Thalamic control of layer 1 circuits in prefrontal cortex
Open accessAbstract
Knowledge of thalamocortical (TC) processing comes mainly from studying core thalamic systems that project to middle layers of primary sensory cortices. However, most thalamic relay neurons comprise a matrix of cells that are densest in the “nonspecific” thalamic nuclei and usually target layer 1 (L1) of multiple cortical areas. A longstanding hypothesis is that matrix TC systems are crucial for regulating neocortical excitability during changing behavioral states, yet we know almost nothing about the mechanisms of such regulation. It is also unclear whether synaptic and circuit mechanisms that are well established for core sensory TC systems apply to matrix TC systems. Here we describe studies of thalamic matrix influences on mouse prefrontal cortex using optogenetic and in vitro electrophysiology techniques. Channelrhodopsin-2 was expressed in midline and paralaminar (matrix) thalamic neurons, and their L1-projecting TC axons were activated optically. Contrary to conventional views, we found that matrix TC projections to L1 could transmit relatively strong, fast, high-fidelity synaptic signals. L1 TC projections preferentially drove inhibitory interneurons of L1, especially those of the late-spiking subtype, and often triggered feedforward inhibition in both L1 interneurons and pyramidal cells of L2/L3. Responses during repetitive stimulation were far more sustained for matrix than for core sensory TC pathways. Thus, matrix TC circuits appear to be specialized for robust transmission over relatively extended periods, consistent with the sort of persistent activation observed during working memory and potentially applicable to state-dependent regulation of excitability.
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Elongated neurogliaform cells resemble typical spherical neurogliaform cells in having a dense axonal arbor surrounding a short multipolar dendritic tree, and in having similar intrinsic and functional properties, including frequent late spiking, apparent lack of spike frequency adaptation at threshold, and mediation of GABAB responses in connected postsynaptic targets.
“Sometimes called “elongated neurogliaform cells” (Jiang et al., 2015; Jiang et al., 2013) this subtype of NGFC resembles typical “spherical” NGFCs not only in having a very dense axonal arbor surrounding a short multipolar dendritic tree, but in having seemingly similar intrinsic and functional properties, including a frequent late spiking firing pattern, an apparent lack of spike frequency adapta”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Cruikshank et al., 2012
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- Authors
- Cruikshank, S. J., Ahmed, O. J., Stevens, T. R., Patrick, S. L., Gonzalez, A. N., Elmaleh, M., & Connors, B. W.
- Affiliations
- Brown University (US)
- Corresponding author
- Cruikshank, Scott J.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-12-05
- Volume
- 32
- Issue
- 49
- Pages
- 17813-17823
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3535493
- OpenAlex
- W2109844392
- Cited by
- 212
- References
- 61
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 7 · 2023: 9 · 2022: 10 · 2021: 19 · 2020: 34 · 2019: 19 · 2018: 25 · 2017: 17 · 2016: 13 · 2015: 20 · 2014: 17 · 2013: 6
- FWCI
- 7.05
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0937848)
- U.S. Department of Defense
- National Institutes of Health (5p50mh086400-05, MH086400)
- Defense Advanced Research Projects Agency (DARPA-BAA-09-27)
- Brown Institute for Brain Science
- National Institute of Mental Health (P-50-MH-086400, MH086400)
- National Institute of Neurological Disorders and Stroke (NS-025983, R01NS050434, R01NS025983)
- Division of Emerging Frontiers in Research and Innovation (0937848)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- thalamocortical circuits, prefrontal cortex, layer 1, thalamocortical neurons, synaptic transmission, feedforward inhibition, inhibitory interneurons, pyramidal neurons, working memory, channelrhodopsin-2
- MeSH terms
- Animals, Electric Stimulation, Interneurons, Mice, Inbred ICR, Neural Inhibition, Neural Pathways, Thalamus, Prefrontal Cortex, Pyramidal Cells, Excitatory Postsynaptic Potentials, Mice, Molecular Imaging, Optogenetics
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