Distinct Thalamic Reticular Cell Types Differentially Modulate Normal and Pathological Cortical Rhythms

Alexandra Clemente-Perez, Stefanie Ritter Makinson, Bryan Higashikubo, Scott Brovarney, Frances S. Cho, Alexander Urry, Stephanie S. Holden, Matthew Wimer, Csaba Dávid, Lief E. Fenno, L. Acsády, Karl Deisseroth, Jeanne T. Paz

Research output: Article

29 Citations (Scopus)

Abstract

Integrative brain functions depend on widely distributed, rhythmically coordinated computations. Through its long-ranging connections with cortex and most senses, the thalamus orchestrates the flow of cognitive and sensory information. Essential in this process, the nucleus reticularis thalami (nRT) gates different information streams through its extensive inhibition onto other thalamic nuclei, however, we lack an understanding of how different inhibitory neuron subpopulations in nRT function as gatekeepers. We dissociated the connectivity, physiology, and circuit functions of neurons within rodent nRT, based on parvalbumin (PV) and somatostatin (SOM) expression, and validated the existence of such populations in human nRT. We found that PV, but not SOM, cells are rhythmogenic, and that PV and SOM neurons are connected to and modulate distinct thalamocortical circuits. Notably, PV, but not SOM, neurons modulate somatosensory behavior and disrupt seizures. These results provide a conceptual framework for how nRT may gate incoming information to modulate brain-wide rhythms.

Original languageEnglish
Pages (from-to)2130-2142
Number of pages13
JournalCell Reports
Volume19
Issue number10
DOIs
Publication statusPublished - jún. 6 2017

Fingerprint

Parvalbumins
Somatostatin
Thalamus
Neurons
Brain
Networks (circuits)
Physiology
Thalamic Nuclei
Somatostatin-Secreting Cells
Rodentia
Seizures
Population

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Clemente-Perez, A., Makinson, S. R., Higashikubo, B., Brovarney, S., Cho, F. S., Urry, A., ... Paz, J. T. (2017). Distinct Thalamic Reticular Cell Types Differentially Modulate Normal and Pathological Cortical Rhythms. Cell Reports, 19(10), 2130-2142. https://doi.org/10.1016/j.celrep.2017.05.044

Distinct Thalamic Reticular Cell Types Differentially Modulate Normal and Pathological Cortical Rhythms. / Clemente-Perez, Alexandra; Makinson, Stefanie Ritter; Higashikubo, Bryan; Brovarney, Scott; Cho, Frances S.; Urry, Alexander; Holden, Stephanie S.; Wimer, Matthew; Dávid, Csaba; Fenno, Lief E.; Acsády, L.; Deisseroth, Karl; Paz, Jeanne T.

In: Cell Reports, Vol. 19, No. 10, 06.06.2017, p. 2130-2142.

Research output: Article

Clemente-Perez, A, Makinson, SR, Higashikubo, B, Brovarney, S, Cho, FS, Urry, A, Holden, SS, Wimer, M, Dávid, C, Fenno, LE, Acsády, L, Deisseroth, K & Paz, JT 2017, 'Distinct Thalamic Reticular Cell Types Differentially Modulate Normal and Pathological Cortical Rhythms', Cell Reports, vol. 19, no. 10, pp. 2130-2142. https://doi.org/10.1016/j.celrep.2017.05.044
Clemente-Perez A, Makinson SR, Higashikubo B, Brovarney S, Cho FS, Urry A et al. Distinct Thalamic Reticular Cell Types Differentially Modulate Normal and Pathological Cortical Rhythms. Cell Reports. 2017 jún. 6;19(10):2130-2142. https://doi.org/10.1016/j.celrep.2017.05.044
Clemente-Perez, Alexandra ; Makinson, Stefanie Ritter ; Higashikubo, Bryan ; Brovarney, Scott ; Cho, Frances S. ; Urry, Alexander ; Holden, Stephanie S. ; Wimer, Matthew ; Dávid, Csaba ; Fenno, Lief E. ; Acsády, L. ; Deisseroth, Karl ; Paz, Jeanne T. / Distinct Thalamic Reticular Cell Types Differentially Modulate Normal and Pathological Cortical Rhythms. In: Cell Reports. 2017 ; Vol. 19, No. 10. pp. 2130-2142.
@article{deffcf361c454fa083b956fc0b39cc5c,
title = "Distinct Thalamic Reticular Cell Types Differentially Modulate Normal and Pathological Cortical Rhythms",
abstract = "Integrative brain functions depend on widely distributed, rhythmically coordinated computations. Through its long-ranging connections with cortex and most senses, the thalamus orchestrates the flow of cognitive and sensory information. Essential in this process, the nucleus reticularis thalami (nRT) gates different information streams through its extensive inhibition onto other thalamic nuclei, however, we lack an understanding of how different inhibitory neuron subpopulations in nRT function as gatekeepers. We dissociated the connectivity, physiology, and circuit functions of neurons within rodent nRT, based on parvalbumin (PV) and somatostatin (SOM) expression, and validated the existence of such populations in human nRT. We found that PV, but not SOM, cells are rhythmogenic, and that PV and SOM neurons are connected to and modulate distinct thalamocortical circuits. Notably, PV, but not SOM, neurons modulate somatosensory behavior and disrupt seizures. These results provide a conceptual framework for how nRT may gate incoming information to modulate brain-wide rhythms.",
keywords = "inhibitory neurons, nRT, optogenetic control of seizures, parvalbumin, reticular thalamic nucleus, seizures, somatosensory, somatostatin, thalamocortical oscillations, TRN",
author = "Alexandra Clemente-Perez and Makinson, {Stefanie Ritter} and Bryan Higashikubo and Scott Brovarney and Cho, {Frances S.} and Alexander Urry and Holden, {Stephanie S.} and Matthew Wimer and Csaba D{\'a}vid and Fenno, {Lief E.} and L. Acs{\'a}dy and Karl Deisseroth and Paz, {Jeanne T.}",
year = "2017",
month = "6",
day = "6",
doi = "10.1016/j.celrep.2017.05.044",
language = "English",
volume = "19",
pages = "2130--2142",
journal = "Cell Reports",
issn = "2211-1247",
publisher = "Cell Press",
number = "10",

}

TY - JOUR

T1 - Distinct Thalamic Reticular Cell Types Differentially Modulate Normal and Pathological Cortical Rhythms

AU - Clemente-Perez, Alexandra

AU - Makinson, Stefanie Ritter

AU - Higashikubo, Bryan

AU - Brovarney, Scott

AU - Cho, Frances S.

AU - Urry, Alexander

AU - Holden, Stephanie S.

AU - Wimer, Matthew

AU - Dávid, Csaba

AU - Fenno, Lief E.

AU - Acsády, L.

AU - Deisseroth, Karl

AU - Paz, Jeanne T.

PY - 2017/6/6

Y1 - 2017/6/6

N2 - Integrative brain functions depend on widely distributed, rhythmically coordinated computations. Through its long-ranging connections with cortex and most senses, the thalamus orchestrates the flow of cognitive and sensory information. Essential in this process, the nucleus reticularis thalami (nRT) gates different information streams through its extensive inhibition onto other thalamic nuclei, however, we lack an understanding of how different inhibitory neuron subpopulations in nRT function as gatekeepers. We dissociated the connectivity, physiology, and circuit functions of neurons within rodent nRT, based on parvalbumin (PV) and somatostatin (SOM) expression, and validated the existence of such populations in human nRT. We found that PV, but not SOM, cells are rhythmogenic, and that PV and SOM neurons are connected to and modulate distinct thalamocortical circuits. Notably, PV, but not SOM, neurons modulate somatosensory behavior and disrupt seizures. These results provide a conceptual framework for how nRT may gate incoming information to modulate brain-wide rhythms.

AB - Integrative brain functions depend on widely distributed, rhythmically coordinated computations. Through its long-ranging connections with cortex and most senses, the thalamus orchestrates the flow of cognitive and sensory information. Essential in this process, the nucleus reticularis thalami (nRT) gates different information streams through its extensive inhibition onto other thalamic nuclei, however, we lack an understanding of how different inhibitory neuron subpopulations in nRT function as gatekeepers. We dissociated the connectivity, physiology, and circuit functions of neurons within rodent nRT, based on parvalbumin (PV) and somatostatin (SOM) expression, and validated the existence of such populations in human nRT. We found that PV, but not SOM, cells are rhythmogenic, and that PV and SOM neurons are connected to and modulate distinct thalamocortical circuits. Notably, PV, but not SOM, neurons modulate somatosensory behavior and disrupt seizures. These results provide a conceptual framework for how nRT may gate incoming information to modulate brain-wide rhythms.

KW - inhibitory neurons

KW - nRT

KW - optogenetic control of seizures

KW - parvalbumin

KW - reticular thalamic nucleus

KW - seizures

KW - somatosensory

KW - somatostatin

KW - thalamocortical oscillations

KW - TRN

UR - http://www.scopus.com/inward/record.url?scp=85020317022&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85020317022&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2017.05.044

DO - 10.1016/j.celrep.2017.05.044

M3 - Article

VL - 19

SP - 2130

EP - 2142

JO - Cell Reports

JF - Cell Reports

SN - 2211-1247

IS - 10

ER -