC loops, shaping the flow of excitation. We consider recent findings in the context of established CTC and CC circuit models, and highlight current efforts to pinpoint cell type-specific mechanisms in CTC loops involved in consciousness and perception. As pieces of the connectivity puzzle fall increasingly into place, this knowledge can guide further efforts to understand structure-function relationships in CTC loops.
MeSH term(s)	Animals ; Axons/ultrastructure ; Cerebral Cortex/cytology ; Cerebral Cortex/physiology ; Connectome ; Consciousness/physiology ; Dendrites/ultrastructure ; Humans ; Mice ; Neural Pathways/physiology ; Neurons/classification ; Neurons/physiology ; Neurons/ultrastructure ; Perception/physiology ; Species Specificity ; Synapses/physiology ; Thalamus/cytology ; Thalamus/physiology
Language	English
Publishing date	2021-05-06
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2034150-7
ISSN	1471-0048 ; 1471-0048 ; 1471-003X
ISSN (online)	1471-0048
ISSN	1471-0048 ; 1471-003X
DOI	10.1038/s41583-021-00459-3
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Book ; Online: Motor Cortex Microcircuits (Frontiers in Brain Microcircuits Series)

Brecht, Michael / Hatsopoulos, Nicholas / Kaneko, Takehsi / Shepherd, Gordon M. G

2015

Abstract: How does the motor cortex enable mammals to generate accurate, complex, and purposeful movements? A cubic millimeter of motor cortex contains roughly ~10^5 cells, an amazing ~4 Km of axons and ~0.4 Km of dendrites, somehow wired together with ~10^9 ... ...

Abstract	How does the motor cortex enable mammals to generate accurate, complex, and purposeful movements? A cubic millimeter of motor cortex contains roughly ~10^5 cells, an amazing ~4 Km of axons and ~0.4 Km of dendrites, somehow wired together with ~10^9 synapses. Corticospinal neurons (a.k.a. Betz cells, upper motor neurons) are a key cell type, monosynaptically conveying the output of the cortical circuit to the spinal cord circuits and lower motor neurons. But corticospinal neurons are greatly outnumbered by all the other kinds of neurons in motor cortex, which presumably also contribute crucially to the computational operations carried out for planning, executing, and guiding actions. Determining the wiring patterns, the dynamics of signaling, and how these relate to movement at the level of specific excitatory and inhibitory cell types is critically important for a mechanistic understanding of the input-output organization of motor cortex. While there is a predictive microcircuit hypothesis that relates motor learning to the operation of the cerebellar cortex, we lack such a microcircuit understanding in motor cortex and we consider microcircuits as a central research topic in the field. This Research Topic covers any issues relating to the microcircuit-level analysis of motor cortex. Contributions are welcomed from neuroscientists at all levels of investigation, from in vivo physiology and imaging in humans and monkeys, to rodent models, in vitro anatomy, electrophysiology, electroanatomy, cellular imaging, molecular biology, disease models, computational modeling, and more
Keywords	Science (General) ; Neurosciences. Biological psychiatry. Neuropsychiatry
Size	1 electronic resource (133 p.)
Publisher	Frontiers Media SA
Document type	Book ; Online
Note	English ; Open Access
HBZ-ID	HT020090131
ISBN	9782889193899 ; 2889193896
Database	ZB MED Catalogue: Medicine, Health, Nutrition, Environment, Agriculture

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Article ; Online: Manipulation-specific cortical activity as mice handle food.

Barrett, John M / Martin, Megan E / Shepherd, Gordon M G

Current biology : CB

2022 Volume 32, Issue 22, Page(s) 4842–4853.e6

Abstract: Food handling offers unique yet largely unexplored opportunities to investigate how cortical activity relates to forelimb movements in a natural, ethologically essential, and kinematically rich form of manual dexterity. To determine these relationships, ... ...

Abstract	Food handling offers unique yet largely unexplored opportunities to investigate how cortical activity relates to forelimb movements in a natural, ethologically essential, and kinematically rich form of manual dexterity. To determine these relationships, we recorded high-speed (1,000 fps) video and multi-channel electrophysiological cortical spiking activity while mice handled food. The high temporal resolution of the video allowed us to decompose active manipulation ("oromanual") events into characteristic submovements, enabling event-aligned analysis of cortical activity. Activity in forelimb M1 was strongly modulated during food handling, generally higher during oromanual events and lower during holding intervals. Optogenetic silencing and stimulation of forelimb M1 neurons partially affected food-handling movements, exerting suppressive and activating effects, respectively. We also extended the analysis to forelimb S1 and lateral M1, finding broadly similar oromanual-related activity across all three areas. However, each area's activity displayed a distinct timing and phasic/tonic temporal profile, which was further analyzed by non-negative matrix factorization and demonstrated to be attributable to area-specific composition of activity classes. Current or future forelimb position could be accurately predicted from activity in all three regions, indicating that the cortical activity in these areas contains high information content about forelimb movements during food handling. These results thus establish that cortical activity during food handling is manipulation specific, distributed, and broadly similar across multiple sensorimotor areas while also exhibiting area- and submovement-specific relationships with the fast kinematic hallmarks of this natural form of complex free-object-handling manual dexterity.
MeSH term(s)	Animals ; Mice ; Forelimb/physiology ; Movement/physiology ; Optogenetics ; Food ; Biomechanical Phenomena
Language	English
Publishing date	2022-10-14
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2022.09.045
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Article ; Online: Axonal Barcode Analysis of Pyramidal Tract Projections from Mouse Forelimb M1 and M2.

Hausmann, Frances S / Barrett, John M / Martin, Megan E / Zhan, Huiqing / Shepherd, Gordon M G

The Journal of neuroscience : the official journal of the Society for Neuroscience

2022 Volume 42, Issue 41, Page(s) 7733–7743

Abstract: Forelimb-related areas of the motor cortex communicate directly to downstream areas in the brainstem and spinal cord via axons that project to and through the pyramidal tract (PT). To better understand the diversity of the brainstem branching patterns of ...

Abstract	Forelimb-related areas of the motor cortex communicate directly to downstream areas in the brainstem and spinal cord via axons that project to and through the pyramidal tract (PT). To better understand the diversity of the brainstem branching patterns of these pyramidal tract projections, we used MAPseq, a molecular barcode technique for population-scale sampling with single-axon resolution. In experiments using mice of both sexes, we first confirmed prior results demonstrating the basic efficacy of axonal barcode identification of primary motor cortex (M1) PT-type axons, including corticobulbar (CBULB) and corticospinal (CSPI) subclasses. We then used multiplexed MAPseq to analyze projections from M1 and M2 (caudal and rostral forelimb areas). The four basic axon subclasses comprising these projections (M1-CSPI, M1-CBULB, M2-CSPI, M2-CBULB) showed a complex mix of differences and similarities in their brainstem projection profiles. This included relatively abundant branching by all classes in the dorsal midbrain, by M2 subclasses in the pons, and by CSPI subclasses in the dorsal medulla. Cluster analysis showed graded distributions of the basic subclasses within the PT class. Clusters were of diversely mixed subclass composition and showed distinct rostrocaudal and/or dorsomedial projection biases. Exemplifying these patterns was a subcluster likely enriched in corticocuneate branches. Overall, the results indicate high yet systematic PT axon diversity at the level of brainstem branching patterns; projections of M1 and M2 appear qualitatively similar, yet with quantitative differences in subclasses and clusters.
MeSH term(s)	Female ; Male ; Mice ; Animals ; Pyramidal Tracts/physiology ; Axons/physiology ; Forelimb ; Motor Cortex/physiology ; Upper Extremity
Language	English
Publishing date	2022-09-07
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.1062-22.2022
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Article ; Online: Manual dexterity of mice during food-handling involves the thumb and a set of fast basic movements.

Barrett, John M / Raineri Tapies, Martinna G / Shepherd, Gordon M G

PloS one

2020 Volume 15, Issue 1, Page(s) e0226774

Abstract: The small first digit (D1) of the mouse's hand resembles a volar pad, but its thumb-like anatomy suggests ethological importance for manipulating small objects. To explore this possibility, we recorded high-speed close-up video of mice eating seeds and ... ...

Abstract	The small first digit (D1) of the mouse's hand resembles a volar pad, but its thumb-like anatomy suggests ethological importance for manipulating small objects. To explore this possibility, we recorded high-speed close-up video of mice eating seeds and other food items. Analyses of ethograms and automated tracking with DeepLabCut revealed multiple distinct microstructural features of food-handling. First, we found that mice indeed made extensive use of D1 for dexterous manipulations. In particular, mice used D1 to hold food with either of two grip types: a pincer-type grasp, or a "thumb-hold" grip, pressing with D1 from the side. Thumb-holding was preferentially used for handling smaller items, with the smallest items held between the two D1s alone. Second, we observed that mice cycled rapidly between two postural modes while feeding, with the hands positioned either at the mouth (oromanual phase) or resting below (holding phase). Third, we identified two highly stereotyped D1-related movements during feeding, including an extraordinarily fast (~20 ms) "regrip" maneuver, and a fast (~100 ms) "sniff" maneuver. Lastly, in addition to these characteristic simpler movements and postures, we also observed highly complex movements, including rapid D1-assisted rotations of food items and dexterous simultaneous double-gripping of two food fragments. Manipulation behaviors were generally conserved for different food types, and for head-fixed mice. Wild squirrels displayed a similar repertoire of D1-related movements. Our results define, for the mouse, a set of kinematic building-blocks of manual dexterity, and reveal an outsized role for D1 in these actions.
MeSH term(s)	Animals ; Food ; Forelimb/physiology ; Functional Laterality ; Mice ; Mice, Inbred C57BL ; Movement
Language	English
Publishing date	2020-01-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2267670-3
ISSN	1932-6203 ; 1932-6203
ISSN (online)	1932-6203
ISSN	1932-6203
DOI	10.1371/journal.pone.0226774
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Article ; Online: Diversity and complexity in the pyramidal tract projectome.

Shepherd, Gordon M G

Nature reviews. Neuroscience

2013 Volume 15, Issue 1, Page(s) 63

MeSH term(s)	Animals ; Cerebral Cortex/physiology ; Corpus Striatum/physiology ; Developmental Disabilities/pathology ; Humans ; Mental Disorders/pathology ; Movement Disorders/pathology ; Neural Pathways/physiology
Language	English
Publishing date	2013-12-04
Publishing country	England
Document type	Letter ; Comment
ZDB-ID	2034150-7
ISSN	1471-0048 ; 1471-0048 ; 1471-003X
ISSN (online)	1471-0048
ISSN	1471-0048 ; 1471-003X
DOI	10.1038/nrn3469-c2
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Zs.A 5473: 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: Corticostriatal connectivity and its role in disease.

Shepherd, Gordon M G

Nature reviews. Neuroscience

2013 Volume 14, Issue 4, Page(s) 278–291

Abstract: Corticostriatal projections are essential components of forebrain circuits and are widely involved in motivated behaviour. These axonal projections are formed by two distinct classes of cortical neurons, intratelencephalic (IT) and pyramidal tract (PT) ... ...

Abstract	Corticostriatal projections are essential components of forebrain circuits and are widely involved in motivated behaviour. These axonal projections are formed by two distinct classes of cortical neurons, intratelencephalic (IT) and pyramidal tract (PT) neurons. Convergent evidence points to IT versus PT differentiation of the corticostriatal system at all levels of functional organization, from cellular signalling mechanisms to circuit topology. There is also growing evidence for IT/PT imbalance as an aetiological factor in neurodevelopmental, neuropsychiatric and movement disorders - autism, amyotrophic lateral sclerosis, obsessive-compulsive disorder, schizophrenia, Huntington's and Parkinson's diseases and major depression are highlighted here.
MeSH term(s)	Animals ; Cerebral Cortex/cytology ; Cerebral Cortex/physiology ; Corpus Striatum/cytology ; Corpus Striatum/physiology ; Developmental Disabilities/pathology ; Humans ; Mental Disorders/pathology ; Movement Disorders/pathology ; Neural Pathways/physiology ; Neurons/physiology
Language	English
Publishing date	2013-03-20
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2034150-7
ISSN	1471-0048 ; 1471-0048 ; 1471-003X
ISSN (online)	1471-0048
ISSN	1471-0048 ; 1471-003X
DOI	10.1038/nrn3469
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Article ; Online: Multiscale model of primary motor cortex circuits predicts in vivo cell-type-specific, behavioral state-dependent dynamics.

Dura-Bernal, Salvador / Neymotin, Samuel A / Suter, Benjamin A / Dacre, Joshua / Moreira, Joao V S / Urdapilleta, Eugenio / Schiemann, Julia / Duguid, Ian / Shepherd, Gordon M G / Lytton, William W

Cell reports

2023 Volume 42, Issue 6, Page(s) 112574

Abstract: Understanding cortical function requires studying multiple scales: molecular, cellular, circuit, and behavioral. We develop a multiscale, biophysically detailed model of mouse primary motor cortex (M1) with over 10,000 neurons and 30 million synapses. ... ...

Abstract	Understanding cortical function requires studying multiple scales: molecular, cellular, circuit, and behavioral. We develop a multiscale, biophysically detailed model of mouse primary motor cortex (M1) with over 10,000 neurons and 30 million synapses. Neuron types, densities, spatial distributions, morphologies, biophysics, connectivity, and dendritic synapse locations are constrained by experimental data. The model includes long-range inputs from seven thalamic and cortical regions and noradrenergic inputs. Connectivity depends on cell class and cortical depth at sublaminar resolution. The model accurately predicts in vivo layer- and cell-type-specific responses (firing rates and LFP) associated with behavioral states (quiet wakefulness and movement) and experimental manipulations (noradrenaline receptor blockade and thalamus inactivation). We generate mechanistic hypotheses underlying the observed activity and analyzed low-dimensional population latent dynamics. This quantitative theoretical framework can be used to integrate and interpret M1 experimental data and sheds light on the cell-type-specific multiscale dynamics associated with several experimental conditions and behaviors.
MeSH term(s)	Mice ; Animals ; Motor Cortex/physiology ; Neurons/physiology ; Thalamus/physiology ; Synapses/physiology ; Biophysics
Language	English
Publishing date	2023-06-09
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2023.112574
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Article ; Online: Cortico-Thalamo-Cortical Circuits of Mouse Forelimb S1 Are Organized Primarily as Recurrent Loops.

Guo, KuangHua / Yamawaki, Naoki / Barrett, John M / Tapies, Martinna / Shepherd, Gordon M G

The Journal of neuroscience : the official journal of the Society for Neuroscience

2020 Volume 40, Issue 14, Page(s) 2849–2858

Abstract: Cortical projections to the thalamus arise from corticothalamic (CT) neurons in layer 6 and pyramidal tract-type (PT) neurons in layer 5B. We dissected the excitatory synaptic connections in the somatosensory thalamus formed by CT and PT neurons of the ... ...

Abstract	Cortical projections to the thalamus arise from corticothalamic (CT) neurons in layer 6 and pyramidal tract-type (PT) neurons in layer 5B. We dissected the excitatory synaptic connections in the somatosensory thalamus formed by CT and PT neurons of the primary somatosensory (S1) cortex, focusing on mouse forelimb S1. Mice of both sexes were studied. The CT neurons in S1 synaptically excited S1-projecting thalamocortical (TC) neurons in subregions of both the ventral posterior lateral and posterior (PO) nuclei, forming a pair of recurrent cortico-thalamo-cortical (C-T-C) loops. The PT neurons in S1 also formed a recurrent loop with S1-projecting TC neurons in the same subregion of the PO. The PT neurons in the adjacent primary motor (M1) cortex formed a separate recurrent loop with M1-projecting TC neurons in a nearby subregion of the PO. Collectively, our results reveal that C-T-C circuits of mouse forelimb S1 are primarily organized as multiple cortical cell-type-specific and thalamic subnucleus-specific recurrent loops, with both CT and PT neurons providing the strongest excitatory input to TC neurons that project back to S1. The findings, together with those of related studies of C-T-C circuits, thus suggest that recurrently projecting thalamocortical neurons are the principal targets of cortical excitatory input to the mouse somatosensory and motor thalamus.
MeSH term(s)	Animals ; Female ; Forelimb/innervation ; Male ; Mice ; Mice, Inbred C57BL ; Neural Pathways/cytology ; Somatosensory Cortex/cytology ; Thalamus/cytology
Language	English
Publishing date	2020-02-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.2277-19.2020
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Article ; Online: Synaptic circuit organization of motor corticothalamic neurons.

Yamawaki, Naoki / Shepherd, Gordon M G

The Journal of neuroscience : the official journal of the Society for Neuroscience

2015 Volume 35, Issue 5, Page(s) 2293–2307

Abstract: Corticothalamic (CT) neurons in layer 6 constitute a large but enigmatic class of cortical projection neurons. How they are integrated into intracortical and thalamo-cortico-thalamic circuits is incompletely understood, especially outside of sensory ... ...

Abstract	Corticothalamic (CT) neurons in layer 6 constitute a large but enigmatic class of cortical projection neurons. How they are integrated into intracortical and thalamo-cortico-thalamic circuits is incompletely understood, especially outside of sensory cortex. Here, we investigated CT circuits in mouse forelimb motor cortex (M1) using multiple circuit-analysis methods. Stimulating and recording from CT, intratelencephalic (IT), and pyramidal tract (PT) projection neurons, we found strong CT↔ CT and CT↔ IT connections; however, CT→IT connections were limited to IT neurons in layer 6, not 5B. There was strikingly little CT↔ PT excitatory connectivity. Disynaptic inhibition systematically accompanied excitation in these pathways, scaling with the amplitude of excitation according to both presynaptic (class-specific) and postsynaptic (cell-by-cell) factors. In particular, CT neurons evoked proportionally more inhibition relative to excitation (I/E ratio) than IT neurons. Furthermore, the amplitude of inhibition was tuned to match the amount of excitation at the level of individual neurons; in the extreme, neurons receiving no excitation received no inhibition either. Extending these studies to dissect the connectivity between cortex and thalamus, we found that M1-CT neurons and thalamocortical neurons in the ventrolateral (VL) nucleus were remarkably unconnected in either direction. Instead, VL axons in the cortex excited both IT and PT neurons, and CT axons in the thalamus excited other thalamic neurons, including those in the posterior nucleus, which additionally received PT excitation. These findings, which contrast in several ways with previous observations in sensory areas, illuminate the basic circuit organization of CT neurons within M1 and between M1 and thalamus.
MeSH term(s)	Action Potentials ; Animals ; Excitatory Postsynaptic Potentials ; Female ; Inhibitory Postsynaptic Potentials ; Male ; Mice ; Mice, Inbred C57BL ; Motor Cortex/cytology ; Motor Cortex/physiology ; Nerve Net/cytology ; Nerve Net/physiology ; Neurons/physiology ; Pyramidal Tracts/physiology ; Synapses/physiology ; Telencephalon/cytology ; Telencephalon/physiology ; Thalamus/cytology ; Thalamus/physiology
Language	English
Publishing date	2015-02-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.4023-14.2015
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